Académique Documents
Professionnel Documents
Culture Documents
AGRICULTURE AND
FOOD SYSTEMS
VOLUME 1
ENCYCLOPEDIA OF
AGRICULTURE AND
FOOD SYSTEMS
EDITOR-IN-CHIEF
Academic Press
Academic Press is an imprint of Elsevier
32 Jamestown Road, London NW1 7BY, UK
225 Wyman Street, Waltham, MA 02451, USA
525 B Street, Suite 1800, San Diego, CA 92101-4495, USA
Copyright r 2014 Elsevier Inc. unless otherwise stated. All rights reserved
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic,
mechanical, photocopying, recording or otherwise without the prior written permission of the publisher
Permissions may be sought directly from Elseviers Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865
843830; fax (+44) (0) 1865 853333; email: permissions@elsevier.com. Alternatively you can submit your request online by visiting the
Elsevier web site at http://elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material
Notice
No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability,
negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein,
Because of rapid advances in the medical sciences, in particular, independent verication of diagnoses and drug dosages should be made
British Library Cataloguing in Publication Data
A catalogue record for this book is available from the British Library
Library of Congress Cataloging-in-Publication Data
A catalog record for this book is available from the Library of Congress
ISBN (print): 978-0-444-52512-3
EDITORIAL BOARD
Editor-in-Chief
Neal K Van Alfen
University of California, Davis, CA, USA
Associate Editors
Brent Clothier
Plant & Food Research
Palmerston North
New Zealand
John P Nichols
Texas A& M University
College Station, TX
USA
Daryl Lund
University of Wisconsin
Madison, WI
USA
Harris A Lewin
University of California
Davis, CA
USA
Mary Delany
University of California
Davis, CA
USA
R James Cook
Washington State University
Pullman, WA
USA
Roger RB Leakey
James Cook University
Queensland
Australia
Jeremy J Burdon
Commonwealth Scientic and Industrial
Research Organisation
Black Mountain, Canberra
Australia
Ronald L Phillips
University of Minnesota
St Paul, MN
USA
CONTRIBUTORS TO VOLUME 1
FK Akinnifesi
Food and Agriculture Organization of the United
Nations (FAO), Rome, Italy
K Anderson
University of Adelaide, Adelaide, SA, Australia, and
Australian National University, Canberra, ACT,
Australia
F Diaz-San Segundo
US Department of Agriculture, Greenport, NY, USA
TJ Dijkman
Technical University of Denmark, Kongens Lyngby,
Denmark
PN Ellinger
University of Illinois, Urbana, IL, USA
BL Backus
Texas Tech University, Lubbock, TX, USA
G Eyles
Napier, New Zealand
J Bayala
World Agroforestry Centre, Bamako, Mali
S Flack
University of Edinburgh, Edinburgh, UK
T Beedy
Plainview, TX, USA
CB Flora
Kansas State University, Ames, IA, USA
D Biswas
University of Maryland, College Park, MD, USA
S Franzel
World Agroforestry Centre, Nairobi, Kenya
CR Black
University of Nottingham, Sutton Bonington, UK
S Green
The New Zealand Institute for Plant & Food Research
Limited, Palmerston North, New Zealand
MD Boehlje
Purdue University, West Lafayette, IN, USA
ST Buccola
Oregon State University, Corvallis, OR, USA
TJ Centner
The University of Georgia, Athens, GA, USA
P Chirwa
University of Pretoria, Pretoria, South Africa
B Clothier
The New Zealand Institute for Plant & Food Research
Limited, Palmerston North, New Zealand
CH Corassin
University of So Paulo. Av. Duque de Caxias Norte,
Pirassununga, SP, Brazil
B Corra
University of So Paulo. Av. Prof. Lineu Prestes, So
Paulo, SP, Brazil
MJ Grubman
US Department of Agriculture, Greenport, NY, USA
K Guay
Tarleton State University, Stephenville, TX, USA
MA Gunderson
Purdue University, West Lafayette, IN, USA
W Hu
China Agricultural University, Beijing, China
WE Huffman
Iowa State University, Ames, IA, USA
NA Jackson
Centre for Ecology & Hydrology, Wallingford, UK
O Jiri
University of Zimbabwe, Harare, Zimbabwe
E Kiptot
World Agroforestry Centre, Nairobi, Kenya
F Corsin
IDH, The Sustainable Trade Initiative, Hanoi, Vietnam
LA Knapp
University of Illinois, Urbana, IL, USA
L Daoping
State Forestry Administration, Beijing, Peoples Republic
of China
W Kositratana
Kasetsart University, Kamphaeng Saen, Nakhon
Pathom, Thailand
KA Darfour-Oduro
University of Illinois, Urbana, IL, USA
Y-J Kung
National Chung Hsing University, Taichung, Taiwan
vii
viii
Contributors to Volume 1
RRB Leakey
James Cook University, Queensland, Australia
P Nyamugafata
University of Zimbabwe, Harare, Zimbabwe
RH Liu
Cornell University, Ithaca, NY, USA
CAF de Oliveira
University of So Paulo. Av. Duque de Caxias Norte,
Pirassununga, SP, Brazil
B Lukuyu
International Livestock Research Institute, Nairobi,
Kenya
AL Olmstead
University of California, Davis, CA, USA
PL Mafongoya
University of Zimbabwe, Harare, Zimbabwe
C Ong
University of Nottingham, Nottingham, UK
RG Maggi
North Carolina State University, Raleigh, NC, USA
IP Oswald
INRA, ToxAlim, UMR1331 and Universit de Toulouse,
Toulouse, France
W Makumba
Chitedze Agricultural Research Station, Lilongwe,
Malawi
M Peng
University of Maryland, College Park, MD, USA
LG Malta
Cornell University, Ithaca, NY, USA
JB Penson Jr.
Texas A& M University, College Station, TX, USA
P Martin
University of California, Davis, CA, USA
CB Peterson
University of California, Davis, CA, USA
K Maxwell
University of Edinburgh, Edinburgh, UK
E Phiri
University of Zambia, Lusaka, Zambia
JJ McGlone
Texas Tech University, Lubbock, TX, USA
PJ Pinedo
Texas A& M University System, Amarillo, TX, USA
I McIvor
Plant & Food Research, Palmerston North, New
Zealand
Z Pu
Chinese Academy of Forestry, Beijing, Peoples Republic
of China
GN Medina
US Department of Agriculture, Greenport, NY, USA
JAJ Raja
National Chung Hsing University, Taichung, Taiwan
A Mistry
University of Edinburgh, Edinburgh, UK
PK Ramachandran Nair
University of Florida, Gainesville, FL, USA
FM Mitloehner
University of California, Davis, CA, USA
G Rausser
University of California, Berkeley, CA, USA
K Mller
The New Zealand Institute for Plant & Food Research
Limited, Hamilton, New Zealand
RM Rees
Scotlands Rural College (SRUC), Edinburgh, UK
C Muthuri
World Agroforestry Centre, Nairobi, Kenya
MF Neves
University of So Paulo, Ribeirao Preto, SP, Brazil
J Njoloma
Chitedze Agricultural Research Station, Lilongwe,
Malawi
PW Rhode
University of Michigan, Ann Arbor, MI, USA
FM Rodrigues
Federal University of Pelotas, Pelotas, Brazil
LA Rund
University of Illinois, Urbana, IL, USA
S Salaheen
University of Maryland, College Park, MD, USA
S Noll
Michigan State University, East Lansing, MI, USA
T de los Santos
US Department of Agriculture, Greenport, NY, USA
G Nyamadzawo
University of Zimbabwe, Harare, Zimbabwe
KM Schachtschneider
University of Illinois, Urbana, IL, USA
Contributors to Volume 1
LB Schook
University of Illinois, Urbana, IL, USA
G Schroth
Santarm, Par, Brazil
EG Schusterman
University of California, Davis, CA, USA
GW Sileshi
Chitedze Agricultural Research Station, Lilongwe,
Malawi
M do Socorro Souza da Mota
Santarm, Par, Brazil
ST Sonka
University of Illinois, Champaign, IL, USA
J Swinnen
University of Leuven (KUL), Leuven, Belgium, and
Stanford University, Stanford, CA, USA
PB Thompson
Michigan State University, East Lansing, MI, USA
ix
A Tiktak
PBL Netherlands Environmental Assessment Agency, AH
Bilthoven, The Netherlands
SJ Werth
University of California, Davis, CA, USA
J Wilson
Centre for Ecology & Hydrology, Penicuik, UK
M Wuta
University of Zimbabwe, Harare, Zimbabwe
K Yamamoto
University of Stirling, Stirling, UK
S-D Yeh
National Chung Hsing University, Taichung, Taiwan
H Youjun
Chinese Academy of Forestry, Beijing, Peoples Republic
of China
Cross-References
Index
Contributors
xi
SUBJECT CLASSIFICATION
Agriculture and People
Agribusiness Organization and Management
Agricultural Cooperatives
Agricultural Ethics and Social Justice
Agricultural Finance
Agricultural Labor: Demand for Labor
Agricultural Labor: Gender Issues
Agricultural Labor: Labor Market Operation
Agricultural Labor: Supply of Labor
Agricultural Law
Agricultural Policy: A Global View
Analyses of Total Phenolics, Total Flavonoids, and
Total Antioxidant Activities in Foods and Dietary
Supplements
Changing Structure and Organization of US
Agriculture
Climate Change, Society, and Agriculture: An
Economic and Policy Perspective
Computer Modeling: Policy Analysis and Simulation
Consumer-Oriented New Product Development
Crop Insurance
Determining Functional Properties and Sources of
Recently Identied Bioactive Food Components:
Oligosaccharides, Glycolipids, Glycoproteins, and
Peptides
Farm Management
Food Chain: Farm to Market
Food Labeling
Food Law
Food Marketing
Food Security, Market Processes, and the Role of
Government Policy
Food Security: Development Strategies
Food Security: Food Defense and Biosecurity
From Foraging to Agriculture
Global Food Supply Chains
Government Agricultural Policy, United States
Human Nutrition: Malnutrition and Diet
Industrialized Farming and Its Relationship to
Community Well-Being
Intellectual Property in Agriculture
International and Regional Institutions and
Instruments for Agricultural Policy, Research, and
Development
International Trade
Investments in and the Economic Returns to
Agricultural and Food R&D Worldwide
Markets and Prices
Mathematical Models to Elaborate Plans for Adaptation
of Rural Communities to Climate Change
xiii
xiv
Subject Classication
Agriculture Products
Advances in Pesticide Risk Reduction
Agricultural Mechanization
Agroforestry: Complex Multistrata Agriculture
Agroforestry: Fertilizer Trees
Agroforestry: Fodder Trees
Agroforestry: Participatory Domestication of Trees
Agroforestry: Practices and Systems
Asian Aquaculture
Beef Cattle
Climate Change: Animal Systems
Climate Change: Cropping System Changes and
Adaptations
Climate Change: Horticulture
Climate Change: New Breeding Pressures and Goals
Critical Tracking Events Approach to Food
Traceability
Dairy Animals
Edaphic Soil Science, Introduction to
Fermentation: Food Products
Fermented Beverages
Food Engineering
Food Microbiology
Food Packaging
Food Safety: Emerging Pathogens
Food Safety: Food Analysis Technologies/Techniques
Food Safety: Shelf Life Extension Technologies
Food Security: Postharvest Losses
Food Security: Yield Gap
Food Toxicology
Forage Crops
Global Agriculture: Industrial Feedstocks for Energy
and Materials
Green Revolution: Past, Present, and Future
Medicinal Crops
Organic Agricultural Production: Plants
Organic Livestock Production
Precision Agriculture: Irrigation
Animal Health
Animal Health: Ectoparasites
Animal Health: Foot-and-Mouth Disease
Animal Health: Global Antibiotic Issues
Animal Health: Mycotoxins
Animal Health: Tuberculosis
Animal Welfare: Stress, Global Issues, and
Perspectives
Biosecurity and Equine Infectious Diseases
Detection and Causes of Bovine Mastitis with
Emphasis on Staphylococcus aureus
Emerging Zoonoses in Domesticated Livestock of
Southeast Asia
Invasive Aquatic Animals
Marek's Disease and Differential Diagnosis with
Other Tumor Viral Diseases of Poultry
Poultry and Avian Diseases
Quarantine and Biosecurity
Swine Diseases and Disorders
Vaccines and Vaccination Practices: Key to
Sustainable Animal Production
Zoonotic Helminths of Livestock
Plant Health
Climate Change and Plant Disease
Emerging Plant Diseases
Integrated Pest Management in Tree Fruit Crops
Invasive Species: Plants
Mineral Nutrition and Suppression of Plant Disease
Pathogen-Tested Planting Material
Plant Abiotic Stress: Salt
Plant Abiotic Stress: Temperature Extremes
Plant Abiotic Stress: Water
Plant Biotic Stress: Weeds
Plant Disease and Resistance
Plant Health Management: Biological Control of
Insect Pests
Subject Classication
xv
Biotechnology: Pharming
Biotechnology: Plant Protection
Biotechnology: Regulatory Issues
Breeding: Animals
Breeding: Plants, Modern
Cloning Animals by Somatic Cell Nuclear
Transplantation
Cloning: Plants Micropropagation/Tissue Culture
Domestication of Animals
Domestication of Plants
Genebanks: Past, Present, and Optimistic Future
Genomics of Food Animals
Genomics: Plant Genetic Improvement
Heterosis in Plants
Plant Cloning: Macropropagation
Plant Virus Control by Post-Transcriptional Gene
Silencing
Regulatory Challenges to Commercializing the
Products of Ag Biotech
Stem Cells
Transgenic Methodologies Plants
PREFACE
Food is absolutely necessary for human existence, yet for most
in wealthy nations it is largely taken for granted because of its
abundance. Sufcient food is a concern, however, for about 1
billion of the earth's inhabitants today who often go to bed
hungry. Food security in a broad sense is becoming a worry of
the future for those who understand the limitations of our
earth's ecosystems. Malthusian prophecies have so far been
wrong, but there is growing concern that we are rapidly
reaching the point where feeding the world's growing and
richer population will be at the cost to our environment that is
unacceptable. In the next few decades we face the challenge of
growing more food, with less water, with less fertilizer on less
land because of the growth of urban areas on prime agriculture land. We also face the largely unknown consequences
that global warming will have on agricultural production.
During the last century agricultural scientists were able to bring
cutting-edge science into traditional agricultural practices and
increase food production sufciently to prevent global food
shortages. The hope that new scientic discoveries will provide
the means to keep ahead of world food demand is complicated by a growing public discomfort with biotechnology
being applied to food production.
The concept of services being provided by the ecosystems of
the earth is a fairly recent attempt to understand and place
value on functions of natural lands that have historically been
assumed to have few limits. In the past, if more food was
needed, new lands were converted from forests or steppe lands
into farm land and new water systems developed to provide
the water needed for agriculture. When human populations
were low our activities were largely buffered by the abundance
of forest and steppe, but too late, we are beginning to
understand that these provisioning services of our ecosystems
are being overused and are no longer buffered by the abundance of wild lands and waters. We are rapidly losing our
planet's biodiversity, irreplaceable ground water is being unsustainably consumed, and major river systems are being
overused and polluted. Our oceans, the last place on the planet that still support our hunter and gathering traditions may
not be able to sustain these activities into the future. And, food
production and processing activities contribute to the greenhouse gas emissions that are rapidly warming our planet.
Agriculture is the single greatest user of the earth's land and
water resources. In the concept of ecosystem services, provisioning or providing food for all organisms is one of the
services provided by ecosystems. Human population growth
has and will continue to overtax the ecosystems we inhabit.
The ultimate outcome of this major diversion of nature's resources into provisioning the human species is unknown, but
it is critically important for us to understand what we must do
to sustain our planet.
The breakthrough discovery about 10 000 years ago that
plants and animals could be bred to provide a more abundant
and secure food source was the foundation upon which
all other human activities were able to ourish. Activities other
than nding food now became possible and our diverse
The issue raised by Dr. Borlaug is probably the most important challenge we face. Human behavior and the food
choices of consumers will determine the outcome of the race
between food supply and population. Population control has
been advocated for decades, and in some cases has become
part of national policy, but the world's population continues
to grow. Science breakthroughs cannot solve our food security
and environmental quality challenges if consumers reject food
that is not traditionally produced. Likewise, if meat products
and other inefciently produced food continue to be in high
demand by consumers, there will be increased pressure on our
food production systems. As supplies become short, prices rise.
While this may be good for farmers, high food prices and food
shortages will probably undermine our efforts to preserve the
xvii
xviii
Preface
fortunate to be joined by a very distinguished group of colleagues who, I hope, are still friends. They spent much more
time and effort in bringing this project to completion than any
of us anticipated. I want to thank our authors who while
overly committed and overworked, fullled their commitments to contribute to this work. I have been impressed with
the quality of their contributions. The editorial staff of Elsevier
have had the professionalism and patience to work with scientists who do not work under the same time and budget
constraints that the staff work. I want to particularly thank
Kristi Gomez, Donna de Weerd-Wilson, and Simon Holt who,
each in succession, oversaw this effort, and I especially thank
the project managers, who worked directly with me, and the
associate editors, Kate Miklaszewka-Gorczyca, Will BowdenGreen, and Sam Mahfoudh.
Neal K Van Alfen
Professor, Department of Plant Pathology Dean Emeritus,
College of Agricultural and Environmental Sciences,
University of California Davis, CA, USA
v
vii
xi
Subject Classification
xiii
Preface
xvii
VOLUME 1
A
Advances in Animal Biotechnology
LB Schook, LA Rund, W Hu, KA Darfour-Oduro, LA Knapp, FM Rodrigues, and KM Schachtschneider
17
35
51
Agricultural Cooperatives
ST Buccola
71
81
Agricultural Finance
PN Ellinger and JB Penson Jr.
92
105
123
131
143
Agricultural Law
TJ Centner
157
Agricultural Mechanization
AL Olmstead and PW Rhode
168
179
xix
xx
195
208
222
235
244
253
270
283
293
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary
Supplements
LG Malta and RH Liu
305
315
327
346
358
378
387
Asian Aquaculture
F Corsin and K Yamamoto
403
VOLUME 2
B
Beef Cattle
AD Herring
Biodiversity and Ecosystem Services in Agroecosystems
K Garbach, JC Milder, M Montenegro, DS Karp, and FAJ DeClerck
1
21
xxi
41
61
69
94
Biotechnology: Pharming
S Kjemtrup, TL Talarico, and V Ursin
117
134
153
Breeding: Animals
GL Bennett, EJ Pollak, LA Kuehn, and WM Snelling
173
187
C
Changing Structure and Organization of US Agriculture
WJ Armbruster and MC Ahearn
201
220
232
244
256
266
284
294
307
317
337
359
xxii
375
387
Crop Insurance
G Schnitkey and B Sherrick
399
Crop Pollination
SG Potts, T Breeze, and B Gemmill-Herren
408
D
Dairy Animals
J Gupta, ID Gupta, and MV Chaudhari
419
435
Determining Functional Properties and Sources of Recently Identified Bioactive Food Components:
Oligosaccharides, Glycolipids, Glycoproteins, and Peptides
M Lange, H Lee, D Dallas, A Le Parc, JMLN de Moura Bell, and D Barile
441
Domestication of Animals
TR Famula
462
Domestication of Plants
P Gepts
474
487
VOLUME 3
E
Ecoagriculture: Integrated Landscape Management for People, Food, and Nature
SJ Scherr, L Buck, L Willemen, and JC Milder
18
35
59
68
82
F
Farm Management
W Edwards and P Duffy
100
xxiii
113
Fermented Beverages
CW Bamforth
124
137
Food Engineering
RM Boom and AEM Janssen
154
Food Labeling
CA Hutt and M Gonzalez
167
Food Law
B van der Meulen
186
Food Marketing
MR Thomsen, G Kyureghian, and RM Nayga Jr.
196
Food Microbiology
HM Hungaro, WEL Pena, NBM Silva, RV Carvalho, VO Alvarenga, and AS SantAna
213
Food Packaging
GL Robertson
232
250
273
289
304
311
324
338
352
Food Toxicology
SL Taylor and JL Baumert
366
Forage Crops
DH Putnam and SB Orloff
381
406
G
Genebanks: Past, Present, and Optimistic Future
C Lusty, L Guarino, J Toll, and B Lainoff
417
xxiv
433
454
461
499
518
529
H
Heterosis in Plants
JA Birchler
539
544
VOLUME 4
I
Industrialized Farming and Its Relationship to Community Well-Being
CW Stofferahn
15
31
International and Regional Institutions and Instruments for Agricultural Policy, Research, and
Development
S Pandey
44
International Trade
TG Schmitz and A Schmitz
49
58
66
Investments in and the Economic Returns to Agricultural and Food R&D Worldwide
PG Pardey, C Chan-Kang, S Dehmer, JM Beddow, TM Hurley, X Rao, and JM Alston
78
L
Land Use: Catchment Management
AR Melland, P Jordan, PNC Murphy, P-E Mellander, C Buckley, and G Shortle
98
Land Use, Land Cover, and Food-Energy-Environment Trade-Off: Key Issues and Insights for
Millennium Development Goals
GG Das
xxv
114
134
139
148
M
Mareks Disease and Differential Diagnosis with Other Tumor Viral Diseases of Poultry
IM Gimeno
Market-Based Incentives for the Conservation of Ecosystem Services in Agricultural Landscapes:
Examples from Coffee Cultivation in Latin America
K Williams-Guillen and S Otterstrom
156
172
186
Mathematical Models to Elaborate Plans for Adaptation of Rural Communities to Climate Change
JB Grau, JM Anton, D Andina, AM Tarquis, and JJ Martn
193
Medicinal Crops
L Zhou, J Xu, and Y Peng
223
231
N
Natural Capital, Ecological Infrastructure, and Ecosystem Services in Agroecosystems
EJ Dominati, DA Robinson, SC Marchant, KL Bristow, and AD Mackay
245
O
Organic Agricultural Production: Plants
JM Wachter and JP Reganold
265
287
P
Pathogen-Tested Planting Material
RR Martin and IE Tzanetakis
304
313
330
335
xxvi
343
349
360
375
388
400
408
425
441
456
460
472
489
504
521
Production Economics
P Berck and G Helfand
536
544
VOLUME 5
Q
Quantitative Methods in Agricultural Economics
DA Bessler, BA McCarl, X Wu, and H Alan Love
Quarantine and Biosecurity
SJ McKirdy, SB Sharma, and KL Bayliss
1
11
R
Regulatory Challenges to Commercializing the Products of Ag Biotech
M Newell-McGloughlin and J Burke
21
xxvii
41
46
Rural Sociology
DH Constance
62
S
Safety of Street Food: Indonesias Experience
A Wirakartakusumah, EH Purnomo, and R Dewanti-Hariyadi
75
Sensory Science
J Prescott, JE Hayes, and NK Byrnes
80
102
113
122
133
140
153
166
185
197
211
Stem Cells
RJ Etches
235
Sugar Crops
SR Kaffka and DA Grantz
240
261
T
Terroir: The Application of an Old Concept in Modern Viticulture
P Clingeleffer
277
289
303
xxviii
V
Vaccines and Vaccination Practices: Key to Sustainable Animal Production
KA Schat
315
333
356
W
Water: Advanced Irrigation Technologies
CB Hedley, JW Knox, SR Raine, and R Smith
378
407
425
437
450
Z
Zoonotic Helminths of Livestock
AR Moorhead
466
Index
475
A
Advances in Animal Biotechnology
LB Schook and LA Rund, University of Illinois, Urbana, IL, USA
W Hu, China Agricultural University, Beijing, China
KA Darfour-Oduro and LA Knapp, University of Illinois, Urbana, IL, USA
FM Rodrigues, Federal University of Pelotas, Pelotas, Brazil
KM Schachtschneider, University of Illinois, Urbana, IL, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Clone A cell, group of cells, or organism that is produced
asexually from and is genetically identical to a single
ancestor.
Genetic marker Gene or other identiable portion of
deoxyribonucleic acid (DNA) whose inheritance can be
followed.
Marker-assisted selection (MAS) The use of DNA markers
to improve response to selection in a population. The
markers will be closely linked to one or more target loci,
which may often be QTL.
Nuclear transfer A laboratory procedure in which a
cells nucleus is removed and placed into an oocyte
with its own nucleus removed so the genetic
information from the donor nucleus controls the
resulting cell. Such cells can be induced to form
embryos.
doi:10.1016/B978-0-444-52512-3.00220-5
Table 1
Center of domestication
11 000
9 000
8 000
5 750
5 250
6 0009 000
4 500
4 000
Insemination procedure
Articial Insemination
History of articial insemination
Articial insemination refers to the introduction of semen and
viable sperm into the female reproductive tract via articial
means. Lazzaro Spallanzani, a French physiologist, was the
rst person to successfully demonstrate articial insemination
in animals, when he articially impregnated a dog in 1784.
However, the use of articial insemination for commercial
purposes began in 1937, when the rst articial insemination
cooperative was established in the US. Articial insemination
is still widely practiced today; approximately 60% of dairy
cows in the US are bred by articial insemination.
In Vitro Fertilization
History of in vitro fertilization
IVF refers to the fertilization of an ovum by a spermatozoon
outside of the body. Research on the possibilities of animal
IVF began in the late 1800s, whereas the rst attempts at
animal IVF began in the early 1930s (Bavister, 2002). The rst
attempts used rabbit oocytes and spermatozoa, but were unsuccessful. In 1951 the discovery of sperm capacitation by
researchers Austin and Chang explained why those initial experiments failed: Spermatozoa need to develop and undergo
changes in the female reproductive tract before fertilization
can occur (Bavister, 2002). This discovery enabled Chang to
successfully fertilize rabbit oocytes in vitro using sperm that
was capacitated in vivo. This led to the rst mammalian IVF
birth, a rabbit born in 1959 (Brackett, 2001). However, it
was approximately 20 years later when the rst successful
mammalian IVF was performed using spermatozoa capacitated in vitro. Today, IVF is still being heavily researched and
the full extent of its promises for animal biotechnology has
not been reached. However, it has already greatly increased
researchers knowledge of animal reproductive mechanisms.
Commercially, the bovine industry has seen the greatest impact from IVF. Hundreds and thousands of bovine embryos
created via IVF are sold and exchanged worldwide each year.
Culture of embryos
Once fertilization occurs, there are a number of different
methods to culture the fertilized oocytes. Some species require
that the 28-cell stage embryos be transferred to the oviduct of
a live animal (Havlicek et al., 2005). For in vitro culturing, there
are numerous protocols that can be used. One method frequently used is a coculture in which the medium contains
oviduct cells to replicate in vivo conditions. A sequential medium method is also commonly used, where the components
of the media are changed depending on the cell stage of the
embryos, mimicking the different chemical environments
embryos experience as they mature in vivo. Many factors affect
the development of embryos, including temperature, pH, and
gas concentrations. Depending on the researchers needs the
embryos may be used for embryo transfer, the implantation of
embryos into viable females, or cryopreserved for shipping or
future use.
allowing females to produce more offspring. These technologies have allowed desirable female donors to produce up
to 20 offspring each year. In addition, embryo transfer has
allowed for genetically inferior females to be utilized for their
birthing capabilities, serving as the recipient female. Embryo
transfer also allows for the diversication of species within
geographical regions, as embryos can be easily shipped
across the globe. This is also a much more cost-efcient and
bio-secure method compared to transporting live animals
(Senger, 2003).
Embryo Flushing
Instead of fertilizing oocytes and culturing the embryos in vitro
(as in IVF), embryos are often produced in vivo and then
ushed out of the uterus. In fact, embryo ushing is much
more prevalent and cost-efcient than IVF for the production
of embryos. Although the rst successful embryo ush and
transfer was performed in rabbits in 1890, the procedure is
primarily done with cattle today. More cattle undergo embryo
ushing each year than all other species combined. Embryo
ushing is primarily accomplished by articially inseminating
a superovulated female donor with spermatozoa from a genetically superior male. The embryos are collected from the
donor after fertilization occurs, typically within 68 days.
Bovine embryo collection typically employs a Foley catheter,
ushing medium, and a collection vessel. The Foley catheter is
inserted into the uterus and the ushing medium is passed
through the catheter. The catheter typically contains a small
balloon that seals off the uterus and prevents the backow of
the ushing medium. The ushing medium is allowed to ow
back out of the catheter and is collected in a vessel. Depending
on the success of superovulation and fertilization, the ushing
medium may contain 130 embryos. The typical yield for
cattle that undergo superovulation and articial insemination
is 57 viable embryos (Senger, 2003). The embryos can be
examined by a microscope for viability and transferred to a
recipient or cryopreserved using the same methods previously
discussed for IVF.
Cloning
History of cloning
Although recent advances have opened bountiful opportunities and discussions on animal cloning, cloning experiments
have been taking place for more than 100 years. An animal
clone is broadly dened as an animal that originates from
another animal, and both animals share identical chromosomal DNA. Hans Dreisch created the rst animal clones in
the late 1800s. He created sea urchin clones by splitting a twocell embryo and allowing both cells to independently develop
into sea urchins. These embryo-splitting experiments continued into the 1900, led by the Nobel Prize winning Hans
Spemmans work on salamander embryos. The next major
advance came in 1952 when Robert Briggs cloned a frog using
a new technique; he used nuclear transfer to transplant the
nucleus of a blastomere from a frog embryo into an enucleated
egg. Although Briggs showed embryonic nuclear transfer could
produce clones, not many believed that adult somatic cells
could be used as donors. However, in 1996 the largest
breakthrough in animal cloning came in the form of a sheep
named Dolly. Dolly became the rst animal to be cloned using
the nucleus of a differentiated adult cell as a donor. Dolly
opened the door to cloning via somatic cell nuclear transfer
(SCNT), and many other species have been cloned in the last
few decades.
species have already been collected. The researchers must now receive
permission from the government to conduct experiments on the 420
samples already collected. Several environmentalists are concerned
about this project because these cloned, hybridized, and captive-bred
animals, if mixed with wild populations, could result in potential environmental risks. However, the project was specically designed to
supply zoos rather than replenishing wild populations.
The cloning of endangered species has raised several issues between conservationists and environmentalists, who say that instead of
cloning to save these species, more efforts to protect and recover their
natural habitats should be made. They believe that conserving the natural
habitat where these animals live would have a greater impact on the
preservation of these species.
Inserting human genes into an animals genome allows animals to produce important human proteins, such as the blood
clotting agent factor IX. However, the methods for producing
transgenic animals are not very efcient. Incorporation rates
of the new gene into their genome are low and occur at random sites which often do not allow the gene to be expressed.
Also, the insertion can cause disruption in the expression of
another gene. Researchers at the Roslin Institute sought to use
cloning as an efcient way to produce transgenic animals. In
theory, once a cell line successfully incorporates and expresses
a transgene, that cell line can be used as a donor cell for
cloning. The clones produced will have the transgene incorporated into their genome and can successfully pass it to
their offspring through traditional breeding methods. This
could lead to entire herds of transgenic animals expressing
important genes for medical and agricultural purposes.
Transgenics and cloning also hold enormous potential for
Genome Editing
Precision Editing Opens a World of Possibilities for Transgenics
The precision of nuclease-based genomic editing can lead to custom
designed animals with improved traits and modications to better serve
as human disease models. Cows milk allergy (CMA) is an immunologically mediated allergic reaction to certain proteins in cows milk. The
CMA-inducing protein beta-lactoglubulin causes diarrhea and vomiting
in children. It is estimated that the prevalence of CMA varies between
0.25% and 4.9% and is higher in children than in adults. For the last few
decades researchers have been trying to create transgenic cows that
produce beta-lactoglobulin-free milk, but have been unsuccessful because of a lack of precision associated with gene editing. Recently
researchers found a gene encoding microribonucleic acid (miRNA) in
mice that targets beta-lactoglubulin mRNA and silences its production.
This technology is known as RNA interference (RNAi), and it allows for
the elimination of beta-lactoglobulin protein without needing to alter the
gene itself. After successfully inserting the miRNA gene into the genome
of cow embryos, one calf was born that produced beta-lactoglobulin-free
milk.
Although RNAi is effective at silencing genes, it cannot eliminate the
protein completely. Transcription activator-like effector nucleases
(TALENs) are articial restriction enzymes created by the fusing of a DNA
binding domain with a DNA cleavage molecule. TALENs work by cutting
DNA at specic sequences, introducing double-stranded breaks into
a gene of interest. When the cells repair the breaks they introduce
mutations into the gene that can render the gene nonfunctional. In
pigs, TALENs have been used to disrupt genes encoding low-density
lipoprotein (LDL) receptors. Pigs lacking these receptors are unable to
remove LDL from the bloodstream, causing them to develop atherosclerotic arteries. Such pigs can be used as disease models to aid
biomedical research in human atherosclerosis.
Silk in milk
Transgenic goats are also being produced for dragline silk in
their milk. Dragline silk is made by orb spiders and is the
strongest known material by weight. Because of its strength as
well as its elasticity, there is much interest in large-scale production of dragline silk for use in military uniforms, medical
sutures, and tennis racket strings. After failing to produce the
material in bacteria and mammalian cell culture, scientists in
Canada have successfully inserted the spider silk genes into
goat embryos. When the transgenic goats matured, the spider
genes were expressed in the mammary glands of females,
which began to secrete tiny strands of spider silk in their milk.
Once protocols are in place for the purication and spinning,
the resulting thread could be used for a number of commercial
as well as medical applications.
10
Xenotransplantation
An estimated 45 000 Americans under age 65 could benet
from a heart transplant each year, but only approximately
2000 human hearts are available. To close this gap, researchers
have begun to study xenografts, the transplanting of organs
and tissues from animals into humans. Although nonhuman
primates such as chimpanzees are genetically closest to
humans, reducing the chances of graft rejection, primates are
endangered in the wild and their use as a source of replacement organs raises ethical concerns because of their high level
of intelligence and the increased risk of disease transmission
between such closely related species. As an alternative, some
have proposed using pigs as a source of organs because they
11
Antimicrobials
The immune system of newborn piglets is immature, and thus
they are susceptible to many bacterial infections, some of which
cause diarrhea. These infections can also signicantly reduce
newborn survival rate. Although it is common to use antibiotic
feed additives for newborns, this has led to a drastic increase in
the number of antibiotic-resistant bacterial strains. This has required alternative approaches to prevent bacterial infections in
piglets. Transgenic approaches offer great promise. Transgenic
goats have been produced that make milk with the same concentration of lysozyme, the natural antimicrobial agent, as
human breast milk (Brundige et al., 2008). This milk was fed to
piglets and it helped protect against Escherichia coli and improved gastrointestinal health. Transgenic cattle have also been
produced that make human lysozyme and milk in their milk so
that it is nutritionally similar to human breast milk.
Antimicrobial peptides (AMPs) exhibit another crossroad
of transgenics and disease resistance. Cecropin B, the AMP that
originates from the giant silk moth, has many antimicrobial
effects. Many of these antimicrobial effects are against gramnegative bacteria. The gene encoding for cecropin B was
transfected into catsh and the Asian medaka sh. Both
transgenic sh breeds showed increased bacterial resistance to
numerous pathogens.
12
Table 2
Available single nucleotide polymorphism (SNP) chips
developed for some animal species
Species
Identication
Provider
Number of SNPs
Cat
Horse
Sheep
Cattle
Cattle
Cattle
Sheep
Cattle
Pig
Dog
Feline
Equine
Ovine
BovineHD
BovineSNP50v2
BOS 1
OvineSNP50
BovineLD
PorcineSNP60
CanineHD
Illumina
Illumina
Illumina
Illumina
Illumina
Affymetrix
Illumina
Illumina
Illumina
Illumina
62 897
65 157
5 409
777 962
54 609
648 000
52 241
6 909
62 163
173 662
13
Environmental Concerns
Several environmental concerns about GE animals are considered of high importance because both early identication
and nding solutions to any problem are so difcult. The main
concern is the possibility of GE animals entering natural environments (through release or escape) and disrupting ecosystems (Animal Biotechnology: Science-Based Concerns,
2002; Cowan, 2011).
For example, animals with high mobility and that have
historic records of causing community damages, such as insects,
shellsh, sh, and mice and rats, which can become feral easily
and cause a high level of environmental concern. GloFish, a
uorescent red zebrash, was the rst transgenic animal commercially available in the US and a really popular aquarium
item. Because this zebrash is from southern Asia and cannot
survive long in the cold US waters, it is believed that these GE
zebrash pose no risk to the environment. However, the
AquAdvantage Salmon (currently being evaluated) grow much
faster than any wild salmon and, if released into the wild, could
pose signicant ecologic and genetic risks to native salmon
stocks (Animal Biotechnology: Science-Based Concerns, 2002).
This is why the company has proposed to sell only infertile
female salmon eggs and which must be grown in inland tanks
to reduce any risk of release into the wild. Furthermore, the
cloning of extinct species, such as the woolly mammoth, is
another focus of recent environmental concerns.
14
the FDA approved the rst biopharmaceutical product produced by a transgenic animal (goats) in 2009. This was ATryn,
antithrombin III manufactured by GCC-Biotherapeutics.
When a product from animal biotechnology comes to the
market, it is subject to FDA and APHIS labeling requirements.
It is considered illegal to introduce food from a GE animal
into the food supply without previous approval by FDA. For
example, in food biotechnology, those products considered
GRAS that are equivalent to food products that are already on
the market, such as milk from cows receiving BST do not need
to be labeled. However, those foods derived from GE animals
that have altered genomes are not considered substantially
equivalent and are required to be labeled. Attempts to create
state laws for labeling of food produced by biotechnology
have failed. Ethical questions regarding such labeling concern
the right of the consumers to know the process by which food
is produced. FDA is not allowed to consider those ethical
questions. Its authority just covers safety issues (Cowan, 2011;
Bazer et al., 2010).
Multimedia Annexes
PDF on Articial Insemination
This PDF gives a basic overview of articial insemination,
beginning with semen collection and ending with the
References
Aigner, B., Renner, S., Kessler, B., et al., 2010. Transgenic pigs as models for
translational biomedical research. Journal of Molecular Medicine (Berlin) 88 (7),
653664.
Ajmone-Marsan, P., Garcia, J.F., Lenstra, J.A., 2010. On the origin of cattle: How
aurochs became cattle and colonized the world. Evolutionary Anthropology:
Issues, News, and Reviews 19 (4), 148157.
Allan, M.F., Smith, T.P.L., 2008. Present and future applications of DNA
technologies to improve beef production. Meat Science 80 (1), 7985.
Andersson, L., 2011. How selective sweeps in domestic animals provide new insight
into biological mechanisms. Journal of International Medicine 271, 114.
Animal Biotechnology: Science-Based Concerns, 2002. National Research Council of
the National Academies. Washington, DC: The National Academy Press.
Bavister, B.D., 2002. Early history of in vitro fertilization. Reproduction 124 (2),
181196.
Bazer, F., Einsiedel, E., Gaskell, G. Murray, J., Riley, M., 2010. Ethical implications
of animal biotechnology: Considerations for animal welfare decision making.
15
Horiuchi, T., Numabe, T., 1999. Intracytoplasmic sperm injection (ICSI) in cattle and
other domestic animals: Problems and improvements in practical use. Journal of
Mammalian Ova Research 16 (1), 19.
Jabed, A., Wagner, S., McCracken, J., Wells, D.N., Laible, G., 2012. Targeted
microRNA expression in dairy cattle directs production of b-lactoglobulin-free,
high-casein milk. Proceedings of National Academy of Science of the USA 109
(42), 1681116816.
Jensen, P., 2006. Domestication From behaviour to genes and back again.
Applied Animal Behaviour Science 97 (1), 315.
Joung, J.K., Sander, J.D., 2013. TALENS: A widely applicable technology for
targeted genome editing. Nature Reviews Molecular Cell Biology 14 (1), 4955.
Kochhar, H.P.S., Evans, B.R., 2007. Current status of regulating biotechnologyderived animals in Canada Animal health and food safety considerations.
Theriogenology 67 (1), 188197.
Lai, L., Kang, J.X., Li, R., Wang, J., et al., 2006. Generation of cloned transgenic
pigs rich in omega-3 fatty acids. Nature Biotechnology 24 (4), 435436.
Larson, G., Albarella, U., Dobney, K., et al., 2007. Ancient DNA, pig domestication,
and the spread of the Neolithic into Europe. Proceedings of the National
Academy of Sciences of the USA 104 (39), 1527615281.
Long, D.B., Zhang, K.Y., Chen, D.W., Ding, X.M., Yu, B., 2009. Effects of active
immunization against myostatin on carcass quality and expression of the
myostatin gene in pigs. Animal Science Journal 80 (5), 585590.
Luikart, G., Gielly, L., Excofer, L., et al., 2001. Multiple maternal origins and weak
phylogeographic structure in domestic goats. Proceedings of the National
Academy of Sciences of the USA 98 (10), 59275932.
Meuwissen, T.H.E., Hayes, B.J., Goddard, M.E., 2001. Prediction of total
genetic values using genome-wide dense marker maps. Genetics 157 (4),
18191829.
Oltenacu, P.A., Broom, D.M., 2010. The impact of genetic selection for increased
milk yield on the welfare of dairy cows. Animal Welfare 19 (1), 3949.
Pedrosa, S., Uzun, M., Arranz, J.-J., et al., 2005. Evidence of three maternal
lineages in near eastern sheep supporting multiple domestication events.
Proceedings of the Royal Society B: Biological Sciences 272 (1577),
22112217.
Prather, R.S., Sutovsky, P., Green, J.A., 2004. Nuclear remodeling and
reprogramming in transgenic pig production. Experimental Biology and Medicine
229 (11), 11201126.
Reh, W., Maga, E.A., Collette, N.M., et al., 2004. Hot topic: Using a stearoyl-CoA
desaturase transgene to alter milk fatty acid composition. Journal of Dairy
Science 87 (10), 35103514.
Richt, J.A., Kasinathan, P., Hamir, A.N., et al., 2007. Production of cattle lacking
prion protein. Nature Biotechnology 25 (1), 132138.
Sax, K., 1923. The association of size differences with seed-coat pattern and
pigmentation in Phaseolus vulgaris. Genetics 8 (6), 552560.
Senger, P.L., 2003. Pathways to Pregnancy and Parturition, second ed. Pullman,
WA: Current Conceptions, Inc.
Skoglund, P., Gtherstrm, A., Jakobsson, M., 2011. Estimation of population
divergence times from non-overlapping genomic sequences: Examples from dogs
and wolves. Molecular Biology and Evolution 28 (4), 15051517.
Tessanne, K., Golding, M.C., Long, C.R., et al., 2012. Production of transgenic
calves expressing an shRNA targeting myostatin. Molecular Reproductive and
Development 79 (3), 176185.
Thoday, J.M., Boam, T.B., 1961. Regular responses to selection. I. Description of
responses. Genetics Research 2, 161176.
Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., Gregory, P.D., 2010. Genome
editing with engineered zinc nger nucleases. Nature Reviews Genetics 11 (9),
636646.
Van Berkel, P.H., Welling, M.M., Geerts, M., et al., 2002. Large scale production of
recombinant human lactoferrin in the milk of transgenic cows. Nature
Biotechnology 20 (5), 484487.
Vigne, J.D., Zazzo, A., Salige, J.F., et al., 2009. Pre-neolithic wild boar
management and introduction to Cyprus more than 11,400 years ago.
Proceedings of the National Academy of Sciences of the USA 106 (38),
1613516138.
Von Baeyer, E., 2010. World Environmental History. The Development and History of
Horticulture. Encyclopedia of Life Support Systems (EOLSS). Oxford, UK: Eolss
Publishers.
Wells, G.A., Scott, A.C., Johnson, C.T., et al., 1987. A novel progressive spongiform
encephalopathy in cattle. Veterinary Record 121 (18), 419420.
Wheeler, M.B., Bleck, G.T., Donovan, S.M., 2001. Transgenic alteration of sow
milk to improve piglet growth and health. Reproduction Supplement 58, 313324.
Wu, X., Ouyang, H., Duan, B., et al., 2012. Production of cloned transgenic cow
expressing omega-3 fatty acids. Trasgenic Research 21 (3), 537543.
16
Zeder, M.A., Emshwiller, E., Smith, B.D., Bradley, D.G., 2006. Documenting
domestication: The intersection of genetics and archaeology. Trends in Genetics
22 (3), 133159.
Relevant Websites
http://www.nature.com/news/animals-engineered-with-pinpoint-accuracy-1.11506?WT.
ec_id=NEWS-20121002
Animals engineered with pinpoint accuracy.
http://www.nifa.usda.gov/nea/animals/in_focus/reproduction_if_assisted.html
Assisted reproductive technologies.
http://emedicine.medscape.com/article/432418-overview#a1
Biologic barriers to xenotransplantation.
http://europa.eu/legislation_summaries/agriculture/food/l28130_en.htm
Deliberate release of genetically modied organisms.
http://www.roslin.ed.ac.uk/public-interest/dolly-the-sheep/
Dolly the sheep.
http://www.fao.org/docrep/004/T0117E/T0117E02.htm#ch2.6
Embryo transfer.
http://www.fda.gov/AnimalVeterinary/GuidanceComplianceEnforcement/
PoliciesProceduresManual/default.htm
FDAs animal policies and procedures manual.
http://cmr.asm.org/content/17/2/465.long
Foot and mouth disease review.
http://www.clonesafety.org/cloning/facts/process/
Process of cloning.
http://www.prrs.org/default.aspx#.UVx-doXHVG5
PRRS eradication project.
http://mmbr.asm.org/content/67/4/657.full
RNA interference.
http://www.fda.gov/animalveterinary/safetyhealth/animalcloning/ucm124765.htm
Somatic cell nuclear transfer.
http://www.nature.com/news/synthetic-vaccine-could-prevent-future-outbreaks-of-footand-mouth-disease-1.12700
Synthetic vaccine for FMD.
Glossary
Active ingredient Part of pesticide formulation that leads
to biological effects of pesticides.
Characterization factors Characterization factors are used
to quantitatively model the impact from each emission/
consumed resource that comes from the life cycle inventory
and are expressed as category indicatory results. The
indicator of an impact category can be chosen anywhere
along the impact pathway (midpoint or endpoint level).
Characterization factors are usually calculated for
continental and global scales.
Ecolabeling A voluntary method of environmental
performance certication and labeling. An ecolabel
identies the proven environmental preference of a product
or service within a specic product or service category.
Endocrine disruptor Chemicals that at certain doses can
interfere with the hormone system in mammals.
Hazard Inherent properties of a pesticide, which gives
potential for adverse effects to humans or the environment
during its production, use, or disposal, depending on the
degree of exposure.
LC50-concentration Statistically derived concentration of
a pesticide expected to kill 50% of test organisms in a given
population under set conditions.
Introduction
A particular challenge for humans of this century is to secure
food for the growing world population accompanied by
unprecedented urbanization and rural exodus rates. This
challenge is exacerbated by the effects of global warming. As a
consequence, risk management in food production systems
urgently needs to be improved (Food and Agriculture Organization of the United Nations (FAO) Committee on World
Food Security reports). Pesticides play a vital role in maintaining and enhancing agricultural efciency and productivity,
ensuring the quality of produce and availability of perfect
produce throughout the year, and minimizing produce losses
postharvest. A recent report concluded that without pesticides,
crop yields would be halved and food prices would increase by
40% (Rickart, 2010).
The value of global crop protection products at the distributor level totaled US$44 Billion in 2011, which was an
increase of 14.9% compared with 2010 (agribusiness consultancy reports). However, data on the global annual total
volume of pesticides used are not available. It is suggested that
the actual volumes have been declining during recent years in
spite of the reported increasing market values (Agrow World
doi:10.1016/B978-0-444-52512-3.00242-4
17
18
Pesticide Fate
In this section, the entire life cycle of pesticides is considered,
from the manufacturing of the active substances to the formulation of the pesticide product, to the use of the products
and the disposal of residual pesticides and containers by the
end user.
19
Human dimension
- Soil
- Production system
- Climate
- Grower
Tree shelter
Volatilization and
photodecomposition
Photolysis
Runoff
Decompostion
transformation
Ad-/desorption to
soil matrix
Leaching
preferential flow
20
Figure 2 Schematic drawing showing pathways for point and nonpoint source pesticide pollution to surface water resources.
limited to the distribution of pesticides in different environmental compartments and environmental pesticide fate
models.
A huge number of pesticide fate models has been developed since the 1980s, including PELMO (Klein et al.,
2000), CREAMS (Knisel, 1980), Opus (Smith, 1992), MACRO
(Jarvis, 1994), HYDRUS-2D (imunek et al., 1996), LEACHM
(Wagenet and Hutson, 1987), PEARL (Tiktak et al., 1998;
Tiktak et al., 2012), RZWQM (Ma et al., 2004), and EuroPEARL
(Tiktak et al., 2004). Comprehensive reviews of models for
pesticide transport in soils are given, inter alia, by Jury and
Ghodrati (1989); Cohen et al. (1995); Tiktak (2000); Simunek
et al. (2003); Nolan et al. (2005); and Dubus and Surdyk
(2006). The majority of these models is deterministic, but
some stochastic models have also been proposed (Lindahl
et al., 2005; Zacharias et al., 1999; Jury and Roth, 1990;
Heuvelink et al., 2010). Deterministic models assume that a
given set of initial and boundary conditions leads to a single
outcome due to certain processes that can be described
mathematically, whereas stochastic models take into consideration the spatial and temporal heterogeneities in soil
properties and processes. The outcome of any one realization
is considered to be uncertain. A large number of sample
realizations lead to the denition of the probability density
function for the underlying process.
Regardless of the model complexity, all models simplify
reality to a certain degree and the algorithms implemented
need to be validated (Arenstein et al., 1993; Armstrong et al.,
1996; Clemente et al., 1998; Thorsen et al., 1998). Generally,
pesticide fate models need to be calibrated for a site before any
attempts of model validation (Dubus et al., 2002; Tiktak,
2000). In spite of extensive efforts in pesticide fate modeling
Pesticide Effects
In this section, some examples of pesticide effects resulting
from the exposure of humans, ora, and fauna to the (eco)
toxicological active ingredients of pesticides are provided. First
of all, it has to be noted that chronic and acute effects of
pesticides can be distinguished. Chronic toxicity is dened as
the capacity for a pesticide to produce injury following
chronic exposure or to produce effects which persist whether
or not they occur immediately on exposure or are delayed
(Holland, 1996). In contrast, acute toxicity is the ability of a
substance to cause adverse effects within a short period following dosing or exposure (Holland, 1996). Furthermore,
adverse effects need further specication. In the simplest case,
lethal and sublethal effects can be distinguished (Desneux
et al., 2007). Duffus (1993) and Nordberg et al. (2007) compiled comprehensive overviews on different toxicological
terms.
For example, pesticide residues in water resources are discussed as one of the potential factors for sh and amphibian
deformations that have been observed globally (Hayes et al.,
2010). Negative effect of pesticides on pollinators (Gill et al.,
2012) and biodiversity in soils (Bhat, 2012) have been reported. Moreover, pesticide exposure is discussed as a potential trigger for cancer (Alavanja and Bonner, 2012; Ventura
et al., 2012; Alexander et al., 2012; Koutros et al., 2013);
neuroanomalies among children have been explained by
pesticide exposure (Rosas and Eskenazi, 2008), and some
pesticides are suspected to act as endocrine disruptors (Mnif
et al., 2011). Health issues related to pesticide usage are associated with signicant costs. A recent paper estimated that in
the US the annual costs linked to pesticide exposures were
approximately US$200 million based on the data from
emergency department visits, hospitalizations, and for deaths
(Langley and Mort, 2012). It has been commonly accepted
that pesticide residues in produce are an issue of concern and
have led some supermarket chains to devise their own
21
22
Problem formulation
Risk
managers
Dialog
Risk
assessors
Exposure
Risk
managers
Effect
Risk management
Ecological realism
23
RACsw;ac derivation
(linked to PECsw;max)
RACsw;ch derivation
(linked to PECsw;max
or PECsw;twa)
TK / TD
models
Tier-3:
Population and community-level
experiments and models
Tier-2: Acute lab tests
with additional species
and/or refined exposure
Complexity
(data)
Figure 4 Schematic representation of the tiered approach within the acute (left part) and chronic (right part) effect assessment for pesticides. For
each pesticide, both the acute and chronic effects/risks have to be assessed. Each tier results in a regulatory acceptable concentration (RAC) that
needs to be compared with a relevant exposure concentration to identify whether a risk is present. PEC, predicted environmental concentration;
TX/TD, toxicokinetic/toxicodynamic. Reproduced from EFSA Panel on Plant Protection Products and their Residues (PPR), 2013. Guidance on
tiered risk assessment for plant protection products for aquatic organisms in edge-of-eld surface waters. European Food Safety Authority Journal
11, 32903558. Available at: www.efsa.europa.eu/efsajournal (accessed 06.02.14). doi: 10.2903/j.efsa.2013.3290.
24
(g L1)
Nonarable
00.01
0.010.1
0.11
110
> 10
(g L1)
Nonarable
00.01
0.010.1
0.11
110
> 10
Figure 5 Leaching concentration of an example substance in two different crops, that is, corn (left) and potatoes (right). As the protection goal is
the 90th percentile of the leaching concentration in a specic crop, percentiles are only calculated for the area where this crop is present. This
implies that the 90th percentile is crop dependent. Calculations are done with a metamodel of EuroPEARL (Tiktak et al., 2006).
Table 1
25
Selection of potential strategies to enhance the safe and effective use of pesticides
Strategy
http://environment.alberta.ca/01598.html http://environment.alberta.
ca/01598.html
http://www.epa.gov/oppfead1/safety/applicators/applicators.htm
Walker, 2005a
http://les.foes.de/de/downloads/tagungvilm2005/norwaystudy.pdf
http://www.extension.umn.edu/pesticides/private.html
http://www.nda.nebraska.gov/pesticide/buffer_strip.html for a
discussion of the usefulness of buffer zones refer to the
comprehensive review by Reichenberger et al. (2007)b
http://www.oecd.org/env/spraydrift/government-laws-policies-andguidance.htm for news/information on spray-drift reduction
technology refer to http://www.sdrt.info/
http://ec.europa.eu/food/plant/pesticides/sustainable_use_pesticides/
index_en.htm
Recommended practice in many European countries
http://www.pesticidesatlas.net/
http://ec.europa.eu/food/plant/pesticides/sustainable_use_pesticides/
index_en.htm
Europe
Walker, J., 2005. Development of good agricultural practice programs in New Zealand's fruit industries. In: International Seminar on Technology Development for Good
Agriculture Practice in Asia and Oceania. Japan: National Agricultural Research Center.
b
Reichenberger, S., Bach, M., Skitschak, A., Frede, H.-G., 2007. Mitigation strategies to reduce pesticide inputs into ground- and surface water and their effectiveness;
A review. Science of the Total Environment 384, 135.
26
Figure 6 Left: Pesticide risk calculation with the GROWSAFE Calculator Version 1.0.6.14. Right: Example of the output of the herbicide-leaching
likelihood ranking tool PESTPROP. This decision-support tool allows the selection of herbicides with low risk of leaching. PESTPROP uses
groundwater ubiquity score (GUS) and the attenuation approach.
27
6
1995
2011
5
4
3
2
1
Average kg ai ha1
Average kg ai ha1
28
12
10
1995
2011
8
6
4
2
0
0
6.1A
6.1B
6.1C
6.1D
6.1E
6.7A
NC
16
14
12
10
8
6
4
2
0
1995
2011
9.1A
9.1B
9.1C
9.1D
6.7B
NC
NC
Average kg ai ha1
Average kg ai ha1
1995
2011
9.2A
9.2B
9.2C
9.2D
NC
Figure 7 Left: Example of effects of introducing integrated management practices on organophoshate insecticide use on apples in New Zealand
(Manktelow et al., 2005). Right: The mean active ingredient use of hazardous substances and new organisms (HSNO) classied 6.1 (human
toxicity) and 9.1 (ecotoxic) insecticides applied to apples (Walker et al., 2009).
in Europe. These consequences include compulsory application of additional risk mitigation measures and withdrawal
of the substance from the market. Recently, concepts and tools
have been developed that aim at such a holistic environmental
assessment of products. These tools include LCAs and product
footprinting. The following section is dedicated to explaining
the principal ideas of these instruments and provides examples
on how these approaches have been applied to the product
pesticide.
29
environmental compartments: air, surface water, and groundwater. An application of the model to leek production is described in de Backer et al. (2009). The technosphere in the
PestLCI approach is dened as the agricultural eld on which
the studied crop grows, up to 1 m of depth, as well as the air
column above the eld, up to 100 m height. Any pesticide
leaving this technosphere is considered an emission to the
environment. In this approach, the agricultural soil is part of
the technosphere. As a consequence there are no pesticide
emissions to soil. Emissions to soils outside the technosphere
are possible; however, this is considered in LCIA models: in
LCI the emissions from the technosphere to the ecosphere are
considered, and LCIA models are used to determine the fate of
chemicals after they enter the ecosphere. The main reason for
excluding the agricultural soil as an emission compartment in
PestLCI is that agricultural soil is a highly manipulated soil
with reduced biodiversity. Therefore, the soil cannot be considered as a part of the natural environment that LCA seeks to
protect.
In the LCIA of pesticides emitted to the environment, a
number of tools are available to assess their (eco)toxicity
impacts. Most of the recently developed impact assessment
methodologies have some way of quantifying these environmental impacts. A frequently applied model is USEtox
(Rosenbaum et al., 2008). This model was developed in a
consensus process by the developers of a number of toxicity
assessment models used in LCA and was found to be the best
existing characterization model at midpoint (Hauschild et al.,
2013). Besides application in LCIA, USEtox can also be used
in comparative risk assessment. USEtox is used to calculate
characterization factors for human toxicity and freshwater
ecotoxicity impacts of (organic) chemicals. These characterization factors can then be combined with emission data
from LCI in order to arrive at the potential environmental
impacts. In USEtox, as in other impact assessment models,
human toxicity impacts are assessed by means of fate, exposure, and effect factors. These factors, respectively, describe
where in the environment a chemical ends up, how much
humans are exposed to the chemical, and the damage it does
once human beings are exposed. Likewise, freshwater ecotoxicity characterization factors are calculated from fate and
exposure factors. Characterization factors are calculated for
two geographical scales: continental and global, where the
continental scale is nested in the global scale. USEtox users
can calculate characterization factors of chemicals not already
included in the model by inserting a number of physical and
chemical properties of the compound, as well as a limited
number of toxicity data.
In current LCA practice, the assessment of environmental
impacts is limited to the active ingredient. Although metabolites of the active ingredient sometimes impact the environment, these compounds have so far been ignored in both LCI
and LCIA, mainly due to a lack of data.
30
Conclusions
Modern agricultural production systems are characterized by
innovative management practices and techniques to meet the
global food challenge, and the commitment to minimize
environmental footprints at the same time and take stewardship of natural capital. There is no doubt that pesticides will
continue to play a vital role in these systems. Risks associated
with pesticide manufacturing, use, and disposal is inevitable
because pesticides are toxic by design. Advances in pesticide
risk management are made in partnership of science, industry,
government, consumers, and pesticide end-users. Enhanced
awareness of consumers, increased product responsibility of
pesticide manufacturers and distributors, informed and educated pesticide users, independent expert advisers, and responsible governmental pesticide regulating agencies are
enhancing the development of successful pesticide risk reduction strategies. Many different approaches to reduce
pesticide impacts on human health and the environment have
been developed. In this article, following strategies are introduced: (1) regulate and control pesticide production and use,
(2) promote safe pesticide use, (3) apply pesticide risk assessment tools to optimize pest management, (4) apply
agricultural management strategies, and (5) enhance pesticide
LCS. Regulation of pesticide production and use is indispensable for reducing pesticide risks. It has led to minimizing or banning the use of pesticides in critical areas for
environmental and health reasons in the past. Similarly,
training, information, and raising awareness to enhance safe
pesticide use are necessary but these strategies would not
automatically translate into reducing risks. The biggest problem for these strategies to be successful is to establish effective
communication channels and to present information in a
form accessible to end-users. The development of risk
References
Adriaanse, P.I., 1996. Fate of Pesticides in Field Ditches: The TOXSWA Simulation
Model. Report 90, 240 pp. Wageningen, The Netherlands: DLO Winand Staring
Centre.
Adriaanse, P.I., 1997. Exposure assessment of pesticides in eld ditches: The
TOXSWA model. Pesticide Science 49, 210212.
Ahmad, R., Kookana, R.S., Megharaj, M., Alston, A.M., 2004. Aging reduces the
bioavailability of even a weakly sorbed pesticide (carbaryl) in soil. Environmental
Toxicology and Chemistry 23, 20842089.
Aislabie, J., Lloyd-Jones, G., 1995. A review of bacterial degradation of pesticides.
Australian Journal of Soil Research 33, 925942.
Alavanja, M.C.R., Bonner, M.R., 2012. Occupational pesticide exposures and cancer
risk: A review. Journal of Toxicology and Environmental Health-Part B-Critical
Reviews 15, 238263.
Alexander, D.D., Weed, D.L., Mink, P.J., Mitchell, M.E., 2012. A weight-of-evidence
review of colorectal cancer in pesticide applicators: The agricultural health study
and other epidemiologic studies. International Archives of Occupational and
Environmental Health 85, 715745.
Anhalt, J.C., Arthur, E.L., Anderson, T.A., Coats, J.R., 2000. Degradation of atrazine,
metolachlor, and pendimethalin in pesticide-contaminated soils: Effects of aged
residues on soil respiration and plant survival. Journal of Environmental Science
and Health Part B-Pesticides Food Contaminants and Agricultural Wastes 35,
417438.
Arenstein, D.J., Workman, S.R., Nokes, S.E., 1993. Calibration and Validation of the
Opus Model for Predicting Soil Water Movement. St. Joseph, MI: ASAE.
Armstrong, A.C., Portwood, A.M., Leeds-Harrison, P.B., Harris, G.L., Catt, J.A.,
1996. The validation of pesticide leaching models. Pesticide Science 48, 4755.
Ashauer, R., Boxall, A.B.A., Brown, C.D., 2007. New ecotoxicological model to
simulate survival of aquatic invertebrates after exposure to uctuating and
sequential pulses of pesticides. Environmental Science & Technology 41,
14801486.
Ashauer, R., Brown, C.D., 2013. Highly time-variable exposure to chemicals-toward
an assessment strategy. Integrated Environmental Assessment and Management
9, e27e33.
31
Dijkman, T.J., Birkved, M., Hauschild, M.Z., 2012. PestLCI 2.0: A second generation
model for estimating emissions of pesticides from arable land in LCA.
International Journal of Life Cycle Assessment 17, 973986.
Dubus, I.G., Beulke, S., Brown, C.D., 2002. Review: Calibration of pesticide leaching
models: Ritical review and guidance for reporting. Pest Management Science 58,
745758.
Dubus, I.G., Surdyk, N., 2006. State-of-the-art on pesticide fate models and
environmental indicators. Report DL#4 of the FP6 EU-funded FOOTPRINT project.
Available at: www.eu-footprint.org (accessed 06.02.14).
Duffus, J.H., 1993. Glossary for chemists of terms used in toxicology. Pure &
Applied Chemistry 65, 20032122.
Duwig, C., Delmas, P., Mller, K., et al., 2008. Quantifying uorescent tracer
distribution in allophanic soils to image solute transport. European Journal of
Soil Science 59, 94102.
van Eerdt, M.M., van Dam, J., Tiktak, A., et al., 2012. Evaluatie van de nota
Duurzame gewasbescherming (Evaluation of the Dutch Policy Plan on
Sustainable Crop Protection). Bilthoven: PBL Publication.
van Eerdt, M., Spruijt, J., Zeijts, H., Tiktak, A., 2014. Costs and effectiveness of onfarm measures to reduce aquatic risks from pesticides in the Netherlands. Pest
Management Science. doi:10.1002/ps.3729.
EFSA Panel on Plant Protection Products and their Residues (PPR), 2010. Scientic
opinion on the development of specic protection goal options for environmental
risk assessment of pesticides, in particular in relation to the revision of the
guidance documents on aquatic and terrestrial ecotoxicology (SANCO/3268/2001
and SANCO/10329/2002). European Food Safety Authority Journal 8,
18211873. Available at: www.efsa.europa.eu/efsajournal (accessed 06.02.14).
doi:10.2903/j.efsa.2010.1821.
EFSA Panel on Plant Protection Products and their Residues (PPR), 2012a.
Scientic opinion on clustering and ranking of emissions of plant protection
products from protected crops (greenhouses and crops grown under cover) to
relevant environmental compartments. European Food Safety Authority Journal
10, 26112698. Available at: www.efsa.europa.eu/efsajournal (accessed
06.02.14). doi:10.2903/j.efsa.2012.2611.
EFSA Panel on Plant Protection Products and their Residues (PPR), 2012b.
Scientic Opinion on the science behind the guidance for scenario selection and
scenario parameterisation for predicting environmental concentrations of plant
protection products in soil. European Food Safety Authority Journal 10,
25622638. Available at: www.efsa.europa.eu/efsajournal (accessed 06.02.14).
doi:10.2903/j.efsa.2012.2562.
EFSA Panel on Plant Protection Products and their Residues (PPR), 2013. Guidance
on tiered risk assessment for plant protection products for aquatic organisms in
edge-of-eld surface waters. European Food Safety Authority Journal 11,
32903558. Available at: www.efsa.europa.eu/efsajournal (accessed 06.02.14).
doi:10.2903/j.efsa.2013.3290.
Ekstrm, G., Ekbom, B., 2011. Pest control in agro-ecosystems: An ecological
approach. Critical Reviews in Plant Sciences 30, 7494.
European Commission, 2010. The CAP Towards 2020: Meeting the Food, Natural
Resources and Territorial Challenges of the Future. Available at: http://ec.
europa.eu/agriculture/cap-post-2013/communication/index_en.htm (accessed
06.02.14).
Evans, J.R., Edwards, D.R., Workman, S.R., Williams, R.M., 1998. Response of
runoff diazinon concentration to formulation and post application irrigation.
Transactions of the American Society for Agricultural Engineering 41,
13231329.
FAO/WHO, 1997. Food Consumption and Exposure Assessment of Chemicals.
Geneva: WHO. WHO/FSF/FOS/97.5.
FAO/WHO, 2001. FAO pesticide residues in food 2000. Plant Production and
Protection Paper, Report 163. Geneva: FAO.
Fischer, P., 1996. Quantizierung der eintragspfade fr panzenschutzmittel in
Fliegewsser. PhD Thesis, Justus-Liebig-Universitt.
Flury, M., 1996. Experimental evidence of transport of pesticides through eld
soils A review. Journal of Environmental Quality 25, 2545.
FOCUS, 2000. FOCUS groundwater scenarios in the EU review of active substances.
Report of the FOCUS Groundwater Scenarios Workgroup, EC Document
Reference Sanco/321/2000 rev2, pp. 202.
FOCUS, 2001. FOCUS surface water scenarios in EU evaluation process under 91/
414/EEC. Report of the FOCUS Working Group on Surface Water Scenarios. EU
Document Reference SANCO/4802/2001-rev2, pp. 245.
FOCUS, 2009. Assessing potential for movement of active substances and their
metabolites to ground water in the EU. Report of the FOCUS Ground Water Work
Group, EC Document Reference Sanco/13144/2010 version 1.
Gevao, B., Semple, K.T., Jones, K.C., 2000. Bound pesticide residues in soils: A
review. Environmental Pollution 108, 314.
32
Ghafoor, A., Jarvis, N.J., Stenstrm, J., 2012. Modeling pesticide sorption in the
surface and subsurface soils of an agricultural catchment. Pest Management
Science. doi:10.1002/ps.3453.
Ghafoor, A., Jarvis, N.J., Thierfelder, T., Stenstrm, J., 2011. Measurements and
modeling of pesticide persistence in soil at the catchment scale. Science of the
Total Environment 409, 19001908.
Gill, R.J., Ramos-Rodriguez, O., Raine, N.E., 2012. Combined pesticide exposure
severely affects individual- and colony-level traits in bees. Nature 491, 105U119.
Gomiero, T., Pimentel, D., Paoletti, M.G., 2011. Environmental impact of different
agricultural management practices: Conventional vs. organic agriculture. Critical
Reviews in Plant Sciences 30, 95124.
Grimm, V., Ashauer, R., Forbes, V., et al., 2009. CREAM: A European project on
mechanistic effect models for ecological risk assessment of chemicals.
Environmental Science and Pollution Research 16, 614617.
Gustafson, D.I., 1989. Groundwater ubiquity score: A simple method for assessing
pesticide leachability. Environment Toxicology and Chemistry 8, 319357.
Gutsche, V., Rossberg, D., 1997. SYNPOS 1.1: A model to assess and to compare
teh environmental risk potential of active ingredients in plant protection products.
Agriculture Ecosystem and Environment 64, 181188.
Hauschild, M.Z., Goedkoop, M., Guine, J., et al., 2013. Identifying best existing
practice for characterization modeling in life cycle impact assessment.
International Journal of Life Cycle Assessment 18, 683697.
Hayes, T.B., Falso, P., Gallipeau, S., Stice, M., 2010. The cause of global amphibian
declines: A developmental endocrinologist's perspective. The Journal of
Experimental Biology 213, 921933.
Heuvelink, G.B.M., Burgers, S.L.G.E., Tiktak, A., van der Berg, F., 2010. Uncertainty
and stochastic sensitivity analysis of the GeoPEARL pesticide leaching model.
Geoderma 155, 186192.
Hilz, E., Vermeer, A.W.P., 2013. Spray drift review: The extent to which a
formulation can contribute to spray drift reduction. Crop Protection 44, 7583.
Holland, P.T., 1996. IUPAC reports on pesticides (36). Glossary of terms relating to
pesticides. (IUPAC recommendations 1996). Pure & Applied Chemistry 68,
11671193.
Hommen, U., Poethke, H.J., Dlmer, U., Ratte, H., 1993. Simulation models to
predict ecological risks of toxins in freshwater systems. ICES Journal of marine
Science 50, 337347.
Jager, T., Albert, C., Preuss, T.G., Ashauer, R., 2011. General unied threshold
model of survival A toxicokinetic-toxicodynamic framework for ecotoxicology.
Environmental Science & Technology 45, 25292540.
Jarvis, N.J., 1994. The MACRO Model (Version 3.1). Technical Description and
Sample Simulations. Uppsala: Swedish University of Agricultural Sciences,
Department of Soil Science.
Jury, W.A., Ghodrati, M., 1989. Overview of organic chemical environmental fate and
transport modeling approaches. In: Sawhney, B.L., Brown, K. (Eds.), Reactions
and Movement of Organic Chemicals in Soils. Madison, WI: Soil Science
Society of America and American Society of Agronomy, pp. 271304.
Jury, W.A., Or, D., Pachepsky, Y., et al., 2011. Kirkham's legacy and contemporary
challenges in soil physics research. Soil Science Society of America Journal 75,
15891601.
Jury, W.A., Roth, C.H., 1990. Transfer Functions and Solute Movement Through
Soils: Theory and Applications. Basel: Birkhuser Verlag.
Kah, M., Beulke, S., Tiede, K., Hofmann, T., 2013. Nano-pesticides: State of
knowledge, environmental fate and exposure modeling. Critical Reviews of
Environmental Science and Technology 43, 18231867.
Klein, M., 2011. PELMO Parameterisation for the FOCUS Groundwater
Scenarios, Available at: http://focus.jrc.ec.europa.eu/gw/par/FOCUS_PELMO_
parameterisation_v2_0.pdf (accessed 06.02.14).
Klein, M., Hosang, J., Schafer, H., Erzgraber, B., Resseler, H., 2000. Comparing and
evaluating pesticide leaching models; Results of simulations with PELMO.
Agricultural Water Management 44, 263281.
Knisel, W.G., 1980. CREAMS: A eld-scale model for chemicals, runoff and erosion
from agricultural management systems. Conservation Report No. 26, pp. 643.
Washington: US Department of Agriculture, Science and Education
Administration.
Kogan, M., 1998. Integrated pest management: Historical perspectives and
contemporary developments. Annual Review of Entomology 43, 243270.
Kookana, R.S., Baskaran, S., Naidu, R., 1998. Pesticide fate and behaviour in
Australian soils in relation to contamination and management of soil and water:
A review. Australian Journal of Soil Research 36, 715764.
Kookana, R.S., Kumar, A., Oliver, D.P., Correll, R.L., 2007. Pesticide risk indicators:
Their role in minimizing off-site impacts of pesticides on water quality. Rational
Environmental Management of Agrochemicals: Risk Assessment, Monitoring, and
Remedial Action 966, 3752.
Koutros, S., Freeman, L.E.B., Lubin, J.H., et al., 2013. Risk of total and aggressive
prostate cancer and pesticide use in the agricultural health study. American
Journal of Epidemiology 177, 5974.
Kruijne, R., Deneer, J., Lahr, J., Vlaming, J., 2011. HAIR2010 documentation.
Calculating risk indicators related to agricultural use of pesticides within the
European Union. Alterra Report 2113.1. Wageningen: Alterra.
Labite, H., Butler, F., Cummins, E., 2011. A review and evaluation of plant
protection product ranking tools used in agriculture. Human and Ecological Risk
Assessment: An International Journal 17, 300327.
Lamine, C., 2011. Transition pathways towards a robust ecologization of agriculture
and the need for system redesign. Cases from organic farming and IPM. Journal
of Rural Studies 27, 209219.
Lang, T., Barling, D., 2007. The environmental impact of supermarkets: Mapping
the terrain and the policy problems. In: Burch, D., Lawrence, G. (Eds.),
Supermarkets and Agri-Food Supply Chains Transformations in the Production
and Consumption of Foods. Glos: Edward Elgar Publishing Limited,
pp. 192215.
Langley, R.L., Mort, S.A., 2012. Human exposures to pesticides in the United States.
Journal of Agromedicine 17, 300315.
Lapworth, D.J., Gooddy, D.C., 2006. Source and persistence of pesticides in a semiconned chalk aquifer of southeast England. Environmental Pollution 144,
10311044.
Larsbo, M., Jarvis, N., 2003. MACRO5.0. A model of water ow and solute transport
in macroporous soil. Technical Description, pp. 47. Uppsala: SLU, Department of
Soil Science. Emergo 2003:6 Studies in the Biogeophysical Environment.
Leistra, M., van der Linden, A.M.A., Boesten, J.J.T.I., Tiktak, A., van den Berg, F.,
2000. PEARL model for pesticide behaviour and emissions in soil-plant systems.
Description of processes. Alterra Report 13, RIVM report 711401009.
Wageningen, The Netherlands: Alterra, Green World Research.
Leon, L.F., Soulis, E.D., Kouwen, N., Farquhar, G.J., 2001. Nonpoint source
pollution: A distributed water quality modeling approach. Water Resources 35,
9971007.
Levitan, L., 2000. How to and why: Assessing the envirosocial impacts of
pesticides. Crop Protection 19, 629636.
Lindahl, A., Kreuger, J., Stenstrom, J., et al., 2005. Stochastic modeling of diffuse
pesticide losses from a small agricultural catchment. Journal of Environmental
Quality 34, 11741185.
Ma, Q., Wauchope, R.D., Rojas, K.W., et al., 2004. The pesticide module of the Root
Zone Water Quality Model (RZWQM): Testing and sensitivity analysis of selected
algorithms for pesticide, fate and surface runoff. Pest Management Science 60,
240252.
Mackay, D., Paterson, S., 1991. Evaluating the multimedia fate of organic
chemicals. A level III fugacity model. Environmental Science & Technology 25,
427436.
Manktelow, D., Stevens, P., Walker, J., et al., 2005. Trends in pesticide use in New
Zealand: 2004. Wellington: HortResearch.
Marer, P., 2000. The Safe and Effective Use of Pesticides. Oakland, CA: University
of California, Agricultural and Natural Resources.
Maud, J., Edwards-Jones, G., Quin, F., 2001. Comparative evaluation of pesticide
risk indices for policy development and assessment in the United Kingdom.
Agriculture Ecosystems & Environment 86, 5973.
Millennium Ecosystem Assessment (MA), 2005. Living Beyond Our Means: Natural
Assets and Human Well-Being. A Statement from the Board, pp. 28. Available at:
http://www.maweb.org/documents/document.429.aspx.pdf (accessed 06.02.14).
Mnif, W., Hassine, A.I.H., Bouaziz, A., et al., 2011. Effect of endocrine disruptor
pesticides: A review. International Journal of Environmental Research and Public
Health 8, 22652303.
Mohaupt, V., Bach, M., Behrendt, H., 2000. Overview on diffuse sources of
nutrients, pesticides and heavy metals in Germany Methods, results and
recommendations for water protection policy. In: 4th International Conference on
Diffuse Pollution, pp. 419428. Bangkok: IAWQ.
Moncrieff, J.E., Bentley, L.R., Palma, H.C., 2008. Investigating pesticide transport in
the Leon-Chinandega aquifer, Nicaragua. Hydrogeology Journal 16, 183197.
Mller, K., Bach, M., Hartmann, H., Spiteller, M., Frede, H.-G., 2002. Point and
non-point source pesticide contamination in the Zwester Ohm catchment
(Germany). Journal of Environmental Quality 31, 308309.
Mller, K., Deurer, M., Northcott, G., Clothier, B.E., 2010. Concept for assessing a
product-related pesticide footprint. New Zealand Plant Protection 63, 3946.
van Nes, E.H., van den Brink, P.J., 2003. PERPEST version 1.0, manual and
technical description. A model that predicts the ecological risks of pesticides in
freshwater ecosystems. Alterra-Rapport 787. Wageningen: Alterra.
Nicholls, C.I., Altierei, M.A., 2007. Agroecology: Contributions towards a renewed
ecological foundation for pest mangement. In: Kogan, M., Jepson, P. (Eds.),
33
Suhre, F.B., 2000. Pesticide residues and acute risk assessment The US EPA
approach. Food Additives and Contaminants 17, 569573.
Surgan, M., Condon, M., Cox, C., 2010. Pesticide risk indicators: Unidentied inert
ingredients compromise their integrity and utility. Environmental Management 45,
834841.
Tumer, K., Stoffregen, H., Wessolek, G., 2006. Seasonal dynamics of preferential
ow in a water repellent soil. Vadose Zone Journal 5, 405411.
Thorbek, P., Forbes, V.E., Heimbach, F., et al., 2009. Ecological Models for
Regulatory Risk Assessments of Pesticides: Developing a Strategy for the Future.
Pensacola and Boca Raton, FL: Society of Environmental Toxicology and
Chemistry.
Thorsen, M., Jrgensen, P.R., Felding, G., et al., 1998. Evaluation of a stepwise
procedure for comparative validation of pesticide leaching models. Journal of
Environmental Quality 27, 11831193.
Tiktak, A., 2000. Application of pesticide leaching models to the Vredepeel dataset II
Pesticide fate. Agricultural Water Management 44, 119134.
Tiktak, A., Boesten, J.J.T.I., Egsmose, M., et al., 2013. European scenarios for
exposure of soil organisms to pesticides. Journal of Environmental Science and
Health, Part B 48, 703716.
Tiktak, A., Boesten, J.J.T.I., van der Linden, A.M.A., Vanclooster, M., 2006. Mapping
ground water vulnerability to pesticide leaching with a process-based metamodel
of EuroPEARL. Journal of Environmental Quality 35, 12131226.
Tiktak, A., Hendriks, R.F.A., Boesten, J.J.T.I., 2012. Simulation of movement of
pesticides towards drains with a preferential ow version of PEARL. Pesticide
Management Science 68, 290302.
Tiktak, A., van der Linden, A.M.A., Boesten, J.J.T.I., 2003. The GeoPEARL model.
Model description, applications and manual. RIVM Report 716601007. Bilthoven,
The Netherlands: RIVM.
Tiktak, A., van der Linden, A.M.A., van der Pas, L.J.T., 1998. Application of the
pesticide transport assessment model to a eld study in a humic sandy soil in
Vredepell, The Netherlands. Pesticide Science 52, 321336.
Tiktak, A., de Nie, D.S., Pineros Garcet, J.D., Jones, A., Vanclooster, M., 2004.
Assessment of the pesticide leaching risk at the Pan-European level. The
EuroPEARL approach. Journal of Hydrology 289, 222238.
Tsui, M.T.K., Chu, L.M., 2003. Aquatic toxicity of glyphosate-based formulations:
Comparison between different organisms and the effects of environmental factors.
Chemosphere 52, 11891197.
US Environmental Protection Agency, 2003. Generic Ecological Assessment
Endpoints (GEAEs) for Ecological Risk Assessment.
Vanclooster, M., Boesten, J.J.T.I., Tiktak, A., et al., 2004. On the use of unsaturated
ow and transport models in nutrient and pesticide management. In: Feddes, R.
A., de Rooij, G.H., van Dam, J.C. (Eds.), Unsaturated-Zone Modeling Progress,
Challenges and Applications. Deventer: Kluwer, pp. 331361.
Vanclooster, M., Boesten, J.J.T.I., Trevisan, M., et al., 2000. A European test of
pesticide-leaching models: Methodology and major recommendations.
Agricultural Water Management Special Issue. Pesticide Leaching Modeling
Validation. A European Experience 44, 119.
Ventura, C., Nunez, M., Miret, N., et al., 2012. Differential mechanisms of action are
involved in chlorpyrifos effects in estrogen-dependent or -independent breast
cancer cells exposed to low or high concentrations of the pesticide. Toxicology
Letters 213, 184193.
Vryzas, Z., Papadakis, E.N., Vassiliou, G., Papadopoulou-Mourkidou, E., 2012.
Occurrence of pesticides in transboundary aquifers of North-eastern Greece.
Science of the Total Environment 441, 4148.
Wagenet, R.J., Hutson, J.L., 1987. LEACHM: Leaching Estimation and Chemistry
Model, vol. 2. Ithaca, NY: Water Resources Institute Continuum, Center for
Environmental Research, Cornell University.
Walker, J.T.S., Park, N.M., Clothier, B.E., et al., 2009. Progress in pesticide risk
reduction in New Zealand horticulture. New Zealand Plant Protection 62,
321327.
Waltz, E., 2010. Glyphosate resistance threatens Roundup hegemony. Nature
Biotechnology 28, 537538.
Wauchope, R.D., 1978. The pesticide content of surface water draining from
agricultural elds A review. Journal of Environmental Quality 7,
459472.
Wauchope, R.D., Williams, R.G., Marti, L.R., 1990. Runoff of sulfometuron-methyl
and cyanazine from small plots: Effects of formulation and grass cover. Journal
of Environmental Quality 14, 132136.
Wauchope, R.D., Yeh, S., Linders, J.B.H.J., et al., 2002. Review. Pesticide soil
sorption parameters: Theory, measurement, uses, limitations and reliability. Pest
Management Science 58, 419445.
van der Werf, H.M.G., Zimmer, C., 1998. An indicator of pesticide environmental
impact based on a fuzzy expert system. Chemosphere 36, 22252249.
34
Willer, H., Lernoud, J., Kilcher, L., 2013. The world of Organic Agriculture. Statistics
and Emerging Trends 2013. Bonn: Research Institute of Organic Agriculture
(FiBL), Frick, Switzerland and International Federation of Organic Agriculture
Movements (IFOAM).
Williams, J.C., 2011. New EU pesticide legislation The view of a manufacturer.
Aspects of Applied Biology 206, 269274.
Winter, M., Lobley, M., 2009. What is Land for? The Food, Fuel and Climate
Change Debate. London, UK: Earthscan.
Zacharias, S., Heatwole, C.D., Persaud, N., et al., 1999. Stochastic simulation of
eld-scale pesticide transport using Opus and GLEAMS. Journal of
Environmental Quality 28, 411423.
van Zeijts, H., Overmars, K., van der Bilt, W., et al., 2012. Greening the Common
Agricultural Practice: Impacts on farmland biodiversity on an EU scale. Bilthoven,
the Netherlands: PBL Netherlands Environmental Assessment Agency. PBL
Publication number 500136005. Available at: www.pbl.nl (accessed 06.02.14).
Zhan, Y., Zhang, M., 2012. PURE: A web-based decision support system to evaluate
pesticide environmental risk for sustainable pest management practices in
California. Ecotoxicology and Environmental Safety 82, 104113.
de Zwart, D., Posthuma, L., 2005. Complex mixture toxicity for single and multiple
species: Proposed methodologies. Environmental Toxicology and Chemistry 24,
26652676.
Relevant Websites
www.agrow.com/multimedia/archive
Agrow World Crop Protection News.
www.agrow.com/multimedia/archive/00068/DS247_68751a.pdf
Agrow World Crop Protection News.
impact.cals.cornell.edu/project/advocating-pesticide-life-cycle-stewardship
Cornell University.
www.croplife.org/responsible_use
CropLife International.
www.ecoinvent.ch
Ecoinvet database.
www.endureinformationcentre.eu/
ENDURE Information Centre.
epp.eurostat.ec.europa.eu
European Commission.
epp.eurostat.ec.europa.eu/cache/ITY_OFFPUB/KS-76-06-669/EN/KS-76-06-669-EN.
PDF
European Commission.
www.efsa.europa.eu/
European Food Safety Authority Publications.
www.fao.org/cfs
FAO.
www.fao.org/cfs/cfs-hlpe/report-3-food-security-and-climate-change/en/
FAO.
www.fao.org/agriculture/crops/obsolete-pesticides/prevention-and-disposal-ofobsolete-pesticides/en/
FAO.
www.fao.org/agriculture/crops/obsolete-pesticides/what-now/acp-mea/en/
FAO.
focus.jrc.ec.europa.eu/
Forum for the Co-ordination of Pesticide Fate Models and their Use.
www.growsafe.co.nz
Growsafe.
www.ifoam.org
International Foundation for Organic Agriculture Movements.
www.maweb.org
Millenium Ecosystem Assessment.
www.phillipsmcdougall.com
Phillips McDougall Crop Protection & Biotechnology Consultants.
pure.ucdavis.edu
University of California, Davis.
www.epa.gov
US Environmental Protection Agency News & Publications.
www.pesticidemodels.eu/
Wageningen University and Research Centre (WUR), the National Institute of
Public Health and the Environment (RIVM), and the Netherlands Environmental
Assessment Agency (PBL).
www1.ifc.org
World Bank Group.
www1.ifc.org/wps/wcm/connect/af3d03804885588b808cd26a6515bb18/Final%2B-%
2BPesticides.pdfMOD=AJPERES&id=1323153151755
World Bank Group.
Glossary
Agrobacterium A soil bacterium that infects susceptible
plants and genetically transforms the infected plant. Certain
species of Agrobacterium (e.g., A. tumifaciens) is used in the
laboratories to genetically transform desired plants for crop
improvement.
Coat protein (CP) A viral structural protein that is
the only or the major component of the proteinaecious
coat of the virus that encapsulates the viral genetic
material.
Genetic transformation Transformation of an organism
(plant, animal, or a microorganism) for a desired
phenotype (trait) using a manipulated DNA fragment
(transgene) from another organism (plant, animal, or a
microorganism).
Hermaphrodite/hermaphroditic A hermaphrodite is a
bisexual organism (plant, animal, or a microorganism) with
both male and female characteristics.
Micropropagation Propagation of plants by articial
means from tissues developed from a single plant cell or a
tiny piece of plant tissue.
doi:10.1016/B978-0-444-52512-3.00252-7
35
36
Table 1
Country
India
Brazil
Indonesia
Nigeria
Mexico
Ethiopia
D. R. Congo
Thailand
Guatemala
China
Philippines
Colombia
Cuba
Peru
Venezuela
Others
Total
Metric ton
(1000)
(1000)
104.3
35.5
11.1
94.0
14.2
17.9
13.2
13.2
2.2
7.3
8.6
5.0
5.8
9.2
6.6
73.4
421.5
4 180.1
1 854.3
958.3
705.0
634.4
340.2
280.3
271.9
205.5
181.2
157.9
153.2
135.0
125.8
125.6
1 503.0
11 838.7
Source: Data digested from Food and Agriculture Organization (FAO), Statistical
Division, 2013 (Available at: http://faostat.fao.org/faostat/).
reduces the number, size, and quality of the fruits and thus
causes severe economic loss to growers (Figure 1(ac)).
In nature, PRSV is transmitted nonpersistently by aphids
(Figure 1(d)) (Purcifull et al., 1984) and is mechanically saptransmissible. Apart from the predominant mosaic strains of
PRSV, certain strains of PRSV cause severe wilting and death of
the infected plants (Chang, 1979). To date, most of the papaya
plantation areas of the world suffer devastation by this virus
and lack of an effective control measure completely thwarts the
farmers from opting for papaya cultivation. PRSV was reported
in 1975 from the southern part of Taiwan, and it destroyed
most of the papaya plantations in the country within a few
years and caused unprecedented yield loss (Wang et al., 1978).
The aphid-borne PRSV belongs to the genus Potyvirus of the
family Potyviridae (King et al., 2011), one of the largest and
economically important plant virus groups. The virion of PRSV
is a 78012 nm exuous particle (Figure 1(e)) with a positive
sense single-stranded RNA genome (De La Rosa and Lastra,
1983; Yeh and Gonsalves, 1985). The genomic RNAs of several
PRSV strains, including those from Hawaii (Yeh et al., 1992)
and Taiwan (Wang and Yeh, 1997), have been sequenced. The
PRSV genomic RNA is 10.3 kb in length and it encodes a single
polyprotein that is proteolytically processed by three viruscoded proteases into nine nal proteins, including the 36 kDa
coat protein (CP) for encapsidation of the viral genome
(Purcifull and Hiebert, 1979; Gonsalves and Ishii, 1980; Yeh
et al., 1992) and the proteins of cylindrical (Purcifull and
Edwardson, 1967) and amorphous (Martelli and Russo, 1976)
inclusions in the cytoplasm of the infected host cells. The PRSV
genomic RNA is uncapped, but it possesses a covalently attached molecule of VPg protein at the 5 end and a polyA tail
at the 3 end. The rst reported PRSV genome contains 10 326
nucleotides with a genetic organization of 5-leader, P1, HCPro, P3, CI, 6K, NIa (processed further into VPg and NIa
protease), NIb, CP, and 3-noncoding region (Yeh et al., 1992).
The genetic organization and gene functions of PRSV are presented in Figure 1(f).
(a)
37
(b)
(c)
(d)
(e)
Replication
membrane attachment
5UTR
PRSV
Vpg
6K
P1
P1
Proteinase
Cell-to-cell movement
Host range
(f)
HC-Pro
P3
CIP
HC-Pro
Vpg NIaPro
CP
NIb
3UTR+Poly (A)
NlaPro
Possible role in
replication?
Proteinase
Pathogenicity
Genome amplification
Aphid transmission
Suppressor of gene silencing
Cell-to-cell movement
Genome amplification
Translation initiation
ATPase-helicase
cell-to-cell movement
Replicase
Proteinase
host determinant
RNA encapsidation
long distance movement
aphid transmission
Figure 1 Disease symptoms, aphid vector and particles of Papaya ringspot virus (PRSV). (a) A papaya plantation devastated by PRSV. (b) and
(c) Symptoms of ringspots on papaya fruit, and mosaic on papaya leaves, respectively. (d) Alate (winged) aphid, the insect vector transmitting
PRSV, perching on a papaya leaf. (e) PRSV particles under electron microscope; the scale bar represents 100 nm. (f) Genetic organization and
gene functions of PRSV.
of the same virus (Gonsalves and Garnsey, 1989). An attenuated mutant strain of PRSV, designated HA 5-1, was selected
following nitrous acid mutagenesis of a severe strain HA
originating from Hawaii (Yeh and Gonsalves, 1984). PRSV HA
5-1 was tested extensively in the eld and has been used
widely in Taiwan and Hawaii since 1985 to permit an economic return from papaya production (Wang et al., 1987; Yeh
et al., 1988; Yeh and Gonsalves, 1994). Similar genetically
stable, broad-spectrum attenuated strains of major papayainfecting viruses may be screened from natural sources or engineered in the laboratory for effective cross-protection.
The effectiveness of cross-protection strategy is limited by
several technical and practical difculties, including nonavailability of efcient and genetically stable attenuated
strains, superinfection by virulent strains, requirement for a
large-scale inoculation facility, and insufcient protection
38
(1)
(2)
(3)
(4)
(5)
(a)
(1)
(2)
(b)
Figure 2 Effective control measures of Papaya ringspot virus (PRSV) by cross-protection and netting. (a) Papaya seedlings were mass-inoculated
with a mild strain PRSV HA 5-1 by pressure spray (1) and kept in insect-proof nethouse (2). The HA 5-1 cross-protected papaya plant was
resistant to severe infection of PRSV HA (3); cross-protected papaya plants loaded with fruits in Taiwan (4); HA 5-1 protected plants loaded with
fruits versus unprotected fruitless plants with severe symptoms in a Hawaii eld test (5). (b) A papaya orchard protected by netting to avoid PRSV
infection (1); Destruction of the protective net by a tropical storm (2). Reproduced with permission from Yeh, S.D., Gonsalves, D., Wang, H.L.,
Namba, R., Chiu, R.J., 1988. Control of Papaya ringspot virus by cross protection. Plant Disease 72, 375380.
widely accepted because HA 5-1 did not provide good protection against Thai PRSV strains (Yeh and Gonsalves, 1994).
39
40
(1)
(2)
(3)
(4)
41
(a)
(1)
(2)
(3)
(4)
(b)
Figure 3 Broad-spectrum resistance of coat protein (CP)-transgenic papaya lines showing single-virus (a) and double-virus resistance (b) to
different papaya viral strains. (a) Papaya ringspot virus (PRSV) CP transgenic papaya line 19-0-1 showing broad-spectrum resistance to PRSV
strain of Taiwan YK (1), Hawaii HA (2), Thailand TH (3), and Mexican MX (e) in contrast to the severely infected nontransgenic papaya plants
(1,2,3, and 4 plants at the right). Reproduced with permission from Bau, H.J., Cheng, Y.H., Yu, T.A., Yang, J.S., Yeh, S.D., 2003. Broad spectrum
resistance to different geographic strains of Papaya ringspot virus in coat protein gene transgenic papaya. Phytopathology 93, 112120. (b) Double
resistance to PRSV and Papaya leaf-distortion mosaic virus (PLDMV) conferred by transgenic line 12-4 carrying a PRSV-PLDMV chimeric CP
transgene. Nontransgenic papaya plants were susceptible to PRSV (1) and PLDMV (2), whereas the plants of line 12-4 were resistant to PRSV (3)
and PLDMV (4). Reproduced with permission from Kung, Y.J., Bau, H.J., Wu, Y.L., et al., 2009. Generation of transgenic papaya with double
resistance to Papaya ringspot virus and Papaya leaf-distortion mosaic virus. Phytopathology 99, 13121320.
42
(b)
(a)
(c)
43
(d)
Figure 4 Devastation of the disease caused by Papaya ringspot virus (PRSV) in Nakhon Pathom, a Province of Central Thailand. (a) Symptoms of
ringspots on papaya fruit. (b) Oily streaks on stem. (c) Mosaic and distortion on leaves. (d) A papaya orchard completely destroyed by the
ringspot disease. The grower (right front) explaining his pain and sorrow to the experts: Dr. Wichai Kositrana, Kasesart University, Thailand (third
from left), Dr. Neal Van Alfen, University of California, Davis (second from left), and Dr. William Lucas, University of California, Davis (rst from
left).
44
To date (September 2013), no eld trials or commercialization of GM crops is allowed in Thailand due to fear of
losing export markets, environmental and health concerns,
and seed business takeover by multinational seed companies.
Little public information is available on the costs and benets
of GM technology to the Thai economy; clear national policies
on research and application of GM crops are yet to be made.
Economic evaluation of transgenic crops is essential for the
development of appropriate future agricultural biotechnology
policies. Ex-ante impact assessment based on scientic data
and economic environment of GM papaya adoption in
Thailand estimated that total economic surplus in the range of
US$ 650 million to 1.5 billion would be generated within the
rst 10 years of adoption. Benets from GM papaya adoption
would accrue primarily to small-scale papaya farmers and
also would accrue even with the loss of export markets
(Napasintuwong and Traxler, 2009). The delay in adopting
transgenic technology in Thailand reects the lack of comprehensive biosafety laws, public skepticism concerning
transgenic plants, the lack of trust in the capability to regulate
biosafety, and the effectiveness of the anti GM groups. This
situation dissuades Thai researchers from using modern biotechnology to improve the quality and quantity of crop and
food productions in Thailand.
45
46
The fruits from hermaphroditic papaya plants are commercially desirable than female plants, for they contain less
seeds and thicker esh (Yeh et al., 2007). However, the sex and
other horticultural and fruit traits of transgenic papaya lines
can be determined only after owering and fruit production.
Hence, despite the time and effort spent, only a subpopulation
of plants is represented by the hermaphrodite plants that are
desirable for their fruit quality.
In general, the breeding programs aiming to incorporate
the desired sex and other useful traits into commercial
hybrid cultivars of papaya are technically complicated, laborintensive, and time-consuming. In papaya genetic transformation for micropropagation, somatic embryos derived from
premature zygotic embryos are the most commonly used
starting materials (Fitch and Manshardt, 1990; Cabrera-Ponce
et al., 1995, 1996; Cheng et al., 1996; Cai et al., 1999). Such
premature zygotic embryo-derived somatic embryos are considered to be the most effective explants for both biolistic
delivery and Agrobacterium-mediated transformation. However, the immature zygotic embryos are very difcult to obtain
and often affected by seasonal factors.
Hermaphrodite plants can be generated as clonal plants
using appropriate tissues from selected hermaphroditic individuals through somatic embryogenesis. As shown by Lin and
Yang (2001), the adventitious roots developed from in vitro
shoots of hermaphroditic individuals can be cultured to induce somatic embryos within four months. Using somatic
embryos derived from the adventitious roots of in vitro shoots
of hermaphroditic individuals as explants, Kung et al. (2010)
transformed the elite hybrid cultivar Tainung No. 2 with a
chimeric transgene comprising portions of PRSV and PLDMV
CP gene sequences. The selected transgenic hermaphrodite
lines confer complete resistance to both PRSV and PLDMV.
This strategy was also used to produce transgenic plants of the
parental lines of Tainung No. 2 hybrid cultivar, including
Thailand and Sunrise (Kung et al., 2010).
To ascertain the hermaphroditic criterion of the obtained
transgenic lines during early seedling stage, Kung et al. (2010)
Concluding Remarks
The transgenic resistance conferred by the viral CP gene has
become the most effective method to prevent papaya from
infection by the noxious PRSV. In 1998, the Hawaiian PRSV
CP gene transgenic papaya cultivars Rainbow and SunUp were
deregulated and granted approval for commercialization,
representing the rst successful application of transgenic fruit
tree in the world. Although the transgenic lines are not resistant to most of the PRSV strains from other different geographical areas, the breakdown of the transgenic resistance to
47
48
Acknowledgments
We thank the supports from the Council of Agriculture
(101AS-1.2.2-ST-aB and 102AS-1.2.2-ST-a4), Taiwan, R.O.C.
and the National Science Council (101-2911-1-005-301 and
102-2911-1-005-301) through the NCHU-UCD Plant and
Food Biotechnology Program, National Chung Hsing University, Taiwan, R.O.C.
References
Adsuar, J., 1946. Studies on virus disease of papaya (Carica papaya) in Puerto
Rico, I. Transmission of papaya mosaic. The University of Puerto Rico
Agricultural Experiment Station Technical Paper I, 110.
Angyurekul, N., Tugsinavisuth, S., 2003. Papaya Production and Marketing
Economic Program. Center for Applied Economics Research, Kasetsart University,
Bangkok, Thailand (in Thai language).
Azad, M.A.K., Rabbani, M.G., Amin, L., 2012. Plant regeneration and somatic
embryogenesis from immature embryos derived through interspecic
Devitt, L.C., Fanning, K., Dietzgen, R.G., Holton, T.A., 2010. Isolation and functional
characterization of a lycopene b-cyclase gene that controls fruit colour of papaya
(Carica papaya L.). Journal of Experimental Botany 61, 3339.
European Parliament and Council of European Union, 2003. Concerning the
traceability and labelling of genetically modied organisms and the traceability of
food and feed products produced from genetically modied organisms and
amending Directive 2001/18/EC. In: Regulation EC No. 1830/2003 of the
European Parliament and of the Council of 22 September 2003. Ofcial Journal
of the European Union. Available at: http://www.biosafety.be/PDF/1830_2003_
EN.pdf (accessed 12.05.09).
Fan, M.J., Chen, S., Kung, Y.J., et al., 2009. Transgene-specic and event-specic
molecular markers for characterization of transgenic papaya lines resistant to
Papaya ringspot virus. Transgenic Research 18, 971986.
FAOSTAT, 2013. Production data. Available at: http://faostat.fao.org/site/339/default.
aspx (accessed 10.04.13).
Fermn, G., Keith, R.C., Suzuki, J.Y., et al., 2011. Allergenicity assessment of the
Papaya ringspot virus coat protein expressed in transgenic rainbow papaya.
Journal of Agricultural and Food Chemistry 59, 1000610012.
Ferreria, S.A., Pitz, K.Y., Manshardt, R., Zee, F., Fitch, M., 2002. Virus coat protein
transgenic papaya provides practical control of Papaya ringspot virus in Hawaii.
Plant Disease 86, 101105.
Fitch, M.M.M., Manshardt, R.M., 1990. Somatic embryogenesis and plant
regeneration from immature zygotic embryos of papaya (Carica papaya L.). Plant
Cell Reports 9, 320324.
Fitch, M.M.M., Manshardt, R.M., Gonsalves, D., Slightom, J.L., Sanford, J.C., 1992.
Virus resistance papaya plants derived from tissues bombarded with the coat
protein gene of Papaya ringspot virus. Bio/Technology 10, 14661472.
Frizzi, A., Huang, S., 2010. Tapping RNA silencing pathways for plant biotechnology.
Plant Biotechnology Journal 8, 655677.
Fuchs, M., Gonsalves, D., 2007. Safety of virus-resistant transgenic plants two
decades after their introduction: Lessons from realistic eld risk assessment
studies. Annual Review of Phytopathology 45, 173202.
Gilissen, L.J., Metz, P.L., Stiekema, W.J., Nap, J.P., 1998. Biosafety of E. coli betaglucuronidase (GUS) in plants. Transgenic Research 7, 157163.
Goldbach, R., Bucher, E., Prins, M., 2003. Resistance mechanisms to plant viruses:
An overview. Virus Research 92, 207212.
Gonsalves, D., 1998. Control of Papaya ringspot virus in papaya: A case study.
Annual Review of Phytopathology 36, 415437.
Gonsalves, D., 2002. Coat protein transgenic papaya acquired immunity for
controlling papaya ringspot virus. Current Topics in Microbiology and
Immunology 266, 7383.
Gonsalves, D., Garnsey, S.M., 1989. Cross-protection techniques for control of plant
virus diseases in the tropics. Plant Disease 73, 592597.
Gonsalves, D., Ishii, M., 1980. Purication and serology of papaya ringspot virus.
Phytopathology 70, 10281032.
Gottula, J., Fuchs, M., 2009. Toward a quarter century of pathogen-derived
resistance and practical approaches to plant virus disease control. Advances in
Virus Research 75, 161183.
Gschwend, A.R., Yu, Q., Moore, P., et al., 2011. Construction of papaya male and
female BAC libraries and application in physical mapping of the sex
chromosomes. Journal of Biomedicine and Biotechnology 2011. Article ID
929472. doi:10.1155/2011/929472.
Hamilton, A.J., Baulcombe, D.C., 1999. A species of small antisense RNA in
posttranscriptional gene silencing in plants. Science 286, 950952.
Herold, F., Weibel, J., 1962. Electron microscopic demonstration of Papaya ringspot
virus. Virology 18, 307311.
Hofmeyr, J.D.J., 1938. Genetical studies of Carica papaya L. South African Journal
of Science 35, 300304.
Horovitz, S., Jimenez, H., 1967. Cruzamientos interspecicos intergenericos en
caricaceas y sus implicaciones totecnicas. Agronoma Tropicale 17, 323343.
Jensen, D.D., 1949a. Papaya virus diseases with special reference to papaya
ringspot. Phytopathology 39, 191211.
Jensen, D.D., 1949b. Papaya ringspot virus and its insect vector relationship.
Phytopathology 39, 212220.
Kertbundit, S., Juricek, M., 2010. Application of transgenic technologies to papaya:
developments and biosafety assessments in Thailand. Transgenic Plant Journal 4,
5257.
Khuspe, S., Hendre, R., Mascarenhas, A., et al., 1980. Utilization of tissue culture
isolate in interspecic hybrids in Carica. In: Rao, P.S., Heble, M. (Eds.), Plant
Tissue Culture, Genetic Manipulation and Somatic Hybridization of Plant Cells.
Bombay, India: Bhaba Atomic Research Center, pp. 198205.
Khvorova, A., Reynolds, A., Jayasena, S.D., 2003. Functional siRNAs and miRNAs
exhibit strand bias. Cell 115, 209216.
49
King, A.M.Q., Lefkowitz, E., Adams, M.J., Carstens, E.B., 2011. Virus Taxonomy: 9th
Report of the International Committee on Taxonomy of Viruses. San Diego, CA:
Elsevier Academic Press.
Kongsawat, C., Kittisenachai, S., Chusaeng, K., et al., 2011. Evaluation of novel
protein expressed in transgenic papaya (Khak Nual) resistant to Papaya ringspot
virus (PRSV). Agricultural Science Journal 42, 717.
Knig, A., Cockburn, A., Crevel, R.W.R., et al., 2004. Assessment of the safety of
foods derived from genetically modied (GM) crops. Food and Chemical
Toxicology 42, 10471081.
Kositratana, W., Thaveechai, N., Attathom, S., Hongprayoon, R.,
Chatchawankanphanich, O., 1991. Control of papaya ringspot disease by cross
protection. Kasetsart Journal 25, 3339.
Kung, Y.J., Bau, H.J., Wu, Y.L., et al., 2009. Generation of transgenic papaya with
double resistance to Papaya ringspot virus and Papaya leaf-distortion mosaic
virus. Phytopathology 99, 13121320.
Kung, Y.J., Yu, T.A., Huang, C.H., et al., 2010. Generation of hermaphrodite
transgenic papaya lines with virus resistance via transformation of somatic
embryos derived from adventitious roots of in vitro shoots. Transgenic Research
19, 621635.
Lana, A.F., 1980. Transmission and properties of virus isolated from Carica papaya
in Nigeria. The Journal of Horticultural Science 55, 191197.
Lin, C.M., Yang, J.S., 2001. Papaya somatic embryo induction from fruiting-bearing
eld plants: Effects of root supporting material and position of the rooting
explants. Acta Horticulturae 560, 489492.
Lin, H.T., Yen, G.C., Huang, T.T., et al., 2013. Toxicity assessment of transgenic
Papaya ringspot virus of 823-2210 line papaya fruits. Journal of Agricultural and
Food Chemistry 61, 15851596.
Liu, Z., Moore, P.H., Ma, H., Ackerman, C.M., 2004. A primitive Y chromosome in
papaya marks incipient sex chromosome evolution. Nature 427, 348352.
Lius, S., Manshardt, R.M., Fitch, M.M.M., et al., 1997. Pathogen-derived resistance
provides papaya with effective protection against Papaya ringspot virus.
Molecular Breeding 3, 161168.
Lomonossoff, G.P., 1995. Pathogen-derived resistance to plant viruses. Annual
Review of Phytopathology 33, 323343.
Ma, H., Moore, P.H., Liu, Z., Kim, M.S., Yu, Q., 2004. High-density linkage
mapping revealed suppression of recombination at the sex determination locus in
papaya. Genetics 166, 419436.
Manshardt, R.M., 1992. Papaya. In: Hammerschlag, F.A., Litz, R.E. (Eds.),
Biotechnology of Perennial Fruit Crops. Wallingford: CAB International,
pp. 489511.
Manshardt, R.M., Wenslaff, T.F., 1989. Zygotic polyembryony in interspecic hybrids
of Carica papaya and Carica cauliora. Journal of the American Society for
Horticultural Science 114, 684689.
Maoka, T., Hataya, T., 2005. The complete nucleotide sequence and biotype
variability of papaya leaf distortion mosaic virus. Phytopathology 95, 128135.
Maoka, T., Kashiwazaki, S., Tsuda, S., Usugi, T., Hibino, H., 1996. Nucleotide
sequence of the capsid protein gene of papaya leaf distortion mosaic potyvirus.
Archives of Virology 141, 197204.
Martelli, G.P., Russo, M., 1976. Unusual cytoplasmic inclusions induced by
Watermelon mosaic virus. Virology 72, 352362.
McKinney, H.H., 1929. Mosaic diseases in the Canary Islands, West Africa, and
Gibraltar. Journal of Agricultural Research 39, 557578.
Mekako, H.U., Nakasone, H.Y., 1975. Interspecic hybridization among 6 Carica
species. Journal of the American Society for Horticultural Science 100, 237242.
Miki, B., McHugh, S., 2004. Selectable marker genes in transgenic plants:
Applications, alternatives and biosafety. Journal of Biotechnology 107,
193232.
Ming, R., Hou, S., Feng, Y., et al., 2008. The draft genome of the transgenic
tropical fruit tree papaya (Carica papaya Linnaeus). Nature 252, 991996.
Ming, R., Yu, Q., Moore, P.H., 2007. Sex determination in papaya. Seminars in Cell
and Developmental Biology 18, 401408.
Napasintuwong, O., Traxler, G., 2009. Ex-ante impact assessment of GM papaya
adoption in Thailand. AgBioForum 12, 209217.
Parasnis, A.S., Ramakrishna, W., Chowdari, K.V., Gupta, V.S., Ranjekar, P.K., 1999.
Microsatellite (GATA) n reveals sex-specic differences in papaya. Theoretical
and Applied Genetics 99, 10471052.
Phironrit, N., Phuangrat, B., Burns, P., Kositratana, W., 2010. Resistance of coat
protein transgenic papaya and development of homozygous transgenic papaya
line 116/5 resistant to Papaya ringspot virus (PRSV) under screenhouse
conditions in Thailand. Transgenic Plant Journal 4, 9093.
Powell, M., Wheatley, A.O., Omoruyi, F., et al., 2010. Comparative effects of dietary
administered transgenic and conventional papaya on selected intestinal
parameters in rat models. Transgenic Research 19, 511518.
50
Powell-Abel, P., Nelson, R.S., De, B., et al., 1986. Delay of disease development in
transgenic plants that express the Tobacco mosaic virus coat protein gene.
Science 232, 738743.
Purcifull, D.E., Edwardson, J.R., 1967. Watermelon mosaic virus: Tubular inclusion
in pumpkin leaves and aggregates in leaf extracts. Virology 32, 393401.
Purcifull, D.E., Edwardson, J.R., Hiebert, E., Gonsalves, D., 1984. Papaya ringspot
virus. CMI/AAB Description of Plant Viruses, No 292 (No. 84 Revised, July
1984). Wallingford, UK: CAB International.
Purcifull, D.E., Hiebert, E., 1979. Serological distinction of Watermelon mosaic virus
isolates. Phytopathology 69, 112116.
Ramessar, K., Peremarti, A., Gmez-Galera, S., et al., 2007. Biosafety and risk
assessment framework for selectable marker genes in transgenic crop plants: A
case of the science not supporting the politics. Transgenic Research 16,
261280.
Roberts, M., Minott, D., Tennant, P., Jackson, J., 2008. Assessment of
compositional changes during ripening of transgenic papaya modied for
protection against papaya ringspot virus. Journal of the Science of Food and
Agriculture 88, 19111920.
Sakuanrungsirikul, S., Sarindu, N., Prasartsee, V., et al., 2005. Update on the
development of virus-resistant papaya: Virus-resistant transgenic papaya for
people in rural communities of Thailand. Food and Nutrition Bulletin 26,
422426.
Sanford, J.C., Johnston, S.A., 1985. The concept of parasite-derived resistance:
Deriving resistance gene from the parasite's own genome. Journal of Theoretical
Biology 113, 395405.
Singh, A.B., 1969. A new virus disease of Carica papaya in India. Plant Disease
Reporter 53, 267269.
Singh, O.V., Ghai, S., Paul, D., Jain, R.K., 2006. Genetically modied crops:
success, safety assessment and public concern. Applied Microbiology and
Biotechnology 71, 598607.
Skelton, R.L., Yu, Q., Srinivasan, R., et al., 2006. Tissue differential expression of
lycopene b-cyclase gene in papaya. Cell Research 2006, 731739.
Sondur, S.N., Manshardt, R.M., Stiles, J.I., 1996. A genetic linkage map of papaya
based on randomly amplied polymorphic DNA markers. Theoretical and Applied
Genetics 93, 547553.
Srisomchai, T., 1975. Studies on Papaya ringspot virus. Annual Report 1975, Ofce
of Northeast Regional Agricalture. Thailand: Department of Agriculture, Ministry
of Agriculture and Cooperatives, pp. 228232 (in Thai language).
Storey, W.B., 1938. Segregation of sex types in Solo papaya and their application to
the selection of seed. Proceedings of the American Society for Horticultural
Science 35, 8385.
Storey, W.B., 1969. Papaya (Carica papaya L.). In: Ferwerda, F.P., Wit, F. (Eds.),
Outline of Perennial Crop Breeding in the Tropics. Wageningen: H. Veenman en
Zonen BV, pp. 389407.
Stubbs, L.L., 1964. Transmission and protective inoculation studies with viruses of
the citrus tristeza complex. Australian Journal of Agricultural Research 15,
752770.
Suzuki, J.Y., Tripathi, S., Fermn, G., et al., 2008. Characterization of insertion sites
in Rainbow papaya, the rst commercialized transgenic fruit crop. Tropical Plant
Biology 1, 293309.
Suzuki, J.Y., Tripathi, S., Gonsalves, D., 2007. Virus resistant transgenic papaya:
Commercial development and regulatory and environmental issues. In: Punja, Z.K.,
DeBoer, S., Sanfac-on, H. (Eds.), Biotechnology and Plant Disease Management.
Wallingford: CAB International, pp. 436461.
Technical Biosafety Committee, 2010. White Paper: Thailand Updated Status and
Perspective on Research and Development of Modern Biotechnology and
Biosafety Regulation, third ed National Center for Genetic Engineering and
Biotechnology.
Tennant, P., Fermn, G., Fitch, M.M.M., et al., 2001. Papaya ringspot virus
resistance of transgenic Rainbow and SunUp is affected by gene dosage, plant
development, and coat protein homology. European Journal of Plant Pathology
107, 645653.
Thomas, J.E., Dodman, R.L., 1993. The rst record of Papaya ringspot virus-type P
in Australia. Australasian Plant Pathology 22, 27.
Tripathi, S., Bau, H.J., Chen, L.F., Yeh, S.D., 2004. The ability of Papaya ringspot
virus strains overcoming the transgenic resistance of papaya conferred by the
coat protein gene is not correlated with higher degrees of sequence divergence
from the transgene. European Journal of Plant Pathology 110, 871882.
Tripathi, S., Suzuki, J.Y., Carr, J.B., et al., 2011. Nutritional composition of Rainbow
papaya, the rst commercialized transgenic fruit crop. Journal of Food
Composition and Analysis 24, 140147.
Urasaki, N., Tokumoto, M., Tarora, K., et al., 2002. A male and
hermaphroditespecic RAPD marker for papaya (Carica papaya L.). Theoretical
and Applied Genetetics 104, 281285.
Wang, C.H., Yeh, S.D., 1997. Divergence and conservation of the genomic RNAs of
Taiwan and Hawaii strains of Papaya ringspot virus. Archives of Virology 142,
271285.
Wang, H.L., Wang, C.C., Chiu, R.J., Sun, M.H., 1978. Preliminary study on Papaya
ringspot virus in Taiwan. Plant Protection Bulletin 20, 133140.
Wang, H.L., Yeh, S.D., Chiu, R.J., Gonsalves, D., 1987. Effectiveness of cross
protection by mild mutants of papaya ringspot virus for control of ringspot
disease of papaya in Taiwan. Plant Disease 71, 491497.
Wang, M.B., Masuta, C., Smith, N.A., Shimura, H., 2012. RNA Silencing and Plant
Viral Diseases. Molecular Plant-Microbe Interactions 25, 12751285.
Warin, N., Chowpongpang, S., Bhunchoth, A., et al. 2003. New papaya cultivars for
Papaya ringspot virus resistance. In: Proceedings of the 41st Kasetsart University
Annual Conference, 37 February, 2003, Bangkok, pp. 539546.
Yeh, S.D., Bau, H.J., Kung, Y.J., Yu, T.A., 2007. Papaya biotechnology. In:
Pua, E.C., Darvery, M.R. (Eds.), Biotechnology in Agriculture and Forestry.
Transgenic crops V. Berlin Heidelberg: Springer-Verlag, pp. 7396.
Yeh, S.D., Gonsalves, D., 1984. Evaluation of induced mutants of Papaya ringspot
virus for control by cross protection. Phytopathology 74, 10861091.
Yeh, S.D., Gonsalves, D., 1985. Translation of papaya ringspot virus RNA in vitro:
Detection of a possible polyprotein that is processed for capsid protein,
cylindrical-inclusion protein, and amorphous-inclusion protein. Virology 143,
260271.
Yeh, S.D., Gonsalves, D., 1994. Practices and perspective of control of papaya
ringspot virus by cross protection. Advances in Disease Vector Research 10,
237257.
Yeh, S.D., Gonsalves, D., Wang, H.L., Namba, R., Chiu, R.J., 1988. Control of
Papaya ringspot virus by cross protection. Plant Disease 72, 375380.
Yeh, S.D., Jan, F.J., Chiang, C.H., et al., 1992. Complete nucleotide sequence and
genetic organization of Papaya ringspot virus RNA. Journal of General Virology
73, 25312541.
Yeh, S.D., Kung, Y.J., Bau, H.J., Yu, T.A., Raja, J.A.J., 2010. Generation of a
papaya hybrid variety with broad-spectrum transgenic resistance to Papaya
ringspot virus and Papaya leaf-distortion mosaic virus. In: Pua, E.C., Davery, M.
R. (Eds.), Transgenic Plant Journal 4. Berlin Heidelberg: Springer-Verlag,
pp. 3744.
You, B.J., 2005. Factors of Papaya ringspot virus affecting strain-specic cross
protection and transgenic resistance breakdown. PhD Dissertation, Department of
Plant Pathology, National Chung Hsing University, Taichung, Taiwan, p. 142.
Yu, Q., Tong, E., Skelton, R.L., et al., 2009. A physical map of the papaya genome
with integrated genetic map and genome sequence. BMC Genomics 10, 371.
Zamore, P.D., Haley, B., 2005. Ribo-gnome: The big world of small RNAs. Science
309, 15191524.
Glossary
Agribusiness The sector of the economy that is the
sequence of interrelated activities made up of genetics and
seed stock rms; agricultural input suppliers, agricultural
producers, agricultural commodity merchandisers, food
processors, food retailers, and food consumers.
Capital structure The mix of debt and equity used by a
rm to nance its purchase of assets.
DuPont analysis of protability A nancial management
tool that decomposes return on equity into its component
parts: operating prot margin, asset turnover, and nancial
leverage.
Introduction
The purpose of this article is to discuss contemporary topics
in food and agribusiness research with a focus on a denition
of agribusiness, a description of the global agribusiness environment, and a discussion of the roles in managing an agribusiness rm.
Concept of Agribusiness
The agribusiness sector is comprised of interrelated subsectors
working in concert to provide goods and services to consumers
around the world. With the need to accommodate economic,
social, and environmental concerns, organizations and managers in the sector share many of the challenges that exist in
other business value chains. However, food is an economic
good with distinctive cultural, institutional, and political aspects shaping the economic environment of the sector, the
organizational structure of its rms, and the choice set available to its managers. Further the fundamental uncertainties
emanating from weather and other sources of variability
within biology-based production sectors add to the complexity
of management in the sector.
doi:10.1016/B978-0-444-52512-3.00117-0
51
52
Figure 1 The agribusiness sector. Adapted from Sonka, S.T., Hudson, M.A., 1989. Why agribusiness anyway? Agribusiness 5, 305314.
53
Developed countries
Parameter of analysis
Emerging countries
Stable
Relatively stable
Relatively stable
GDP
Population
Urbanization of population
Mature or declining
Small effect on consumption
Food markets
Income growth and income distribution
Well educated
More homogenous group
Consumer prole
Countries characteristics
Adoption of biofuels
Consumption directed to:
Growing
Growing
Urbanization growing fast and emerging of
mega-cities
Sales are booming
Huge impact on consumption (still a high
percentage of income spent on food)
Being educated
Different segments of emerging
economies, difcult to aggregate
High level of informal markets and food
safety under construction
Smaller participation of expenditure in
food service
In transformation
High possibility
Low sensitivity of population and
regulation being built
Low growth
Quantity and animal protein
Retail systems
Expansion of commodity production
Environment and preservation issues
Source: Adapted from Neves, M.F., 2014. The Future of Food Business, second ed. Singapore: World Scientic, 336 pp.
54
11. Shoe and leather: leather comes from cattle and other
animals.
12. Construction and furniture: wood from planted farms
using eucalyptus, compensated woods, and other sources.
13. Paper and packing: materials come from processed
farmed wood, producing a pulp that is transformed into
paper products.
Table 2
55
Political-legal system
Sociocultural system
Technological system
consumer/user. Boehlje (1999) identies six critical dimensions of a value chain reaching from (1) the processes and
activities that create the products or services demanded by
consumers or end users, (2) the product ow features, (3) the
nancial ows, (4) the information ows across the chain, (5)
the incentive systems to reward performance and share risks,
and (6) the governance and coordination systems.
Agribusiness value chain for food could be described as
two chains that become one at the consumer end (Figure 2).
One value chain follows plants and plant products, and another chain follows animals and animal products. These two
chains blend into one chain at the processing and retailing stages of the chain. Value chains can be as simple as ve
56
Plants
and
plant
products
Input
suppliers
Producers
Processors
and
handlers
Retailers
Animals
and
animal
products
Input
suppliers
Producers
Consumers
Processors
and
handlers
n
ch
Te
Th
rea
new t of
en
tra
nts
ol o
gy
Rivalry
among
existing
firms
Bargaining
power of
buyers
f
to
rea te
Th stitu nd
a
b
su cts
du ces
pro ervi
s
O
driv ther
e
cha rs of
nge
Bargaining
power of
suppliers
behind. New technology can alter not only the efciency and
cost of the production process, but also the actual products
and services offered and demanded by others in the value
chain. New chains may be created due to a new technology in
communication as well as in products and services.
Other drivers of change: Other drivers of change include
changes in government policy and regulations, changes in
international trade agreements, demographic changes, and
other factors not included in the rst six forces. Competitive
pressure comes from differing abilities of rms to respond and
adapt to these changes. The impact of these forces depends on
the scope of the change, the speed at which change is anticipated or actually felt, and the depth and breadth of the
responses needed to adapt to these changes.
57
58
Value creation, providing goods and services that earn revenues that exceed the cost of doing so, is an elemental reason
for a rm to exist. As detailed by Schumpeter (1942), competitive economies rely on market entry and the creative destruction of innovation to shift value to consumers. Value
Firm Strategy
Agribusiness rms can employ a number of concepts and
tools to craft the best t between their strengths and the
current and future needs of the market. These efforts focus on
resources, competencies, and capabilities that create a sustainable competitive advantage, contributing to superior
nancial performance and mitigating risk from changing
market conditions.
Support
activities
Firm infrastructure
rgi
Ma
Technology development
Procurement
Outbound
logistics
Primary activities
Figure 4 The value plate.
Marketing
and sales
Service
rgin
Operations
Ma
Inbound
logistics
Growth
For long-run success, growth is a necessary consideration for
the agribusiness manager. Growth introduces vitality into an
organization. Further, competitors can be expected to attack
the weaker product offerings of the rm. Therefore, growth in
some dimension is almost always necessary just to stay even.
Although protable growth is a key managerial focus, sustained protable growth has proven difcult to achieve with
an estimate that 90% of companies worldwide failed to
achieve sustained protable growth in recent years (Zook,
2010).
59
60
Marketing
Marketing is one of the most important activities for food and
agribusiness companies. Marketing is the relationship development, or the contract building process with possible customers. Successful companies are the ones driven by demand,
or companies that pay attention, innovate, and build strong
and stable relationships with customers.
Perreault et al. (1997) state that if the majority of people,
including managers, were forced to dene marketing they
would say it means sales or advertisement. This answer is
not completely true. Sales and advertisement are just two parts
of a broader set of marketing strategies. Thus, marketing is
dened as a social and managerial process by which individuals and groups obtain what they need and want through
the creation, offer and trade of products and values with others
(Kotler, 1997). Thus, it is a process that aims at satisfying the
needs of the customers through trade.
Marketing activities can be divided into two blocks:
understanding food and agribusiness customers and performing to meet customers needs and wants. Understanding
the food and agribusiness customers requires rms to assess
the needs of the nal consumers and intermediaries through a
research process. The rms analyze the behavior of consumers
to gauge their needs and wants. The rms also scan the macroenvironment (political-legal, economic, natural, sociocultural, and technological) to anticipate changes. The rms
also react to competitors moves in the market. The goal is to
identify opportunities to create additional value for customers.
61
Identify the target public that will receive the communication and develop the desired objectives (brand knowledge, brand memory, and persuasion, among others).
Dene the communication mix that will be used: the advertisement plan, public relations and publicity plan, sales
promotion plan, as well as direct marketing actions, and
web activities, among others.
Budget and possibly determine the expected return for
these investments, measuring well these activities and their
impact.
62
It is more than just brands in the store and in advertisements, electronic communication is more pervasive and
provides more opportunities for communication. For example, rms maintain their own websites and maintain fan
pages on social media websites.
Finance
Firms use nance concepts to measure the efciency of investments and the protability of operational decisions. Finance is concerned with the sources and uses of cash in the
business and the returns to assets (Brigham and Ehrhardt,
2009). Generally speaking, riskier investments should generate
higher expected returns to investment. Thus, when agribusiness rms consider investment opportunities, the cost of
nancial capital is the benchmark return that the investment
must return. Once investments are made, managers of agribusinesses use nancial statements (income statement, balance sheet, and cash ow statement) to measure, monitor, and
correct operational decisions.
63
Operating margin
(EARNS)
x=
Return on assets
(ROA)
Asset turnover
(TURNS)
Earnings leverage
x=
Return on equity
(ROE)
Financial structure
leverage
Figure 7 DuPont identity of return on equity.
Liquidity concerns the ability of the agribusiness to generate cash ows to service its debt obligations as they come due
in the near term. Working capital, working capital turnover,
the current ratio, and the quick ratios are all frequently employed to assess liquidity. Solvency concerns the ability of the
agribusiness to meet its long-term debt obligations and is
frequently measured by considering some form of the debt-toasset ratio. Some research has considered the impacts of
working capital and accrual changes on the protability of
agribusiness rms (e.g., Trejo-Pech et al., 2009).
Cash management
Short-run cash management requires agribusiness rms to
have the cash necessary to settle accounts as they come due.
The rm must have sufcient cash to pay suppliers, employees,
management, and other expenses to continue daily operations.
Typically, holding large amounts of cash to meet these needs is
inefcient because cash held in checking accounts typically
generates insufcient return for the rm to compensate the
suppliers of cash. Investments in inventories, accounts receivable, and other current assets are additional important uses
of cash that are part of operating cash ow. Firm will need to
optimize investments in current assets and use of current liabilities to meet the operating needs of the rm. The management of these accounts is related to the cash conversion
cycle (Figure 8).
Long-run cash management requires agribusiness rms to
have sufcient cash or rapid access to sufcient cash to invest
in long-term growth opportunities. Investments in xed assets,
typically termed investing cash ows, can require large
amounts of additional capital to acquire the new, long-term
assets.
Capital structure
The mix of debt and equity used to nance the purchase of
assets is termed as rms capital structure. The rm must balance the relatively lower cost of debt with the increased nancial risk of borrowing. Firms should choose capital
structure such that the WACC is minimized, which maximizes
the value of the rm. An additional important consideration
64
Operations
The operational activities of the rm are the set of actions
taken to transform strategy and plans into deliverable products
and services to generate nancial and performance results (e.g.,
customer satisfaction). Operations activities include the full
spectrum of work done in a business running the manufacturing plant, shipping or transporting the product to the
customer, sourcing the raw materials to produce the product
or service, organizing and implementing the product/service
sales activity, etc. Efcient and effective operations require an
understanding and assessment of, for example, costs and cost
components, product and work force ow scheduling and
logistics, inventory management, sales and customer relationship management, selecting and managing the workforce,
and capital access and nancial management.
Logistics
Given the highly perishable nature of many agricultural
products, regional production of some widely distributed
products and the biological processes that govern agricultural
production, excellent logistical management is very important
for most agribusiness sectors. Moving products through time
and space so that they reach the end consumer is the essence of
logistics. Optimizing logistics focuses on reducing waste
(shrinkage), minimizing transportation costs, and ensuring
timely delivery.
Given that many agricultural products are very perishable,
such as raw milk, many sectors are dominated by time specicity. Products must reach the end consumer when they are
most desirable and useful, within a relatively limited period of
time. Delays can cause enormous losses to the product.
Many agricultural sectors are dominated by complex distribution systems, which further complicate logistics. This
interdependent network can delay important customer feedback along the supply chain. For example, many manufacturing sectors, such as farm equipment manufacturers, rely
on others to distribute their products to the end users. Farm
Farms (millions)
6
5
4
3
2
1
0
1850
70
90
1910
25
35
45
54
64
74
82
92
2002
Census year
Figure 9 Farms, land in farms, and average acres per the US farm, 18502007. The break in the lines after 1974 reects the introduction of an
adjustment to estimates of the farm count and land in farms. Beginning in 1978, the data are adjusted to compensate for undercoverage by the
Census of Agriculture. For more information, see Allen (2004). Reproduced with permission from Hoppe, R.A., Banker, D.E., 2010. Structure and
Finances of U.S. Farms: Family Farm Report, 2010 Edition, EIB-66, July. U.S. Department of Agriculture, Economic Research Service, compiled
from Census of Agriculture data.
Inventory management
Inventory management can play a large role in the success of
agribusinesses. Production along the entire chain, particularly
in the grain sectors, is dominated by the weather. As a result
seasonality has a large impact on inventory management.
Agribusiness rms growing seed for future crops must predict
several years in advance to have the correct hybrids on hand
for agricultural producers.
Inventory management should minimize total inventory
costs by considering both carrying costs and opportunity costs.
The carrying costs of inventory include the cost of storage facilities and equipment, the interest cost of inventory investment, and shrinkage of inventory. The opportunity costs of
inventory are largely composed of missed sales due to insufcient inventory on hand to meet customer demands.
Inventory management can be complicated by the distribution channel. Given that each stage of the supply chain will
hold inventories, communication along the chain will be
critical in managing inventories of the sector.
65
Organizational structure
As a rm moves beyond an entrepreneurial owneroperator
size to a larger, more complex organization, frequently a corporate organizational structure emerges. The organizational
structure varies by rm needs, but typically there is a hierarchy
of responsibility and authority. At the top of the organizational structure is the President/Chief Executive Ofcer of the
rm, which is hired by a board of directors to lead all functions of the business. Many rms then organize the structure
around functional areas. They do so by having a senior manager (often with the title, vice-president) in charge of each
functional area, who would report to the CEO. Many of these
vice-presidents would have titles such as chief marketing ofcer, chief nancial ofcer, and chief operating ofcer, among
others. Additional members of the senior leadership team
would be added as specic to the rm, such as a vice-president
for human resources, vice-president for research and development, or a chief information ofcer. Firms might also have
each of these roles for signicant geographical areas or other
market segments. One potential drawback to this particular
structure is that the functional areas become silos that do not
collaborate well with each other.
For the largest organizations the structure might become
very complex. Each vice-president might have additional midlevel managers reporting to them that would be responsible
for specic divisions within the functional role. These midlevel managers are termed middle management and can serve
as a pool of candidates for senior leadership. Additional layers
of management may be added between senior management
and frontline employees (i.e., factory line workers, sales and
service representatives, etc.). The number of layers between the
president and frontline employees is an indication of whether
the rm has a vertical or at reporting structure. Vertical
structures are very hierarchical with clearly delineated reporting and authority relationships. Flatter structures tend to
empower lower-level employees to a greater degree, which
might negatively impact rm performance if the employees
make poor choices.
66
Leadership
As employees move from a frontline role up the organizational structure, they may become managers and acquire
direct reports. Direct reports are employees for whose actions
the manager is responsible. Becoming a manager requires
employees to develop a set of skills that will allow them to
motivate their direct reports to maximize productivity for
the rm.
Empirical studies by Lombardo and Eichinger at Korn/
Ferry International have led to the Lominger Leadership
Architect. This leadership development program identies 67
competencies that are part of eight factors and 21 clusters
(Figure 10). The eight factors are strategic skills, operating
skills, courage, energy and drive, organizational positioning
skills, personal and interpersonal skills, trouble with people,
and trouble with results. The clusters help to identify skills
that are closely related. Many of the competencies identied
in the Lominger Leadership Architect are closely related to the
development of the managers and executive leaders of food
and agribusiness rms.
Currently, little empirical research has been done in the
food and agribusiness industries to identify the application of
these principles. The opportunities are abound as there has
been documented need for additional human capacity to
manage and lead the food and agribusiness sectors. Some data
indicate, however, that an agribusiness talent gap exists and
that the demand for professionals in the sector exceeds the
amount of graduates from colleges of agriculture in the United
States (USDA National Institute of Food and Agriculture).
The USDA issued a report indicating that between 2010 and
2015 an estimated 54 400 jobs would be created annually
in agricultural, food, and renewable natural resources. Only
approximatey 29 300 students, however, are expected to earn
degrees in traditional agriculture and life science-related elds
during that same time span.
67
Energy
and drive
Focusing on the bottom line
Operating skills
Keeping on point
Getting work done through others
Getting organized
Managing work processes
Organizational
positioning
skills
Courage
Dealing with trouble
making tough people calls
Personal and
interpersonal
skills
Relating skills
Demonstrating personal flexibility
Acting with honor and character
Managing diverse relationships
Inspiring others
Being open and receptive
Balancing work and life
Caring about others
Strategic skills
Trouble
with people
Trouble
with results
Doesnt deliver results
too narrow
Figure 10 Library structure based on concepts from Lombardo, M., Eichinger, R.W., 1994. FYI: For Your Improvement, A Guide for Development
and Coaching, fourth ed. Lominger Ltd Inc.
opportunity to market and generate superior (or at least acceptable) nancial performance. Entrepreneurs are commonly
perceived as risk-takers they embrace new ideas and are
68
Table 3
University
Country
Purdue University
Kansas State University
University of Florida
Harvard University
Santa Clara University
Texas A&M University
Wageningen University
Zamorano
INCA
University of Sao Paulo
University of Buenos Aires
INSEAD
MAPP (Denmark Arhus School of Business)
Massey
University of Pretoria
Indian Institute of Management
Nanjing Agriculture University
USA
USA
USA
USA
USA
USA
The Netherlands
Honduras
Costa Rica
Brazil
Argentina
France and Singapore
Switzerland
Australia
South Africa
India
China
69
Establish the
Entrepreneurial Frame
Redesign
Redifferentiate
Resegment
Reconfigure
Build breakthrough
competences
Adaptive Execution
Define entry strategies
and likely competitive
response
Create discovery-driven
plans
Assess project progress
System integration
Farmer
needs
Discovery
Phase one
Phase two
Phase three
Phase four
Product concept
generation
Proof
of concept
Early
development
Advanced
development
Prelaunch
Launch with
customers
Positioning options
Stepping stones
High
Advanced auto
track/guidance/headland management
Variable rate seed/fertilizer/chemical
application
Synchronized and
autonomous/robotic
multiunit
operations
Medium
Platform launches
Power, tillage, and harvesting
equipment to residential, commercial
not for profit
Enhancement
audience
launches
Low
Technical uncertainty
Scouting options
Telematics
Information
management
Power, tillage,
and harvesting
equipment to
farmers (all sizes
and enterprises)
Low
Medium
High
Market uncertainty
Figure 13 Deere portfolio of innovations. Adapted from Boehlje,
M.D., Roucan-Kane, M., Broring, S., 2011. Future agribusiness
challenges: Strategic uncertainty, innovation and structural change.
International Food and Agribusiness Management Review 14 (5),
5382.
Conclusions
The purpose of this article is to discuss contemporary topics in
food and agribusiness with a focus on denition of agribusiness, description of the global agribusiness environment,
70
References
Aaker, D.A., 1995. Strategic Market Management. New York, NY: John Wiley and Sons.
Allen, R., 2004. How to interpret new demographic information in the preliminary
2002 census of agriculture release. Paper Presented at the 2004 Agricultural
Outlook Forum. Arlington, VA, February 1920, 2004. Available at: http://
ageconsearch.umn.edu/bitstream/33028/1/fo04al02.pdf (accessed 16.04.14).
Apgar, D., 2007. Risk Intelligence. Cambridge, MA: Harvard Business School Press.
Boehlje, M.D., 1999. Structural changes in the agricultural industries: How do we
measure, analyze and understand them? American Journal of Agricultural
Economics 81 (5), 10281041.
Boehlje, M.D., Roucan-Kane, M., Broring, S., 2011. Future agribusiness challenges:
Strategic uncertainty, innovation and structural change. International Food and
Agribusiness Management Review 14 (5), 5382.
Brigham, E.F., Ehrhardt, M.C., 2009. Financial Management: Theory and Practice.
Mason, OH: South-Western Cengage Learning.
Coase, R.H., 1937. The nature of the rm. Economica 4 (16), 386405.
Cooper, R.G., 2001. Winning at New Products: Accelerating the Process from Idea
to Launch, third ed. Reading, MA: Perseus Books.
Davis, J.H., Goldberg, R., 1957. A Concept of Agribusiness. Cambridge, MA:
Division of Research, Graduate School of Business Administration, Harvard
University.
Deming, W.E., 1982. Out of the Crisis. Cambridge, MA: The MIT Press.
Garvin, D.A., 1987. Competing on the eight dimensions of quality. Harvard Business
Review 65, 101109.
Gertner, J., 2008. Mad Scientist. Fast Company. February. Available at: http://www.
fastcompany.com/641126/mad-scientist (accessed 16.04.14).
Gray, A.W., Boehlje, M.D. 2005. Risk sharing and transactions costs in
producerprocessor supply chains. Choices, 4th Quarter, pp. 281286. Available
at: http://farmdoc.illinois.edu/policy/choices/20054/theme2/2005-4-13.pdf
(accessed 01.09.13).
Harrigan, K.R., 1988. Joint ventures and competitive strategy. Strategic Management
Journal 9 (2), 141158.
Iacobucci, D., 2001. Quantitative marketing research. In: Iacobucci, D. (Ed.), Kellogg
On Marketing. New York, NY: Wiley, pp. 195211.
Kotler, P., 1997. Marketing Management: Analysis, Planning, Implementation, and
Control. Upper Saddle River, NJ: Prentice Hall.
Lambin, J., 2000. Market-Driven Management. Houndmills, England: Macmillan Press.
McGrath, R.G., MacMillan, I.C., 2000. The Entrepreneurial Mindset: Strategies for
Continuously Creating Opportunity in an Age of Uncertainty. Boston, MA:
Harvard Business School Press.
Murcott, A., 1986. You are what you eat Anthropological factors inuencing food
choice. In: Ritson, C., Gofton, L., McKenzie, J. (Eds.), The Food Consumer. New
York, NY: Wiley.
Perreault, W.D., Cannon, J.P., McCarthy, E.J., 2010. Basic Marketing: A Marketing
Strategy Planning Approach, eighteenth ed. New York, NY: McGraw-Hill/Irwin.
Polanyi, M., 1962. Personal Knowledge. Chicago, IL: University of Chicago Press.
Roucan-Kane, M., 2010. How do food and agribusiness companies select their
product innovation projects? PhD Thesis, Purdue University, Agricultural
Economic Department.
Schumpeter, J.R., 1942. Capitalism, Socialism, and Democracy. New York, NY:
Harper and Brothers.
Sonka, S.T., 2011. JBS United and the Future: Too Many Opportunities. West
Lafayette, IN: Center for Food and Agricultural Business, Purdue University.
Sonka, S.T., Hudson, M.A., 1989. Why agribusiness anyway? Agribusiness 5,
305314.
Stern, L., El-Ansary, A., Coughlan, A., 1996. Marketing Channels, fth ed. Upper
Saddle River, NJ: Prentice Hall.
Teece, D.J., Pisano, G., Shuen, A., 1997. Dynamic capabilities and strategic
management. Strategic Management Journal 18, 509533.
Trejo-Pech, C., Weldon, R.N., Gunderson, M.A., House, L.A., 2009. The accrual
anomaly in the food supply chain. Agribusiness: An International Journal 25 (4),
113.
Williamson, O.E., 1979. Transaction-cost economics: The governance of contractual
relations. Journal of Law and Economics 22 (2), 233261.
Zoltners, A.A., Sinha, P., Zoltners, G.A., 2001. The Complete Guide to Accelerating
Sales Force Performance. New York, NY: Amacom.
Zook, C., 2010. Prot from the Core. Boston, MA: Bain and Company.
Agricultural Cooperatives
ST Buccola, Oregon State University, Corvallis, OR, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Equity subscription and redemption Procedures used to
determine each memberpatrons required annual capital
contributions to, and capital withdrawal entitlements from,
the cooperative.
Investor-owned rm A rm in which ownership and
control are proportionate to equity capital invested, rather
than according to use of the rms services.
Liquidity The ease or cost with which an investors capital
can be converted into cash.
New generation cooperative A marketing cooperative
structure stressing closed membership, transferrable
and appreciable stock shares, proportionality between
equity contribution and patronage, and well-dened
marketing contracts requiring as well as guaranteeing
member raw product deliveries on stated quantity and
quality terms.
Patronage The value of a members raw product supplied
to or inputs purchased from a cooperative, which is
calculated at estimates of the current market prices of the
products supplied or inputs purchased.
Pool The combined net revenue from the whole or a
subset of the cooperatives operations, which is allocable to
the members who contributed to that subset of operations.
Introduction
A cooperative is a business owned by the users of its services.
In particular, it is a rm whose net revenues are paid to the
rms patrons and on the basis of that patronage. The principal
alternative to a cooperative is an investor-owned rm one
owned by those who have invested capital in it, but who do
not necessarily patronize its services. An investor-owned rms
net revenues are paid to its equity holders in proportion to the
capital they invest rather than, as in a cooperative, according to
their patronage. Farmer cooperatives supply farmers with their
production inputs, process and market their products, and
sometimes provide other services such as price bargaining and
trucking. Hence, understanding cooperative organization is
essential to understanding the business of agriculture.
members at cost and to be controlled on a one-member-onevote basis. Services to members were to be provided at cost.
In modern cooperatives, democratic member control is still
regarded as an essential principle, although voting rights in
some rms are distributed according to the members patronage rather than on a one-person-one-vote basis. The principle of at-cost service also remains. This second principle
essentially means that the bulk of the cooperatives net income
is distributed (in cash or stock) as a return to patronage, in
turn requiring strict limits on the proportion of income distributed as a return to equity. Memberpatron control, service
at cost, and limited payments to equity capital are, then, the
basic elements of a cooperative rm.
Operation at Cost
Concept of a Cooperative
Cooperative Principles
Cooperative organization of economic activity has a long history, including the collective work efforts of early agricultural
societies. The rst group of individuals to organize as a modern
cooperative was the Society of Equitable Pioneers (1844), a
rm established in Rochdale, England to supply its 28 members
with weaving materials. Its purpose was to provide inputs to its
doi:10.1016/B978-0-444-52512-3.00125-X
71
72
Agricultural Cooperatives
Table 1
Cooperative costs
Wholesale cost of fertilizers
Operating costs
Per unit
$0.30
Per unit
$0.10
Total
$3000.00
Total cost
Total
$1000.00
Per unit
$0.40
Total
$4000.00
Retail price
$0.45
Patronage
$3150.00
Patronage refund
$350.00
Shipments to members
Member A
Units
3000
Member B
Retail price
$0.45
Total patronage
$1350.00
Units
7000
Member B
Patronage refund
$150.00
Patronage share
7000/10 000 70%
Agricultural Cooperatives
2001
83
32
45
19
13
83
43
38
19
13
Totala
31
28
Types of Function
Agricultural cooperatives in the US consist of supply, marketing, service, and bargaining cooperatives. Supply coops, illustrated in Table 1, provide members with farm inputs such
as machinery, fertilizers, pesticides, feed, and fuel. Marketing
coops assemble, process or handle, and sell members farm
products. Service coops provide trucking, storage, and other
services in which the member retains title to his farm commodity. An important form of service cooperative is the bargaining coop, which acts as farmermembers agents in
negotiating prices and other trade terms with farm product
buyers. Some cooperatives provide supply as well as marketing
services. Business volume in both supply and marketing cooperatives appears, in constant dollar terms, to have remained
approximately at from 1980 to 2005, and then risen after
2005. Marketing cooperative volume usually has been well
over twice that of supply cooperative volume, although since
2005 it has declined to just less than twice (US Department of
Agriculture, Rural Development Division, 2010).
Cooperatives are encountered frequently outside agriculture. Examples in the nancial sector are mutual insurance
companies, mutual savings banks, credit unions, group health
plans, stock exchanges, and boards of trade. In the housing
sector, they include community associations and condominiums and, in the consumer sector, utility cooperatives, food
coops, cooperative nursery schools, and buying clubs of various kinds. Such organizations are true cooperatives if they are
run democratically and refund net returns to members in
proportion to patronage. Mutual insurance companies, for
example, distribute prots in the form of dividends on customers policies.
Types of Centralization
An agricultural cooperative in the US is considered a local,
federated, centralized, or mixed one. Local cooperatives serve
farmers in a small area such as one or two counties. A federated cooperative is one whose members are local cooperatives.
A federated supply coop might engage in phosphate mining
Products marketed
Farm input
2001
Fertilizer
Petroleum
Crop protectants
Feed
Seed
44
44
32
21
10
45
46
34
15
13
Totalb
28
26
73
74
Agricultural Cooperatives
NARP
NMRP
S
S
F
G
H
J
NARP
NMRP
O
Agricultural Cooperatives
75
Cooperative Management
Pricing and Pooling
The cooperatives elected board of directors establishes
policy and oversees the activities and performance of hired
management. Board members usually are chosen on a rotating
basis at the annual meeting or by mail ballot. Issues about
which the board must decide include types of offered services,
pricing and pooling, nancial structure, credit, and member
and employee relations. The authors will consider pricing and
pooling in the next two paragraphs. The context used is again
that of a marketing cooperative.
A few marketing cooperatives credit a member with the
full market value of raw product on its delivery to the coop
for processing or handling. This market value is then debited,
along with other costs, from the cooperatives revenue to
determine the net margins that will be allocated back to
the member on a patronage basis. Coops that operate this
way may be termed buy/sell coops. Pooling cooperatives
are those which do not credit members with the market
value of their raw products on delivery and which, therefore,
do not debit raw product value from the returns eventually
allocated back to members on a patronage basis. In either
event, part of the members allocation usually is paid in cash,
part in equity certicates. If raw products are homogeneous
across members, the decision whether to credit a member on
delivery with the market value of his/her product does not
affect the sum of payments he/she will receive from the
cooperative.
A complicating factor is that most cooperatives deal in
heterogeneous products, either in the sense of various grades
of the same commodity or of various commodities. Such
grades and commodities can, for payment purposes, be
grouped in any way the cooperative chooses. Let Pj be the perunit valuation (often the raw-product market price) of the jth
raw product, Qj the quantity of j supplied by members, and Rj
its per-unit resale revenue in the nal product market less the
cooperatives per-unit operating cost (including any member
credits at delivery time). Assume the rm operates a number of
separate pools and let Jk represent the subset of the rms
products included in the kth pool. The cooperatives per-unit
payment to members for the jth raw product shipped to the
kth pool is (Buccola, 1991):
h
1 i
Jk Rj Qj
Unit payment Pj Jk Pj Qj
76
Agricultural Cooperatives
Taxation
The Revenue Act of 1913, which established income taxation
in the US, exempted agricultural and horticultural associations from income tax. The argument was that such associations allocate most of their net earnings to individual
members and hence do not earn a prot as corporate entities.
Plan name
Description
Age of patron
38
30
50
43
58
45
17
13
Estate settlement
Revolving fund
Percentage pool (% of
all equities)
Base capital
Because cooperatives often simultaneously use more than one equity redemption method, percentages do not sum to 100.
Source: Reproduced from US Department of Agriculture, Rural Development Division, 2010. Cooperative equity redemption. Rural Business Cooperative Programs, Research Report
220. Washington, DC: US Department of Agriculture.
Agricultural Cooperatives
Table 4
77
78
Agricultural Cooperatives
Free riding is encountered most likely when coop membership is heterogeneous or the rm operates away from the
maximum point on its net average revenue product (NARP)
curve. At cooperative volume OC in Figure 1, the additional
cooperative net margin created by one more unit of raw
product is vertical distance OJ (height of the NMRP function
above C). If net margins are distributed in proportion to
patronage, the same extra unit instead will be paid the greater
amount CI (height of the corresponding NARP function).
Hence, other members subsidize that last unit by amount JI.
Any side payments to nullify such subsidies tend to be divisive. For this reason, a cooperatives success depends partly on
the degree of cooperative spirit among the members, including
certain individuals willingness to bear an excess share of the
total burden (Cechin et al., 2013).
The third or agency problem is that, on account of the
traditional cooperatives one-person-one-vote rule, those with
little capital in the cooperative have, besides equal per-dollar
benet of the rms services, equal control of the policy decisions. This disproportionality between investment and voting
power discourages large-volume patrons from participating
because the interests of smaller patrons typically differ from
those of larger ones (Pozzobon and Zylbersztajn, 2013). Finally, an information or oversight problem is created by the
absence of cooperative stock from public exchanges. Public
stock prices encapsulate outsiders judgments about a rms
nancial health, which can be used, for example, to determine
executive salaries. If such a piece of information is absent, cooperative members must rely on their own direct evidence,
such as operating statements and balance sheets, to assess
management performance. Perusals of that sort are usually
impractical they involve high monitoring costs.
All four of the above problems arise because member
property rights in a cooperative are poorly dened. In particular,
the member has an inadequately dened: (1) claim to the cooperatives net income and (2) control over the cooperatives
assets over its investments, contracts, and business policies
(Chaddad and Cook, 2004). The control problem is connected,
as already seen, to the disproportionality between a members
investment and voting rights (Chaddad and Iliopoulos, 2013).
Analysis of the net-income issue is more complicated. Four
aspects of a members net-income claim (cooperative stock
share) can be distinguished: whether the claim is: (1) restricted
to member patrons, (2) redeemable from the cooperative, (3)
transferrable to other individuals, or (4) appreciable in value. In
traditional cooperatives, income claims are restricted to member patrons, redeemable only with board approval, and nontransferable. They also are nonappreciable, that is, their value
cannot change with the rms protability. The members
property rights are, in short, weak and unclear, severing members interests from the rms interests. In most cooperatives, as
already seen, a members net return share is not even held
proportionate to his/her share of the rms capital, although
some capital contribution plans do ensure such proportionality.
Agricultural Cooperatives
79
prot. The cooperative entrant worries only about its potentially depressing inuence on nal-product prices because any
raw-product price change would be passed on to farmer
members in the form of higher farm revenue. Thus, the threat
of a cooperatives entry is more credible than of an IOFs entry,
implying that the freedom to form a cooperative is an especially potent force toward market efciency.
Summary
The cooperative or user-owned way of organizing an agricultural services rm is fundamentally different from the
investor-owned way. In the former, net returns are paid to
the farm products supplied to or inputs purchased from the
rm. In the latter, net returns are paid to the capital. Efforts
to keep cooperative members capital investments proportionate to the values of their product supplies or input
purchases are difcult to implement. And their implementation moves the organization in the direction of an investorowned model.
Because a farmers products and input uses are far less
mobile than his/her capital potentially is, user-based control
of a services rm is much less exible than capital-based
control. Farmer capital can quickly be moved from Brazilian
sugar rening to Canadian phosphate mining. The farms own
sugarcane production and phosphate use cannot. This difference lies at the heart of the allocative inefciencies to which
cooperatives are prone, and explains why cooperatives tend to
fail when investment markets are widespread and liquid.
Such a competitive ideal can, however, never be fully realized in given situations. Regulation often pushes prices above
the competitive norm or below what attracts enough supply.
The scale of investor-owned marketing or input services often is
inadequate, especially in low-population areas or, especially,
when the services are new, innovative, or specialized.
Cooperatives then arise to protect members from these government and capital failures.
Yet the cooperative itself is an element of the market system, as one can see from the coops enhancement of competition even in the face of being injured by it. The rise of
vertical integration a contract-specic relationship between
two rms that bypasses the more anonymous marketplace is
a case in point. Being supplier- or buyer-owned, a cooperative
is itself an instance of vertical integration and therefore a
natural part of market development. Governments declining
use of cooperative federations as agents of farm subsidies more
likely underscores this essentially market nature of cooperative
organization.
References
Barton, D.G., Schmidt, R.L., 1988. An evaluation of equity redemption alternatives in
centralized cooperatives. Journal of Agricultural Cooperation 3, 3958.
80
Agricultural Cooperatives
Relevant Websites
http://accc.k-state.edu/index.html
Arthur Capper Cooperative Center, Kansas State University.
http://www.uwcc.wisc.edu
Center for Cooperatives, University of Wisconsin.
http://www.uwcc.wisc.edu/pdf/staff%20papers/staff%20paper%207.pdf
Center for Cooperatives, University of Wisconsin, Summary of Recent State
Statutes Authorizing Limited Cooperative (New Generation) Associations.
http://usaskstudies.coop
Centre for the Study of Cooperatives, University of Saskatchewan.
http://www.cobank.com
CoBank, US Nationwide Cooperative Bank.
http://www.rurdev.usda.gov/rbs/pub/sr22.htm
Directory of Farmer, Rancher, and Fishery Cooperatives 2010.
http://www.ica.coop
International Cooperative Alliance.
http://accc.k-state.edu/ncera210/index.html
Journal of Cooperatives, Kansas State University.
http://www.nonghyup.com/eng/main/main.aspx
National Agricultural Cooperative Federation (NACF), Korea.
http://www.ncfc.org/about-ncfc/about-ncfc
National Council of Farmer Cooperatives.
http://www.copac.coop/
UN Committee for the Promotion and Advancement of Cooperatives.
http://social.un.org/index/Cooperatives.aspx
UN Cooperatives Webpage.
http://social.un.org/index/Home/tabid/40/news/339/Default.aspx
UN Social Policy and Development Division.
http://social.un.org/coopsyear/global-launch.html
UN Year of Cooperatives.
http://www.rurdev.usda.gov/BCP_Coop_DirectoryAndData.html
USDA, Cooperative Directory and Data.
http://www.rurdev.usda.gov/BCP_Coop_RurCoopMag.html
USDA, Rural Cooperatives Magazine, Bi-Monthly.
http://www.rurdev.usda.gov/LP_CoopPrograms.html
USDA, Rural Development, Cooperative Programs.
Glossary
Analytical agricultural ethics The review and
investigation of concepts, arguments, and implicit norms as
they are deployed in developing an understanding of
agricultural practice.
Burdens of proof The criteria that must be met for a
particular ethical judgment to be made or reversed.
Communitarianism A philosophical approach that
emphasizes the importance of tradition, the fundamental
role that a society plays in forming political and moral
reasoning, and the slow change of culture.
Consequentialism A philosophical approach that
stipulates that all human actions be justied solely in terms
of their consequences or effects on others' welfare.
Ethical reductionism A philosophical approach where
ethical concepts are reduced to statements about individual
and subjective experiences; it promotes a strong division
between fact and value.
Ethics The systemization and defense of values, standards,
and conceptions that are used to make ethical judgments
regarding human conduct.
Food deserts Urban areas with limited access to nutritious
foods that are often disproportionately made up of poor
socioeconomic classes and minority communities.
Food security The establishment of market-based
mechanisms meant to ship food to other areas experiencing
scarcity.
Food sovereignty A broader conception of food that
moves away from market-based systems where human
rights concerns are bound up within the food systems
themselves.
Informed consent Occurs when parties (that must bear
risks) voluntarily agree to do so under conditions of full
disclosure; when informed consent is lacking, even low-level
benecial risks may be rejected.
Justice The terms ethics and justice are often used
interchangeably, as there is no standard method to
distinguish between the two. However, justice is commonly
dened in two ways within philosophical traditions. First,
traditional philosophers, such as Plato, used the word
justice to indicate a personal or individual virtue. Second,
philosophers such as John Rawls and Ronald Dworkin
argued that the locus or the appropriate place of justice is
Introduction
The word ethics is often used interchangeably with the word
morality to indicate goals, norms, and values that are taken to
guide human action. A common, but far from universal, distinction is to dene ethics as the systematic study of moral
doi:10.1016/B978-0-444-52512-3.00128-5
81
82
possible to provide considerably more explicit, locally coherent, and rigorous arguments on goals, norms, and values
than are typically found in ordinary life.
Agricultural ethics is the criticism, analysis, and justication
of systematic moral codes and the acceptability of social norms
that exist or are applied to practices of food and ber production, distribution, and consumption. Given this denition,
agricultural ethics can be understood as an interdisciplinary
research and education area. Research and teaching on ethics
take place to some degree in all disciplines of the social sciences
and humanities, although some practitioners of these disciplines have disavowed work on ethics. The most typical disciplinary home for work in ethics has been philosophy, although
departments of theology, religious studies, and political science
also typically have specialists in ethics. Recent work in agricultural ethics emphasizes (1) unintended health, safety, and
environmental impacts of agricultural technology; (2) the
structure of agriculture, including distribution of benets from
agricultural production; and (3) questions of conduct, character, and professional ethics. In addition, special attention has
been given to the moral standing of agricultural animals and to
ethics as it relates to agricultural biotechnology. Depending on
the ethical framework utilized by specic theorists working in
this eld, the above topics can also be framed as justice issues.
As is illustrated below, the ethics of agriculture and justice are
tightly linked.
Agricultural Ethics
Broadly speaking, ethics (also known as moral philosophy) is
the systemization and defense of values, standards, and conceptions that are used to make ethical judgments regarding
human conduct. Ethicists study how people should act and
ethical norms are understood to be implicitly found within
cultural practices, grounded in psychology, and able to be
discovered through reason. Here ethical norms are understood
to be an accessible part of the world. This branch of philosophy
can, roughly, be divided into three major areas: metaethics,
normative ethics, and practical ethics. Metaethics attempts to
understand the presuppositions and logical structure of ethical
properties, attitudes, and judgments (Sayre-McCord, 2012).
This branch can be understood as a broader (or meta) analysis
of ethics. In contrast, normative ethics is the development of
general principles or standards that make particular actions
right or wrong and the creation of theories that explain why
some choices are better than others. This branch of ethics maps
on well to the general denition given above and is often what
is meant when the word ethics is used without qualication.
Engaged or practical ethics also focuses on determining right
action but specically with respect to real life situations.
Sometimes engaged ethics not only involves the application of
ethical theories to particular cases, but it also includes the
derivation of ethical norms from specic contexts and integration with factual matters that can signicantly inuence the
content and meaning of a normative claim or judgment.
Although metaethics is an important subeld, normative
ethics and engaged ethics are of particular importance for
those attempting to better understand agricultural science,
technology, and farming methods. The following two
83
become topics for symposia at disciplinary meetings of agricultural scientists and at consensus conferences intended to
establish priorities for research and for policy change. Attempts
to extend work on ethics to producer groups have thus far been
limited. Although agricultural ethics remain somewhat marginal in the agricultural disciplines, the role of ethics in curriculum, research, and public policy has been increasingly
accepted. Today both analytic agricultural ethics and substantive agriculture ethics are blooming with many agricultural
ethicists making use of historical ethical frameworks, such as
(1) rights-based ethics, (2) consequentialism, (3) communitarianism, and (4) environmental ethics.
84
85
In addition, many of these ethics and competing conceptions of justice are being blended and incorporated as
citizen movements apply them on the ground. For example, as
partially illustrated above, the local food movement utilizes
communitarian, rights-based, and radical conceptions of justice. It utilizes communitarianism due to the fact that, within
this movement, people are understood to be deeply imbedded
in local contexts and just actions, be that to others or to the
land, can be distilled from the traditions of specic societies or
traditions. It utilizes an expanded liberal conception of justice,
as it includes a mandate for the just distribution of resources.
Finally, it also incorporates radical conceptions of justice, as it
expands the sphere of moral patients to include the surrounding environment, and conceptualizes food systems as
regenerative or guided by principles of ethics, equity, and
ecology. Thus, ethics and understandings of justice are not
static but are social constructs and are thus constantly in the
process of transformation and change.
Although an understanding of agricultural ethics can be
gained through the analysis of the ethical frameworks utilized
by the eld, it is important to recognize themes emphasized by
recent work. Such themes include (1) unintended health,
safety, and environmental impacts of agricultural technology;
(2) the structure of agriculture, including distribution of
benets from agricultural production; and (3) questions of
conduct, character, and professional ethics. These themes form
the topics of the following sections.
Unintended Consequences
Many criticisms of modern agriculture have noted unwanted
and unintended consequences of agricultural chemicals.
Pesticides have had documented effects on wildlife populations, and some are known carcinogens. Nitrogen fertilizers
can pollute groundwater and surface water. Many agricultural
chemicals have long been known to have toxic effects when
improperly handled, stored, or applied. It is clear that neither
manufacturers nor producers intended or wanted these consequences, and both groups have made efforts to mitigate and
control unintended consequences. Nevertheless, unintended
consequence of agricultural chemicals pose ethical problems
in that it is impossible to eliminate the risk of an unwanted
event entirely. Furthermore, there is often disagreement about
the degree of risk associated with agricultural chemicals. Some
individuals express far greater concern about exposure to
pesticides than others. Producers, scientists, and chemical
manufacturers thus face the problem of managing concern for
unwanted effects, even when the empirical evidence for such
effects is scant, controversial, and even nonexistent. Whether
real or imagined, unwanted consequences of chemical have
signicantly affected the reception of many agricultural technologies, including mechanization and biotechnology, among
producers and food consumers since 1962.
An analysis of ethical issues associated with unintended
consequences surveys the assumptions and implicit norms
that have guided action contributing to the unintended outcomes. Public claims expressing a rationale or justication of
such action are scrutinized, and the pattern of reasoning is
exposed. In many cases, disagreement over agricultural
86
Structure of Agriculture
Ethical issues associated with the structure of agriculture
overlap with those of unintended consequences to the extent
that changes in the size distribution or number of farms can be
understood as an unwanted consequence of technological
change. The general relationship between means of agricultural production and norms for land entitlement and
property rights has, however, been an enduring philosophical
question. As noted above, Aristotle thought that achievement
of moral virtue among the elite of society depended on a release from labor of agricultural production that could only be
provided through a system of agricultural production based on
human slavery. In the eighteenth century, John Locke defended the enclosure movement that removed English lands
from common pastoral use and converted them into privately
controlled croplands on the grounds that enclosure returned
far more benets in the form of increased food availability. At
about the same time, Jean Jacques Rousseau argued that the
primary impact of privatization of agricultural lands was to
87
88
89
Animal Well-Being
The legal and ethical protection of animals has a long standing
in the United States. Anticruelty statutes were enacted in some
colonies before the Revolutionary War. More recently, animal
protectionists have noted concern for the well-being of farm
animals in connement settings, especially since the publication of Ruth Harrison's Animal Machines in 1966. However,
the principal focus of the recent animal rights movement has
been to oppose the use of animals in product testing and
biomedical research. The biomedical debate has become quite
acrimonious, with some parties on both sides taking extreme
positions. Few in ethics would deny that caregivers have ethical
responsibilities to assure well-being of farm and food animals.
Farmers and ranchers have traditionally been thought to be
especially respectful of the well-being of food and farm animals. They have been thought to possess personal moral
concern for animals. Also, animal health and well-being have
been thought to correspond closely to a producer's interest in
efciency and marketability of animal products. The correlation between producer and animal interests fails to obtain
when any one of three conditions obtains. First, some products, such as foie gras or pale veal, may require production
methods contrary to animal well-being. Second, some elements of animal well-being may be realizable only under ideal
conditions seldom realized in either wild or domesticated
settings. Third, with large operations or high stocking rates, the
management costs of attending to the needs of a few individual animals will not always be matched by returns based on
average or aggregated sales of animal products. Animal protection organizations have criticized agricultural producers on
each of these three points. The political rhetoric of the animal
experimentation debate inuences criticisms of agriculture,
and ambiguous terminology presents a barrier to any clear
presentation of ethical issues. Multiple uses for the terms
animal welfare and animal rights are especially confusing. For
some, the term animal rights implies an extreme reformist
position, whereas animal welfare is taken to imply an attitude
favoring moderate or no reform in animal agriculture. Popular
use suggests that those who express support for animal rights
merely feel that individual animals' interests deserve consideration and do not propose radical change in animal agriculture. More formal uses of these terms have been introduced
into the literature by two inuential philosophers, Peter Singer
and Tom Regan.
Peter Singer advocates an animal welfare philosophy in a
series of articles and in his book Animal Liberation. Singer is a
utilitarian philosopher who believes that the morality of an
action is to be evaluated by assessing its consequences. The key
to the animal welfare philosophy is the belief that comparable
interests deserve equal consideration without regard to species.
This means that comparable experience of physical pain, for
example, would be given equal consideration without regard
to whether the pain is experienced by a pig, monkey, or a
human being. Singer explicitly notes that many interests do
not admit of meaningful cross-species comparisons and that
the complex cognitive interests of human beings establish
bases for evaluating consequences to humans in a manner that
is unparalleled for other species. Hence, Singer's view admits
of many opportunities in principle where human interests are
90
Agricultural Biotechnology
The rapid growth of recombinant deoxyribonucleic acid
(DNA) transfer techniques and their application to agricultural
science have created a situation in which agricultural
biotechnologies present excellent case studies for many of
the ethical issues discussed above. Unintended consequences
of agricultural biotechnology have stimulated the most
References
Bell, D., 2012. Communitarianism. In: Zalta, E. (Ed.), The Stanford Encyclopedia of
Philosophy. Spring 2012 ed. Available at: http://plato.stanford.edu/archives/
spr2012/entries/communitarianism/ (accessed 15.01.14).
Cranston, M., 1967. Liberalism. In: Edwards, P. (Ed.), The Encyclopedia of
Philosophy. New York, NY: Macmillan and the Free Press, pp. 458461.
Dahlberg, K., 1993. Regenerative food systems: Broadening the scope and agenda of
sustainability. In: Allen, P. (Ed.), Food for the Future. New York, NY: Wiley,
pp. 75102.
DeLind, L.B., 2011. Are local food and the local food movement taking us where we
want to go? Or are we hitching our wagons to the wrong stars? Agriculture and
Human Values 28, 273283.
Dworkin, R., 1996. Do liberty and equality conict? In: Barker, P. (Ed.), Living as
Equals. New York, NY: Oxford University Press.
Gaus, G., Courtland, S., 2010. Liberalism. In: Zalta, E. (Ed.), The Stanford
Encyclopedia of Philosophy. Fall 2010 ed. Stanford, CA: The Metaphysics
Research Lab, Center for the Study of Language and Information, Stanford
University.
Gaus, G.F., 1996. Justicatory Liberalism: An Essay on Epistemology and Political
Theory. New York, NY: Oxford University Press.
Leopold, A., 1966. A Sand County Almanac. New York, NY: Oxford University Press.
MacIntyre, A., 1984. After Virtue. South Bend, IN: University of Notre Dame Press.
Rawls, J., 2001. Justice as Fairness: A Restatement. Cambridge, MA: Harvard
University Press.
Regan, T., 2003. Animal Rights, Human Wrongs. Oxford, UK: Rowman & Littleeld
Publishers.
Sandel, M., 1981. Liberalism and the Limits of Justice. Cambridge, MA: Cambridge
University Press.
91
Sayre-McCord, G., 2012. Metaethics. In: Zalta, E. (Ed.), The Stanford Encyclopedia
of Philosophy. Spring 2012 ed. Available at: http://plato.stanford.edu/archives/
spr2012/entries/metaethics
Schanbacer, W., 2010. The Politics of Food: The Global Conict between Food
Security and Food Sovereignty. Santa Barbara, CA: Praeger Security International.
Schrader-Frechette, K., 1999. Risk and Rationality: Philosophical Foundations for
Populist Reforms. Berkeley, CA: University of California Press.
Sen, A.K., 1987. On Ethics and Economics. Oxford, UK: Basil Blackwell.
Sen, A.K, 2000. Development as Freedom. New York, NY: Anchor Books.
Sen, A.K., 2009. The Idea of Justice. Cambridge, MA: Harvard University Press.
Sinclair, U., 2012. The Jungle. New York, NY: Simon and Brown.
Smith, K.K., 2003. Wendell Berry and the Agrarian Tradition: A Common Grace.
Lawrence, KS: University of Kansas Press.
Taylor, C., 1989. Sources of the Self: The Making of the Modern Identity.
Cambridge, MA: Cambridge University Press.
Thoreau, H.D., 2004. A week on the Concord and Merrimack rivers (Edited by
Hovde, C.F., Howarth W.L., Witherell, E.H.). Princeton, NJ: Princeton University
Press.
Warren, K.J., 2000. Ecofeminist Philosophy. Lanham, MD: Rowman and Littleeld
Publishers.
Relevant Website
http://kelloggchair.anr.msu.edu/
W. K. Kellogg Foundation.
Agricultural Finance
PN Ellinger, University of Illinois, Urbana, IL, USA
JB Penson Jr., Texas A&M University, College Station, TX, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Agribusiness Refers to farm input supply rms, food
processing rms, ber manufacturing rms, and other rms
in the nations food and ber system other than crop and
livestock producers.
Credit scoring Approach used by lenders to quantitatively
evaluate the credit worthiness of a borrower.
Farm Credit System System of federally chartered,
privately owned banks, and associations that lend primarily
to agricultural producers and their cooperatives.
Farm Service Agency Governmental agency involved in
direct lending and loan guarantees to creditworthy
borrowers that may have a difcult time obtaining nancing
from commercial sources.
Financial intermediaries Entities that obtain loanable
funds from savers in the economy and then lend these funds
to borrowers.
Food and ber industry Network of input supply rms,
crop and livestock producers, food processing rms, ber
Introduction
The eld of agricultural nance encompasses a broad range of
interest ranging from micro issues associated with rm-level
investment and nancing decisions made by crop and livestock producers as well as agribusiness rms to macro issues
associated with the effects that macroeconomic policy, farm
commodity policy, resource policy, and international trade
policy have on the nancial structure and performance of the
nations food and ber system.
Microagricultural Finance
Topics in microagricultural nance include concepts of investment and nancing decisions under both certainty and
uncertainty, including the methods used to evaluate investment projects and alternative approaches to acquiring these
resources.
92
doi:10.1016/B978-0-444-52512-3.00109-1
Agricultural Finance
93
C1
P1
Utility (C1)
U2
C1
U1
B
Utility (C0)
C
A
C0
P0
C0
94
Agricultural Finance
Expected
return
Risk
Figure 3 Indifference curves and attitudes toward risk. Indifference
curves between risk and return for risk adverse investors. Preference
is upwards and to the left.
Agricultural Finance
adjusted discount rate. The certainty equivalent criterion involves selecting the decision alternative with the highest certainty equivalent. This criterion incorporates the risk aversion
of the decision maker. However, the values that are used to
estimate a decision makers utility function and certainty
equivalent are subject and difcult to estimate quantitatively.
95
Leasing
Resource Acquisition in Agriculture
The nancial barriers to enter production agriculture have increased. Ination, technological change, and increases in farm
size have been the primary causes of the increased capital requirements. The combination of increasing capital requirements and low prot margins restricts crop and livestock
producers in their capacity to acquire control of the land,
machinery, livestock, and other resources necessary to compete. The increased capital requirements also limit growth.
Crop and livestock producers are evaluating and using alternative methods of resource control and management.
Sources of funds used to acquire control of resources can be
broadly classied as debt and equity capital. The degree to
which that debt capital is used by a producer is a key issue. Tax
deductibility and cost usually favor the use of debt capital over
equity capital, whereas administrative and bankruptcy costs
increase as the proportion of debt capital increases. Thus,
theoretically each decision made may have an optimal equilibrium combination of debt and equity.
Equity capital
The primary source of equity capital in production agriculture
is through retained earnings or surplus prots kept in the
business. Other common sources of equity capital have resulted from gift and inheritances from previous generations
and pooling of equity capital through partnerships or
corporations.
There are two types of partnerships common in agriculture:
general partnerships and limited partnerships. With general
partnerships, each partner is explicitly involved in both ownership and management. Furthermore, each partner has unlimited liability for obligations incurred by the business and
the liabilities incurred by other partners. Limited partnerships
are comprised of limited and general partners. The liability of
the limited partners is restricted to the investment in the
business.
The corporation is a legal entity held as share or claims on
the net worth and prot stream of the business. Although
partnerships and sole proprietors dissolve on death, corporations permit continuity over generations. Two types of corporations are important in agriculture: Subchapter S and
Subchapter C. A Subchapter S corporation is limited to 35
stockholders and taxed as a partnership. With the Subchapter S
corporation, all prots are allocated to the stockholders for
income tax purposes. A Subchapter C corporate stockholder
must pay taxes only on the cash dividends received and thus
this entity may offer some income tax incentives for high-taxbracket stockholders.
Many corporations and partnerships are created for the
purpose of pooling family equity capital. However, public and
private placements of equity shares in production agriculture
Contract production
Agriculture has witnessed strong trends toward increasing
specialization and coordination at the various stages of the
production cycle. The coordination may be with successive
stages in production and distribution (vertical) or between two
or more units of production within the same economic stage
(horizontal). Vertical integration of input suppliers, processors, and distributors is becoming more common in agriculture. An increasing proportion of assets used in the farming
sector is being supplied or nanced by input suppliers, processors, and distributors. Vertical integration of vegetable and
fruit industries has been in existence for a long time. Livestock
industries, such as poultry and hogs, are also becoming more
vertically coordinated. A producer may be able to shift price
and yield uncertainties to the contracting rm with vertical
coordination. However, future contractual arrangements create
additional uncertainties.
Debt capital
Debt capital are funds acquired from nancial intermediaries.
Costs include interest costs, fees, and closing costs. Interest costs
are fully tax deductible and thus typically carry a lower cost than
equity capital. Debt capital is typically distinguished between
operating debt and term debt. Operating debt is used to nance
the purchase of operating inputs, whereas term debt is often
used to nance depreciable assets and farm real estate. Operating debt is typically repaid during the production cycle,
whereas term debt is paid over several years.
96
Agricultural Finance
Accounting practices
In conjunction with the 1987 Agricultural Credit Act, a presidentially appointed commission on agricultural nance emphasized the need for greater standardization of nancial
reports and analysis of the farm industry. As a result, the
Agricultural Division of the American Bankers Association
formed a task force of representatives from lending institutions, academic institutions, regulatory agencies, computer
software rms, the farm management consulting industry, and
the accounting industry. The Farm Financial Standards Task
Force, renamed to Farm Financial Standards Council (FFSC),
provided guidelines regarding the reporting of nancial information for farm and ranch businesses.
The four nancial statements recommended by the FFSC
include the following: (1) the balance sheet, (2) the income
statement, (3) the statement of cash ows, and (4) the statement of owner equity. These four statements are linked to
provide a business (assets) and the levels of debt and equity
used to acquire the assets. The income statement is a summary
of the revenue and expenditures of the business over a specied period of time. The statement of cash ows is a detailed
summary of the cash inows and outows over a specied
period of time. The cash inows and outows are separated
according to operating, nancing, and investment activities of
the rm. The statement of owner equity reconciles the change
of equity from one period to the next.
Each of these statements may be prepared on a historical
basis or a pro forma (projected) basis. These nancial statements organized the data needed to analyze the risk and
performance of the business. The primary areas of analysis
include solvency, protability, liquidity, repayment capacity,
and nancial efciency. Solvency measures the level of debt
relative to the equity capital or the overall capital of a business.
Protability is the ability of the rm to generate earnings,
whereas liquidity relates to the rms capacity to generate cash
to meet nancial commitments without loss of value. Repayment capacity measures related cash generated by the operation to cash obligations of the rm. Financial efciency
measures refer to the utilization of assets within the business.
Other nancial efciency measures relate operating and nancing expenses to total production.
borrowers and loans from the highest credit default risk to the
lowest.
Risk rating models have been developed through lenders
experiences as well as statistical methods. The lender experience models are formulated by lenders based on historical
observations of variables that are related to overall loan performance. Statistical development of risk rating models involves the mathematical representation of a group of
subjective and objective independent variables into an equation that determines the credit worthiness of a business. The
objective variables often include collateral value, nancial
ratios, production efciency measures, and trend values of nancial measures. Management ability is a common subjective
measure included in risk rating models. The applications of
risk rating models include determination of credit acceptance,
loan pricing based on riskiness of the loan, establishment of
loan loss provisions, and loan portfolio monitoring. The dependence on the model results varies among lenders. In some
cases, model results are used as the sole determinant in the
decision process, whereas other lenders use the results in
conjunction with other criteria.
The statistical approaches used to determine the variables
and their respective coefcients include linear regression, discriminant analysis, and logistic regression. The independent
variables include various nancial, economic, and subjective
variables, whereas the dependent variable is a measure of
historical loan performance. In general, results indicate that
the independent variables selected and their respective coefcients differ substantially across studies and are very sensitive to the data sample.
Agricultural Finance
Role and performance of the farm credit system
Institutions in the Farm Credit System are federally chartered
and privately owned. One objective of the charter is to improve the income and well-being of crop and livestock producers by furnishing competitively priced credit and related
services to creditworthy borrowers through all economic
conditions.
The primary sources of funds for the Farm Credit System
district banks are obtained through the sale of system-wide
securities in the national nancial markets. The Federal Farm
Credit Bank Funding Corporation is responsible for selling
the securities. The securities are treated as Governmental
Agency Securities and trade at 2050 basis points above US
Treasury securities. Equity capital of the various cooperatively
controlled banks and associations is obtained by sale of stock
to borrowers and through retained earnings. The banks are
regulated by the Farm Credit Administration.
During the early 1980s, the Farm Credit System experienced severe nancial problems. The systems capital and
surplus declined to more than US$6.1 billion in 1985 and
1986. The problem involved loan losses resulting from producers nancial problems as well as lowering net interest
margins. The Farm Credit System held a large volume of longterm securities at high interest rates whereas current market
rates on loans were low. As a result, in December of 1987, the
US Congress passed the Agricultural Credit Act of 1987. The
major provisions included restructuring options of the Farm
Credit System, federal nancial assistance, greater exibility in
capitalizing the system, and creation of an insurance fund.
Currently, the Farm Credit System institutions have restored the soundness of their operations: restructuring of the
Systems banks and lending associations is continuing as these
institutions seek great efciency and risk-bearing capacity in
their lending operations. On 1 January 1988, there were 12
districts with a total of 377 associations. On 1 July 2013, there
were 4 districts and 82 associations. The impact the corporate
restructuring of the Farm Credit System has on the delivery of
debt capital to farm and ranch borrowers has also received
considerable interest among policy makers, academicians,
credit institutions, and borrowers themselves.
97
98
Agricultural Finance
Government lending
As an agency of the US Department of Agriculture, the FSA
serves as a source of debt capital for rural Americans. The FSA
originates loans and guarantees loans to qualied applicants
who have experience in farming and ranching, who are the
owners or operators of a farm or ranch at the time of borrowing the loan, and whose livelihoods depend on farming or
ranching.
Concerns have surfaced regarding government subsidies
that have focused increased interest on reducing FSA direct
lending and increasing its emphasis on loan guarantees. Loan
guarantees transfer the funding and loan administration to
private lenders and provide greater exibility in loan pricing.
Macroagricultural Finance
The second major area of emphasis in agricultural nance reects an aggregate or macro view of the economic performance and nancial structure of the nations farms and ranches
and their relationship to other sectors in the general economy.
Information on macroagricultural nance developments is of
interest to macroeconomic policy makers, farm commodity
policy makers, nancial institutions and their regulators,
agribusinesses, and rural development specialists.
Agricultural Finance
$140
$120
Billion dollars
$100
$80
$60
$40
$20
2012
2009
2006
2003
2000
1997
1994
1991
1988
1985
1982
1979
1976
1973
1970
$0
16.00%
14.00%
12.00%
10.00%
8.00%
6.00%
4.00%
2.00%
2012
2010
2006
2008
2004
2002
2000
1998
1994
1996
1992
1990
1988
1986
1984
1982
1980
1978
1976
1974
1972
1970
0.00%
$140
$120
Billion dollars
$100
$80
$60
$40
$20
With payments
Figure 6 Importance of government payments.
Without payments
2012
2009
2006
2003
2000
1997
1994
1991
1988
1985
1982
1979
1976
1973
1970
$0
99
100
Agricultural Finance
$3000
Billion dollars
$2500
$2000
$1500
$1000
$500
2012
2009
2006
2003
2000
1997
1994
1991
1988
1985
1982
1979
1976
1973
1970
$0
$3000
$2500
$2000
$1500
$1000
$500
2010
2008
2006
2004
2002
2000
1998
1996
1994
1992
1990
1988
1986
1984
1982
1980
1978
1976
1974
1972
1970
$0
Agricultural Finance
101
0.25
0.20
0.15
0.10
0.05
2012
2009
2006
2003
2000
1997
1994
1991
1988
1985
1982
1979
1976
1973
1970
0.00
Research applications
The information contained in the US Department of Agricultures sector economic accounts and related data sets is not
only useful in current situation analysis but also represents a
major source of data for research designed to project the effects
that a broad range of macroeconomic, farm commodity, and
international trade policies can have on the economic growth
and nancial performance of agriculture. Researchers dating
back to the early 1950s have been developing statistical-based
models of agricultural activity using, to varying degrees, information contained in these and related time series published
by the US Department of Agriculture.
Although the sector provides a rich database to support
positive and normative analysis of its structure and performances, the potential for aggregation bias is signicant. Drawing
implications from national data and models can lead to
102
Agricultural Finance
The record levels of net farm income in the 2010s thus far
have been helped by historically low interest rates and ination rates. Studies focusing on demand systems for food
products have provided estimates of elasticity for a wide range
of commodities. Results suggest an inelastic demand and lowincome elasticity for agricultural products. This has implications for price variability as supply shifts and muted effect of
changes in disposable personal income as conditions change
in the economy. Agriculture fared relatively well during the
200709 recession when most sectors exhibited weakened
performance.
Domestic linkages
The interface between agriculture and the domestic economy
occurs where producers acquire inputs (including loan funds)
as well as in the markets where they sell their production. (The
large integrated rms in the broiler, turkey, egg, and hog
businesses frequently endogenize many of these relationships
with the rm, thereby increasing the efciency of their operations.) Furthermore, policy actions and other economic
shocks occurring outside agriculture can be transmitted to crop
and livestock producers in these markets. For example, research has shown that monetary policy directly affects the
current operations and growth of agriculture through the cost
and availability of loan funds. This represents a direct linkage
between the policy action and the farm borrower. This same
monetary policy, however, has an impact on other sectors of
the economy as well and thus can alter the equilibrium levels
of prices in all markets.
International linkages
Another factor contributing to record net farm income levels in
the 2010s is the net export demand for agricultural products.
This has been aided by a weak US dollar versus currencies of
exporting nations. Considerable attention has been given in
the literature to modeling international agricultural trade
ows, including the effects that changes in foreign currency
exchange rates can have on net exports for specic agricultural
commodities like wheat and corn. The implication for nance
is that low exchange rates can induce exports of agricultural
products and vice versa. The record levels of net farm income
in the 2010s thus far have also been helped by historically low
value of the dollar.
The global nancial crisis following the 200709 US recession has had an impact on all nations to varying degrees.
The European Union and euro zone nations, for example, were
Agricultural Finance
Role of Policy
An important dimension to macroagricultural nance is the
impact that macroeconomic, farm commodity, international
trade, and other policies have on agriculture and the rest of the
food and ber industry. In discussing each of these areas, it is
important to distinguish between the general impacts of these
policies, in addition to their nancial implications.
103
Federal Reserve buying long-term securities while selling shortterm securities in an effort to keep long-term interest rates low.
Agriculture is typically a beneciary of expansionary
macroeconomic policies. Although the unemployment rate
has remained sticky above the Federal Reserves target, interest
rates, ination, and the foreign exchange rate three important macrovariables for agriculture fell to historic lows. This
helped to lower interest expenses (Figure 5), to avoid inationary pressures pushing up input costs, and helped to
make US agricultural products more affordable to emerging
economy nations, like China.
Several scal policy actions during the 200709 recession,
including stimulus checks and bailouts of General Motors,
Chrysler, and AIG, helped the economy by minimizing the
depth of the 200709 recession. However, scal policy makers
did little to alleviate the uncertainty about future taxation and
spending programs following the recession. This uncertainty
created an environment where businesses in general and nancial markets remain conservative regarding future expansion. This environment has had a much greater impact on
other sectors of the economy like housing than it had on
agriculture.
Policy effects on
Crop price
Domestic demand
Export demand
Net impact
Livestock prices
Farm input prices
Farm interest rates
Net farm income
Farmland prices
Expansionary monetary
policy
Expansionary scal
policy
Contractionary monetary
policy
Contractionary scal
policy
Raise
Raise
Raise
Lower
Raise
Lower
Raise
Raise
Raise
Lower
Lower
Raise
Raise
Raise
Lower
Lower
Lower
Lower
Lower
Raise
Lower
Raise
Lower
Lower
Lower
Raise
Raise
Lower
Lower
Lower
Raise
Raise
Note: Direction of change is not unambiguous, but rather conditional on the relative market share for export demand and relative price elasticity of export demand. A relatively high
market share or relatively high price elasticity of export demand is assumed in this table. It is assumed the impact on crop prices and interest payments offsets the impacts on
livestock prices when calculating net farm income and farmland prices for both crop and livestock producers.
104
Agricultural Finance
Disclaimer
In this article, Sections Microagricultural Finance and Macroagricultural Finance were written by the authors Paul N.
Ellinger and John B. Penson, Jr. respectively.
References
Penson Jr., J.B., Capps, O., Rosson III, C.P., Woodward, R.T., 2014. Introduction to
Agricultural Economics, sixth ed. Upper Saddle River, NJ: Pearson-Prentice Hall.
U.S. Department of Agriculture, 2013. U.S. Farm Income and Wealth Statistics.
Washington, DC: US Government Printing Ofce.
Relevant Website
www.ers.usda.gov
Economic Research Service, US Department of Agriculture.
Glossary
Capital Services of a machine, equipment, or building.
Isoquant A graph showing all combinations of
inputs (labor, capital, and materials) needed to
produce a particular amount of output with given
technology.
Labor Services of a worker or laborer.
Labor demand Derived from the demand for the
output, given the prices of output and inputs and
technology.
Introduction
Agriculture has historically been a sector characterized by
much hard physical labor performed sometimes under adverse
weather and environmental conditions. However, farming in
the US has advanced through oxen, horses and mules, steam
tractors, and then tractors with internal combustion engines to
provide power on farms. Tractors started to be a competitive
source of power in the early twentieth century, as progress
moved from steam to internal combustion engines and steel to
air-inated rubber tires. Early reapers and binders were forerunners of stationary threshing machines, and mobile combines or mechanical harvesters for grain, beans, and cotton
became available over 19301960s. However, hand harvesting
of fruits and vegetables continued into the late 1960s. The
invention and later adoption of the self-propelled mechanical
processed tomato harvester in the mid-1960s was a major
labor-saving factor in fruit and vegetable harvesting. However,
with later related inventions, further saving in labor and improvement in product quality were the result. Mechanical
harvesters were developed for some other processing fruits.
Although fresh fruit and vegetable harvesting continues largely
by hand, mechanical aids have made harvesting faster and
with less stress on workers backs.
US agriculture competes with other sectors of the economy
for inputs of labor, chemicals, building materials, and land.
Since 1980s, an increase in international competition in
grains, oilseeds, fruits and vegetables, and livestock and livestock products has occurred with, for example, Mexico and
Chile, as low cost suppliers of fresh fruits and vegetables
(Calvin and Martin, 2010). However, for an extended period,
US growers have drawn on illegal and legal workers from
Mexico as sources of planting and harvesting labor in these
crops. In particular, mechanization and modication of production practices and improved management practices have
been central to reducing labor requirements for the growing
and harvesting of all kinds of crops. Calvin and Martin
(2010) report that mechanical harvesting is most prevalent in
horticultural crop harvesting, being 75% of vegetables and
melons and 55% of fruits. In 2009, the largest (harvested)
1
In agriculture, farm labor includes the farm operator, unpaid family labor and other labor hired by the farm operator
or manager, but contract farm labor, fertilizer, and pesticide
application and custom harvesting are part of the materials.
doi:10.1016/B978-0-444-52512-3.00100-5
105
106
K
Q00
Note:
Q01
Q = F(L, K; )
Q02
Q = MPLL + MPKK = 0
MPKK = MPLL
MPL
K
MRSKL =
=
MPK
L
L
Q00: K and L with generally variable input ratios or combinations (curved isoquant)
Q01: K and L used in fixed proportions (right angle isoquant)
Q02: K and L are perfect substitute 1-to-1 (straight line isoquant)
Figure 1 Isoquant showing combinations of capital (K) and labor (L) to product Q: variable input proportions, xed proportions and perfect substitutes.
between capital and labor for wheat across countries that have
very different wage to capital rental rates.
The most notable production function is the (general)
CobbDouglas (CD), which relates output Q to a special
power function in input quantities (Douglas, 1976).
Q AL K X ; A A;
0o; ; o1
2
S PQ ; WL ; K ; X ; C0 ; PQ FL; K ; X ; WL LC0
3
107
1.5
no
fiat
ge
ca
sw
ja
de
fr
us it
ir
0.5
yu
li
sz
uk
be
po
tu
sp
as
ne gr sa
nz
is
arsu ve
ch br sy
pe
co ta ma
me
pr
ph
sl
pk
eg
in
bg
0.2
Labor per unit output
0.6
0.4
WL
K
/ %
0
WK
L
Figure 2 Labor and capital (as horsepower) use per unit of agricultural (wheat) output. Data across 44 countries. Figure was constructed from
data reported in Hayami, Y., Ruttan, V.W., 1985. Agricultural Development: An International Perspective. Baltimore, MD: Johns Hopkins University
Press.
80
us
as
nz
60
ca
be
40
de
sw
uk
ge
ne
fifr
is
no
at
sz
ar
ir
20
itsu
sp
ja
gr
ve
ch
po
co
sayu
br
litu
ta ma
pe
sy
0
0
me pr ph
sleg pk
in
0.2
bg
0.4
0.6
108
LS dS PQ ; WL ; K;X;C0 ;
4
_ _
QS SL PQ ; WL ; K;X;C0 ;
5
WL
b
WL
PQ ; WL ; WK ; WX ; C0 ; PQ FL; K; X;
WL
dL WL ; K, PQ, , C0
6
Lb
La
=L PQ MPL L; K; X; WL 0
7
30
sw
no
de
20
ne
ca
ge
us
be
uk
nz
fiir
at ja
10
is
fr
sp
su
ar
yu
po tu
ma
sy
0
0
ph
sl
pk
in
0.2
0.4
0.6
5
at fi
fr
nz
ir
is
sp
ar
po
su
tu
109
us ca
no
ge de
be
uk
ne
sw
ja
yu
sy
0
sl
pk
in
ma
ph
5
1
Log of wage
Figure 6 Capital per unit of labor as wage to labor rises: labor use in wheat production across 44 countries. Figure was constructed from data
reported in Hayami, Y., Ruttan, V.W., 1985. Agricultural Development: An International Perspective. Baltimore, MD: Johns Hopkins University
Press.
X dX PQ ; WL ; WK ; WX ; C0 ;
PQ
13
Ss (Q;WL2, K, C0, )
ACs (Q;WL2, K, C0, )
Ss (Q;WL1, K, C0, )
Q2
Q1
PQ
=K PQ MPK L; K; X; WK 0
8
=X PQ MPX L; K; X; WX 0
9
PQ ; WL ; WK ; WX ; C0 ; 0
10
1
1
WL
WK WX 1=1
L 1 A1 PQ
1 1 1=1
A PQ
WL
WK WX
14
15
L WK = 1o0;
L dL PQ ; WL ; WK ; WX ; C0 ;
11
L WX = 1o0
16
K dK PQ ; WL ; WK ; WX ; C0 ;
12
L PQ 1= 140
17
110
18
Q PQ
WL
1=1o0
20
21
Q02
Q01
C0
Kb
Ka
L
Lb
La
C0
111
112
100.00%
90.00%
80.00%
70.00%
60.00%
West
50.00%
South
40.00%
Southwest
30.00%
20.00%
10.00%
0.00%
1949 1951 1953 1955 1957 1959 1961 1963 1965 1967 1969 1971
Figure 9 Percentage of cotton mechanically harvested by region, South, Southwest, and West, 194972. South includes Alabama, Arkansas,
Georgia, Louisiana, Mississippi, Missouri, North Carolina, South Carolina, and Tennessee. Southwest includes Oklahoma and Texas. West includes
Arizona, California, and New Mexico. US Department of Agriculture, Statistics on Cotton and Related Data, 19201972 (1974).
113
12
10
Labor-hours/ton
Machine harvest
Electronic sorter
Brush shaker
2
0
0
1960
1970
1980
1990
2000
Figure 10 Typical harvest labor use and annual production of processing tomatoes: California, 196097. Reproduced from Thompson, J.F.,
Blank, S.C., 2000. Harvest mechanization helps agriculture remain competitive. California Agriculture 54 (3), 5155.
114
115
116
100
HT soybeans
93
Percent of acres
80
78
73
70
63
HT cotton
60
BT cotton
40
Bt corn
20
HT corn
10
20
09
20
08
20
07
20
06
20
05
20
04
20
03
20
02
20
01
20
00
20
99
19
98
19
97
19
19
96
Data for each crop category include varieties with both HT and Bt (stacked) traits.
Sources: 19961999 data are from FernandezCornejo and McBride (2002). Data for 200010 are
available in the ERS data product, Adoption of genetically engineered crops in the U.S., tables 13
Figure 12 Rapid growth in adoption of genetically engineered crops continues in the US.
blowing the vines, and chaff upward and out of the rear of the
machine. This machine can unload 125 bushels in 20 s.
In Florida orange and orange juice production, historically
the trees were hand-picked by workers on ladders with a bag,
and when the bags were lled, the worker transferred the fruit to
a large metal box on the ground. Several companies, for example, Coe-Collier, OXBO, and Korvan, manufacture and sell
tree fruit harvesters to Florida orange growers. These machines
are basically of two types. One type is a shake-and-catch system
consisting of a two-part self-propelled unit, with the main
power unit grasping the trunk of the tree. The second part of the
harvester moves along the opposite side of the tree with a
117
At one time, all California wine grapes were hand harvested, but growing international competition in the wine
market has induced major cost savings, except in high-end
wines. Currently, a large share of CA wine grapes is mechanically harvested. These machines are relatively tall, self-propelled units that straddle the trellised grapevine rows. The
harvester has rotating arms that dislodge the fruit, which is
then caught on a table and conveyed into a wagon. See the
Korvan machine (Figure 17).
All strawberries continue to be hand harvested because,
they are quite delicate and mainly harvested for the fresh
market. Although other berries were traditionally hand harvested, the Korvan Company manufactures and sells a mechanical berry picker for processing berries (largely for
raspberries and blueberries). This machine is self-propelled
and surrounds the row of berry bushes similar to the wine
grape harvester (Figure 18). This machine does some damage
to the fruit, but because it is going immediately for processing,
this is not generally viewed a serious problem.
A little experimentation has been done with robotic harvesters that use GPS to scout fruit locations and then pick
the fruit. However, electronic assessment of tree fruit is
118
complicated by the fact that tree limbs and unripe fruit may
block the view of the electronic eye sensors.
As suggested above, advances in mechanical harvesting of
fresh fruits and vegetables for the fresh market have progressed
more slowly than for processed produce. However, the share
of potatoes harvested for the fresh market has been and remains substantial, and the rst mechanical harvesters were
invented almost 100 years ago. Incremental innovations have
transformed these machines into modern, self-propelled
mechanical potato harvesters. Although simple mechanical
potato diggers existed in the early 1900s, the rst complete
harvester-separator machines did not exist until the 1950s.
Today, large-scale harvesting is done by a self-propelled machine that scoops up the potato plant and the soil beneath it.
This material is elevated by a rotating apron-chain consisting
of steel links several feet wide, which allows loose dirt to fall
away, while retaining ripe potatoes. The chain deposits this
mixture into an area where further separation occurs. Potatoes
are then continuously elevated into a trailing wagon or truck.
The most complex designs use vine choppers and shakers,
electronic sorters and a blower system to separate good potatoes from rotten potatoes, stones, dirt, and vines (Figure 19).
These are used for harvesting potatoes for the fresh and processing markets.
Other mechanical harvesters for fresh fruits and vegetables
are largely experimental. Fresh market CA iceberg and organic
lettuce, melons, strawberries, and tomatoes have substantial
harvesting costs, and harvester-aids have reduced the workload. For example, the heads of iceberg lettuce are cut by hand
and trimmed, then laid on a table that coveys them to the
center, where workers on the eld wrap them in plastic and
place 32-heads per box, which are then stacked on the wagon.
This process has signicantly reduced the cost of harvesting
and packing iceberg lettuce. A similar process is applied to
melons and cantaloupes, with the slight distinction that they
Figure 20 Washington State University and the USDA-ARS selfpropelled mechanical fresh market apple (sweet cherry) harvester.
119
US$150 000 (in 2010 prices) for the smaller rear-loading model
and US$200 000 for a larger top-loading model.
Structure of Farms
spongy material that reduces impact, and the padded conveyers move the fruit gently to the outer top side of each of the
machine catching tables. As the fruit rolls over the table, a fan
blows away leaves and trash, and the fruit passes to two slowly
rotating modest sized storage bins or boxes.
A benet to growers and consumers is that mechanically
harvested cherries have less bruising or damage than handharvested fruit and reduced exposure to bacteria-laden human
hands. However, sweet cherry consumers are accustomed to
their cherries having stems, but the mechanical harvested
cherries are stemless. For mechanically harvested sweet cherries
and apples, a special tree architecture is needed short with a
Y shape, as opposed to the 2025 feet tall conventional trees
(see Figure 20). The mechanical sweet cherry harvester has
excellent long-term potential for harvesting high-quality sweet
cherries for the fresh market, at an 8090% reduction in harvest labor costs, with less damage than hand-harvested cherries
(Whiting, 2006).
The new BEI Black Ice Harvester works with delicate bush
berries raspberries, blackberries, and blueberries. The Black Ice
Harvester uses jets of air to create a turbulent local environment
within the machine and around the berries, which then gently
dislodge those that are ripe. Between padded walls, the berries
fall onto a bed or table (the Centipede Scale catching frame),
and then are gently conveyed to one pound or smaller containers that are carried on the machine (Figure 21). A major
advantage of this machine is that berries and bushes are not
touched by a picking or rotating-arm mechanism. This helps
minimize damage to ripe berries and scarring of the bushes.
Given the minimal plant damage from the harvester, the machine can be used to make multiple passes over the same
bushes as the berries ripen at different dates. With this machine,
quality meets or exceeds that of hand-harvested fruit, and because no human handling of the fruit is required in the harvesting and packing, there are reduced food safety concerns. The
machine is currently being farm tested, and its estimated cost is
120
450
400
Labor
Land
Machinery
Chemical
350
Index
300
250
200
150
100
50
0
1910
1920
1930
1940
1950
1960
Year
1970
1980
1990
2000
Figure 22 US aggregate usage of farm labor, land, machinery, and chemicals, 191094 (1948100). Adapted from Huffman, W.E., Evenson, R.,
1989. Supply and demand functions for multiproduct U.S. cash grain farms: Biases caused by research and other policies. American Journal of
Agricultural Economics 71, 761773.
Table 1
Output supply and input demand price elasticities: US cash grain farms, 42 states, data at 5-year intervals (194974)
Quantity
Fuel
Machinery
Labor
Wheat output
Soybean output
Inputs:
Fertilizer
Fuel
Machinery
Labor
1.203
0.342
0.199
0.130
0.237
0.717
0.285
0.117
0.334
0.690
0.606
0.363
0.278
0.362
0.464
0.508
0.283
0.370
0.203
0.416
1.000
0.370
0.008
0.033
0.364
0.278
0.147
0.516
Outputs:
Wheat
Soybeans
Feed Grain
0.116
0.852
0.094
0.105
0.082
0.050
0.140
0.011
0.064
0.367
0.059
0.285
0.968
2.l78
0.404
1.051
1.313
0.565
0.646
1.871
0.016
Note: The elasticities in the last row and column are derived residually, others are estimates; all evaluated at the sample mean of the data.
Source: Reproduced from Huffman, W.E., Evenson, R., 1989. Supply and demand functions for multiproduct U.S. cash grain farms: Biases caused by research and other policies.
American Journal of Agricultural Economics 71, 761773.
price elasticity (i.e., smallest negative) of demand. The ownprice elasticities of supply of outputs are positive, as expected,
and large for soybean and wheat, but quite small for feed
grains, which may be because of a restrictive government farm
program on feed grain acreage during this era.
The off-diagonal elements are cross-price elasticities, for
example, 0.237 at the top of the second column represents the
0.24% change in the quantity demanded of fertilizer, because
of a 1% change in the price of fuel. The own-price elasticity of
demand for farm labor is shown to be 0.51, or a 1% increase
in the real wage reduces the demand for farm labor by 0.51%.
A 1% increase in the price of machinery (fertilizer) increases
the demand for labor by 0.36% (0.13%), but an increase in
the price of fuel by 1% reduces the demand for fuel by 0.12%.
These are largely as expected.
Table 2
121
Output supply and input demand elasticities: eight Midwestern states, annual data (19652004)a
Quantity
Corn
Wheat
Livestock
Farm capital
Farm labor
Farm energy
Farm chemical
Outputs:
Soybean
Corn
Wheat
Livestock
0.110
0.149
0.055
0.045
0.233
0.315
0.594
0.109
0.007
0.052
0.927
0.032
0.134
0.208
0.706
0.032
0.093
0.086
0.047
0.060
0.052
0.041
0.274
0.018
0.008
0.028
0.224
0.002
0.078
0.110
0.277
0.014
0.056
0.058
0.040
0.152
Inputs:
Farm capitalb
Farm labor
Farm energy
Farm chemical
Other materials
0.073
0.022
0.028
0.122
0.019
0.106
0.028
0.152
0.269
0.030
0.005
0.016
0.108
0.059
0.002
0.140
0.023
0.022
0.067
0.153
0.016
0.004
0.137
0.021
0.029
0.008
0.045
0.038
0.033
0.027
0.031
0.005
0.409
0.035
0.015
0.010
0.009
0.078
0.667
0.080
0.067
0.035
0.154
0.370
0.229
The elasticities in the last row and column are derived residually, others are estimates; all evaluated at the sample mean.
Farm machinery and breeding stock, but not farm land.
Source: Adapted from Schuring, J., Huffman, W.E., Fan, X., 2013. Aggregate Supply and Demand Functions for Midwestern U.S. Farms Under Rapid Technical Change. Ames, IA:
Department of Economics, Iowa State University.
b
Acknowledgments
The author is C.F. Curtiss Distinguished Prof. of Agriculture
and Life Science and Prof. of Economic, Iowa State University.
Helpful comments were obtained from Jonathan McFadden
and Kristin Senty. Project funded by the Iowa Agricultural
Experiment Station, Ames, IA.
Conclusions
With continued innovation in farm machinery, genetic improvement of crops and farm animals, and a return to rising
real wage rates, we can safely predict that the quantity of labor
122
References
Beattie, B.R., Taylor, C.R., 1993. The Economics of Production. Malabar, FL: Krieger
Publishing Co.
Bogue, A.G., 1983. Changes in mechanical and plant technology: The Corn Belt,
19101940. The Journal of Economic History 93, 125.
Calvin, L., Martin, P.L., 2010. The U.S. produce industry and labor: Facing the future
in a global economy. USDA, ERS Economic Research Report No. 106, Nov.
Colbert, T.B., 2000. Iowa farmers and mechanical corn pikers, 19001952.
Agricultural History 74, 530544.
Douglas, P.A., 1976. The Cobb-Douglas production function once again: Its history,
testing and some new empirical values. Journal of Political Economy 84,
903916.
Fernandez-Cornejo, J., 2008. The impact of adoption of genetically engineered crops
on yields, pesticide use and economic returns in the USA. Presented at the Farm
Foundation Conference on Biotechnology, Washington, DC.
Fernandez-Cornejo, J., McBride, W.D., 2002. Adoption of bioengineered crops.
Agricultural Economics Report No. 810. Washington, DC: U.S. Department of
AgricultureEconomic Research Service.
Griliches, Z., 1960. Hybrid corn and the economics of innovation. Science 132,
275280.
Hayami, Y., Ruttan, V.W., 1985. Agricultural Development: An International
Perspective. Baltimore, MD: Johns Hopkins University Press.
Heinicke, C., Grove, W.A., 2005. Labor market, regional diversity and cotton harvest
mechanization in the post-World War II United States. Social Science History 29,
269297.
Huffman, W.E., 1996. Labor markets, human capital, and the human agent's share of
production. In: John Antle Sumner, D. (Eds.), The Economics of Agriculture:
Papers in Honor of D. Gale Johnson, Vol. 2. Chicago, IL: University of Chicago
Press, pp. 5579.
Huffman, W.E., 2009. Technology and innovation in world agriculture: Prospects for
20102019, Working Paper #09007. Ames, IA: Department of Economics, Iowa
State University.
Huffman, W.E., 2012. The status of labor-saving mechanization in U.S. fruit and
vegetable harvesting. Choices 27 (2nd Quarter), pp. 17.
Huffman, W.E., Evenson, R.E., 1993. Science for Agriculture: A Long-Term
Perspective. Ames, IA: Iowa State University Press.
Huffman, W.E., Evenson, R.E., 2001. Structural adjustment and productivity change
in U.S. agriculture, 195082. Agricultural Economics 24, 127147.
Huffman, W.E., Evenson, R.E., 2006. Science for Agriculture: A Long Term
Perspective, second ed. Ames, IA: Blackwell Publishing, Foreword to second ed.
by V.W. Ruttan.
Huffman, W.E., Evenson, R., 1989. Supply and demand functions for multiproduct U.
S. cash grain farms: Biases caused by research and other policies. American
Journal of Agricultural Economics 71, 761773.
Huffman, W.E., Orazem, P.F., 2007. Agriculture and human capital in economic
growth: Farmers, schooling and nutrition. In: Robert Evenson Pingali, P. (Eds.),
Handbook of Agricultural Economics, Vol 3, Agricultural Development: Farmers,
Farm Production and Farm Markets. New York, NY: Elsevier Science,
pp. 22812342.
Hutchinson, W.D., Burkness, E.C., Mitchell, P.D., et al., 2010. Areawide suppression
of European corn borer with Bt maize reaps savings to nonBt maize growers.
Science 330, 222225.
Meier, F., 1969. An economic analysis of the adoption of the mechanical cotton
picker. PhD Dissertation, The University of Chicago.
NRC (National Research Council, Committee on the Impact of Biotechnology on
Farm-Level Economics and Sustainability), Committee on the Impact of
Biotechnology on Farm-Level Economics and Sustainability), 2010. The Impact of
Biotechnology on Farm-Level Economics and Sustainability. Washington, DC:
The National Academies Press.
Olmstead, A.L., Rhode, P.W., 2008. Creating Abundance: Biological Innovation and
American Agricultural Development. New York, NY: Cambridge University Press.
Orazem, P.F., 1998. Empirical isoquants and observable optimal: Cobb and Douglas
seventy. Review of Agricultural Economics 20, 489501.
Peterson, D.L., 2005. Harvest mechanization progress and prospects for fresh market
quality deciduous tree fruits. Hortechnology 15, 7275 JanMar.
Schmitz, A., Seckler, D., 1970. Mechanized agriculture and social welfare: The case of
the tomato harvester. American Journal of Agricultural Economics 52, 569577.
Schuring, J., Huffman, W.E., Fan, X., 2013. Aggregate Supply and Demand
Functions for Midwestern U.S. Farms Under Rapid Technical Change. Ames, IA:
Department of Economics, Iowa State University.
Street, J., 1957. The New Revolution in the Cotton Economy: Mechanization and Its
Consequences. Chapel Hill, NC: University of North Carolina Press.
Taylor, R.D., DeVuyst, E.A., Koo, W., 2003. Potential impacts of GM wheat on
United States and Northern Plains wheat trade. Fargo, ND: North Dakota State
University, Center for Agricultural Policy and Trade Studies, Department of
Agribusiness and Applied Economics, Agribusiness & Applied Economics Report
No. 515, May.
Thompson, J.F., Blank, S.C., 2000. Harvest mechanization helps agriculture remain
competitive. California Agriculture 54 (3), 5155.
US Department of Agriculture, National Agriculture Statistics Service, 2011a. Citrus
Fruits 2010 Summary. Available at: http://usda01.library.cornell.edu/usda/nass/
CitrFrui//2010s/2010/CitrFrui-09-23-2010.pdf (accessed 24.05.13).
US Department of Agriculture, National Agriculture Statistics Service, 2011b.
Noncitrus Fruits and Nuts. 2010 Summary. Available at: http://usda01.library.
cornell.edu/usda/nass/NoncFruiNu/2010s/2011/NoncFruiNu-07-07-2011.pdf
(accessed 24.05.13).
US Department of Agriculture, National Agriculture Statistics Service, 2011c.
Vegetables 2010 Summary. Available at: http://usda01.library.cornell.edu/usda/
nass/VegeSumm//2010s/2011/VegeSumm-01-27-2011.pdf (accessed 24.05.13).
Whiting, M., 2006. Mechanical harvesting of sweet cherries. Resource. St. Joseph,
MI: American Society of Agricultural Engineers.
Wilson, W.E., Janzen, E.L., Dahl, B.L., 2003. Issues in development and adoption of
genetically modied (GM) wheat. AgBioForum 6 (3), 120.
Zilberman, D., 2004. The economics of pesticide usage. Berkeley, CA: Department
of Agricultural and Resource Economics, University of California Berkeley
Available at: http://are.berkeley.edu/%7Ezilber/.
Relevant Website
http://www.econ.iastate.edu/people/faculty/huffman-wallace
Iowa State University.
Glossary
Encomienda Grants of land that included rights to the
labor of all residents on that land.
GlobalGAP International standard for good agricultural
practices.
Guest workers Individuals invited (by receiving a limited
visa) to work in a specic country for a specied time
period.
Hacendado Owner of large land areas.
Hacienda A large land area.
Inelastic demand Demand that does not respond to
changes in price.
Introduction
Women and girls have worked in agriculture since plants and
animals were domesticated (Flora, 1985). Agricultural labor
can be unpaid (such as on-farm family labor), paid-in-kind
(such as barter or labor exchange), self-employed (such as
marketing of ones own produce), or wage labor (World Bank,
2009). As a few accumulated land from the many, women
work as comanagers, unpaid household labor, eld hands, or
in packing sheds. With the industrialization of family farms,
women shifted from producers of agricultural goods to consumers (Barlett, 1993; Akyeampong and Fofack, 2012). Global
production, distribution, and marketing systems are increasingly exible and feminized (Bain, 2010, p. 343). This has
increased the vulnerability of women farm workers, and at the
same time it has increased the protability of labor-intensive
agricultural production. Women farm workers, who represent
2030% of the approximately 450 million people employed
worldwide as waged agricultural workers (the proportion is
higher, at approximately 40%, in Latin America and in the
Caribbean and parts of Africa), face specic difculties
(DeSchutter, 2012; Fontana et al., 2010). Moreover, when all
agricultural workers, paid and unpaid, are considered, women
make up the majority of those workers.
doi:10.1016/B978-0-444-52512-3.00103-0
123
124
125
126
127
128
Data from 2012 state that only 18% of the 6 76 000 farm
laborers and supervisors are female. Other key information has
not been analyzed by gender. Almost three-quarters of hired
crop farmworkers are not migrants, but are considered settled,
meaning they work at a single location within 75 miles of their
home. This number is up from 42% in 199698. Such proximity increases the possibilities of women becoming exible
farmworkers.
In other countries, the data are equally difcult to access,
and probably equally threatening. Like in the US legal status of
the worker or members of the worker household make it imperative that trust exists between the entity collecting the data
and the employer, contractor, or worker. Less obtrusive data
can be gathered from program records (numbers of farm operators trained in occupational health and safety issues), administrative records (incidence of occupational health and
safety incidents and measures taken to prevent future incidents; number of women and men from district employed in
agricultural enterprises annually), union records (percentage
of women and men in activist or leadership positions),
training records (number of women and men receiving training on labor standards and employment rights per quarter),
government social security records (access of women and men
to social security and unemployment insurance), legal authority records (change in number of cases of women and men
accessing legal advice regarding legal rights), among others.
Subcontracting makes this all more difcult, as it is often
unclear who the employer is and what obligations and responsibilities fall to which entity. In many countries, labor
contractors remain unregulated and continue to operate with
questionable legality. It is, however, a vicious circle for female
agricultural workers, for without the number of workers it is
difcult for auditors to verify the adequacy of standards that
must be determined by the numbers, such as provision of
toilets and adequate living quarters (Bain, 2010).
Conclusion
Although mechanization has decreased the number of farmworkers worldwide, women make up an increasing proportion
of those who do farm work. They are more likely than men to
be employed as exible farm labor in intensive agricultural
production, particularly horticulture, including the ower industry. The increasing use of contract labor and the lack of
clear legal protections, particularly for immigrant farm workers, make women vulnerable to sexual and wage exploitation.
Family responsibilities drive them into exible farm labor increase their work load as they perform both domestic and paid
labor.
Availability of affordable child care and transportation
services to farmworkers increases the well-being of both
mothers and children, as they must no longer choose between
children in the eld or left in a compound alone.
Around the world, women's groups are educating women
agricultural workers about the legal rights as workers and encouraging them to demand them. These groups also provide
support as women join together to demand their rights from
labor contractors, employers, and the state. Increasing the
ability of women agricultural workers to bargain collectively,
References
Akyeampong, E., Fofack, H., 2012. The Contribution of African Women to Economic
Growth and Development: Historical and Policy Implications. Washington, DC:
The World Bank.
Allen, P., Sachs, C., 2007. Women and food chains: The gendered politics of food.
International Journal of Sociology of Agriculture and Food 15, 123.
Bain, C., 2010. Structuring the exible and feminized labor market: GlobalGAP
standards for agricultural labor in Chile. Signs: Journal of Women in Culture and
Society 35, 343370.
Barlett, P.F., 1993. American dreams, rural realities: Family farms in crisis. Chapel
Hill, NC: University of North Carolina Press.
Barrientos, S., Perrons, D., 1999. Gender and the global food chain: A comparative
study of Chile and the UK. In: Afshar, H., Barrientos, S. (Eds.), Women,
Globalization and Fragmentation in the Developing World. London: Macmillan,
pp. 15173.
Bello Barros, R., 1993. Labor processes within a commodity system: A comparative
study of workers in apple packing houses. PhD dissertation, Virginia Polytechnic
Institute and State University.
Capps, R., Bachmeier, J.D, Fix, M., Van-Hook, J., 2013. A demographic,
socioeconomic, and health coverage prole of unauthorized immigrants in the
129
130
Pearson, E., Punpuing, S., Jampaklay, A., Kittisuksathit, S., Prohmmo, A., 2006. The
Mekong challenge. Underpaid, overworked and overlooked: The realities of young
migrants in Thailand, vol. 1. Report of the Mekong Subregional Project to
Combat Trafcking in Children and Women. Bangkok: International Labour
Organization.
Pearson, R., 2007. Beyond women workers: Gendering CSR. Third World Quarterly
28, 731749.
Pontn, J., Pontn, y.D., 2008. Situacin de las Mujeres Rurales: Ecuador. Rome:
FAO.
Preibisch, K.L., Encalada Grez, E., 2010. The other side of el otro lado: Mexican
migrant women and labor exibility in Canadian agriculture. Signs 35, 289316.
Raworth, K., 2004. Trading away our rights: Women working in global supply
chains. Oxfam Campaign Report. Oxford: Oxfam International.
Raynolds, L.R., 2001. New plantations, new workers: Gender and production politics
in the Dominican Republic. Gender and Society 15, 728.
Roenblum, M.R., Brick, K., 2011. US Immigration Policy and Mexican/Central
American Migration Flows: Then and Now. Washington, DC: Migration Policy
Institute.
Runsten, D., Mines, R., Nichols, S., 2013. Immigration Reform and Labor
Requirements in Manually-Skilled Industries: A Market-Based Approach. Policy
Brief no. 2013-1. Davis, CA: Community Alliance with Family Farmers.
Silva, A.E., 1996. De mujer campesina a obrera orista. In: Len, M. (Ed.) Debate
Sobre la Mujer en America Latina y el Caribe, vol. 1. Bogot: Asociacin
Colombiana para el Estudio de la Poblacin, pp. 2842.
Singh, R.D., 1996. Female agricultural workers' wage, male-female wage differentials,
and agricultural growth in a developing country, India. Economic Development
and Cultural Change 45, 89123.
Standing, G., 1999. Global feminization through exible labor: A theme revisited.
World Development 27, 538602.
Tzannatos, Z., 1999. Women and labor market changes in the global economy:
Growth helps, inequalities hurt and public policy matters. World Development 27,
551569.
USAID/GATE Project, 2006. A pro-poor analysis of the shrimp sector in Bangladesh.
Report Prepared for the Greater Access to Trade Expansion (GATE) Project.
Arlington, VA: Development Training Services.
White, J., White, B., 2012. Gendered experiences of dispossession: Oil palm
expansion in a Dayak Hibun community in West Kalimantan. Journal of Peasant
Studies 39, 9951016.
World Bank, 2009. Gender in Agriculture Sourcebook. Washington, DC: International
Bank for Reconstruction and Development.
Relevant Websites
http://caff.org/programs/policy/farmlabor/
Community Alliance with Family Farmers.
http://www.fao.org/home/en/
Food and Agriculture Organization.
http://www.fao.org/docrep/013/i1638e/i1638e.pdf
Food and Agriculture Organization.
http://www.pbs.org/wgbh/pages/frontline/rape-in-the-elds/
Frontline Public Broadcasting Service.
http://www.ifad.org/gender/pub/sourcebook/gal.pdf
International Fund for Agricultural Development.
http://www.ilo.org/public/english/gender.htm
International Labor Organization.
http://www.ohchr.org/EN/Issues/Food/Pages/FoodIndex.aspx
Ofce of the High Commissioner for Human Rights.
http://www.oxfam.org/en/grow/campaigns/behind-brands
Oxfam America Grow Campaign.
http://www.ers.usda.gov/topics/farm-economy/farm-labor/background.
aspx#demographic
United States Department of Agriculture, Economic Research Service.
http://progress.unwomen.org/
UN Women, Progress of the World's Women.
Introduction
Agriculture is full of paradoxes. Farmers are often praised as
the independent yeomen who provide living links to the nation's founding fathers, yet agriculture receives more federal
subsidies than many other US industries. There were too many
farmers during the 1950s, when a million Americans a year
moved to cities, whereas alleged shortages of farm workers
were the rationale for importing almost 500 000 Mexican
Braceros a year to work in the elds.
Thomas Jefferson, the third US President, believed that
family farmers were the backbone of American democracy.
Jefferson's phrase, engraved on the wall of a reading room in
the Library of Congress, proclaims that Those who labor in
the earth are the chosen people of God. Jefferson believed
that rural life was superior to urban life and a nation of selfsufcient family farmers who owned the land they farmed
would guarantee respect for private property and preserve
American democracy.
Family farms were the ideal as well as a widespread reality
in 1790, when the rst Census of Population found that 90%
of the four million US residents lived in rural areas. The
model farm included farmer, a large family, and perhaps a
hired hand, usually a young man who lived with the farmer's
family temporarily before becoming a farmer in his own right.
Everyone on family farms worked to meet peak seasonal labor
needs, explaining why school schedules were adjusted so that
children were available when needed on the farm.
The fact that crops needed more workers during some
seasons than others encouraged diversication to spread out
the work and to make farm families self-sufcient. Most family
farms in the early nineteenth century raised crops and tended
livestock, and most did not generate a surplus to sell because
there were few large US cities and European farmers produced
similar crops. As technology increased the productivity of
farmers, family farms got larger, producing a surplus to sell to
urban residents in expanding US cities and abroad.
There were two other US farming systems that dealt very
differently with the need for seasonal farm workers. In the
southeastern states, plantations produced cotton and tobacco
that were exported to northern Europe and other areas that
could not grow these long-season crops. Slaves were bound to
their plantations, ensuring that seasonal workers were available when needed. Slaves were eventually replaced by sharecroppers who lived and worked on small plots of what had
been plantation land, and in the twentieth century, mechanization reduced the need for seasonal workers on cotton farms,
although tobacco farms continued to rely on foreign-born
farm workers.
The western US states had large landholdings often assembled by entrepreneurs who grazed cattle or raised wheat in
the mid-nineteenth century. The transcontinental railroad, irrigation, and other changes made it protable to switch to
labor-intensive commodities in the 1870s. Large landowners
doi:10.1016/B978-0-444-52512-3.00102-9
131
132
133
134
benches installed along the sides of the van in order to accommodate more workers. The California Legislature responded to the tomato workers' accident with a law in 2000
that requires all vans that charge farm workers fees to have
regular seats with seat belts.
Mexican Braceros
The rst MexicoUS Bracero program began on 23 May 1917,
as farm employers complained of labor shortages during
World War I. The US DOL, which included the Bureau of
Immigration at the time, allowed the admission of Mexicans
primarily for employment in the sugar beet elds of California, Colorado, Utah, and Idaho and the cotton elds of
Texas, Arizona, and California (Scruggs, 1960, p. 322). By the
early 1920s, Mexicans were the principle workforce in many
southwestern farming areas (Scruggs, 1960, p. 319).
The American-workers-rst principle of subsequent guest
worker programs was laid out in this rst Bracero program. US
farm employers had to recruit US workers and to make written
offers of wages, housing conditions, and duration of employment. If they could not nd US workers, they could hire
Mexican Braceros, who were to receive the prevailing wage,
which was the wage paid for similar labor in the community in
which the admitted aliens are to be employed. (CRS, 1980,
p. 10). Farm employers had to provide housing for Braceros,
and this housing had to satisfy state laws or standards set by
DOL if there were no state laws governing farm worker housing.
There were several features of the rst and subsequent guest
worker programs that proved troublesome. For example, some
of the wages earned by Braceros were withheld by the US farm
employers, deposited with the US Postal Savings Bank, and
then transferred to Mexico, where Braceros who returned were
supposed to receive these forced savings. However, many returned Braceros never received these withheld wages. A second
issue involved the debt accumulated by Braceros in the farm
labor camps where they lived. Some Braceros wound up owing
more than the wages they earned to the US farm where they
worked because of purchases of food and alcohol in the
camps. The Mexican government complained about these
issues, and the two governments allowed the Bracero program
to end in 1921. Some ex-Braceros migrated illegally to the US
during the 1920s because there was no US Border Patrol until
1924.
During the 1930s, Dust Bowl migration brought 1.3 million people known as Okies and Arkies to California, swelling
135
136
H-2A Workers
After the Bracero program ended, many California farmers expected to employ Mexican workers under the H-2 guest worker
program, which was established in the 1952 Immigration and
Nationality Act and was used to import Caribbean workers who
primarily hand cut sugarcane in Florida and harvested apples
along the eastern seaboard. Unlike the Bracero program based
on a MexicanUS Memorandum of Understanding, the H-2
program was part of the US immigration law.
However, the H-2 program included requirements that
drew protests from California farmers, such as a requirement
to pay H-2 guest workers the highest of three wages: the federal
or state minimum wage, the prevailing wage for similar work
in the area, or the DOL-calculated Adverse Effect Wage Rate
(AEWR), which was typically the highest of the three. The DOL
also limited H-2 guest workers to 120 days in the US, which
was not a problem in the eastern states that had shorter
growing seasons, but California farmers wanted to employ
Mexican workers for 11 months a year.
The DOL Secretary, Wirtz, asserted that the purpose of these
H-2 regulations was to reduce admissions of foreign workers
in order to reduce unemployment among US farm workers.
Farmers were unhappy, and Senators from California and
Florida in 1965 introduced legislation to transfer responsibility for certifying farm employer's requests for foreign
workers from the DOL to the USDA. Their effort failed on a
46:45 vote because Vice President Hubert Humphrey cast a
vote to break the previous tie and keep the administration of
the H-2 program within the DOL (Congressional Research
Service, 1980, p. 42).
Most H-2 guest workers between the mid-1960s and -1980s
were Jamaicans who cut sugarcane in Florida and picked
apples from Maine to Virginia. There were ongoing disputes
between worker advocates who believed that the DOL was
failing to protect US workers and farm employers who believed that the DOL was putting unnecessary hurdles between
them and the H-2 guest workers on whom they relied. For
example, apple growers sued the DOL when it ordered them to
hire inexperienced Louisiana workers who responded to their
required recruitment advertisements rather than experienced
Jamaican apple pickers. However federal courts ruled that US
employers must hire US workers who can do the job even if
the foreign workers are more productive.
The H-2 program was changed into the H-2A program by
the Immigration Reform and Control Act of 1986, which
Proposed Reforms
Farm employers would like three major changes to the H-2A
program that could change the farm labor market by increasing the share of guest workers among US crop workers. First,
farm employers would like to attest or promise in documents
led with the DOL that they need guest workers and are paying
prevailing wages, ending the current processes that involves
the DOL supervising their efforts to recruit US workers. Attestation would effectively shift control of the border gate from
the US DOL to employers.
Second, rather than provide free housing to H-2A workers,
farm employers would like to pay a housing allowance of US
$12 h1, depending on local costs to rent two-bedroom units
that are assumed to house four workers, if state governors
certied that there was sufcient rental housing for the guest
workers in the area where they would be employed. Substituting a housing allowance for providing housing would make
it much easier for farm employers in California and other
states where most labor-intensive agriculture is in urban or
metro counties with strict zoning regulations to hire guest
workers.
Third, farmers would like the AEWR, the special minimum
wage that must be paid to guest workers, to be rolled back and
studied. The AEWR for California in 2012 was US$10.24 h1,
whereas the state's minimum wage was US$8, so reducing the
AEWR to US$9 h1 or less would help to offset the cost of the
housing allowance.
These three employer-favored reforms to the H-2A program
are included in the Agricultural Jobs, Opportunity, Benets,
and Security Act (AgJOBS), a proposal negotiated between
farm worker and farm employer advocates in the fall of 2000
(Martin, 2005). Many farm worker union and farm employer
groups support AgJOBS, but not the American Farm Bureau
Federation, which in the fall of 2012 unveiled its own proposed new guest worker program that was embraced by many
other farm groups that joined the Agriculture Workforce
Coalition (www.agworkforcecoalition.org).
Under the AFBF proposal, farm employers would have two
options to employ guest workers. The rst would give an unlimited number 11-month visa to foreign workers who could
move between different US farm employers who were registered with the USDA. These free-agent guest workers would
have to leave the US for a month a year but could return year
after year. The second option would allow farm employers to
offer renewable 12-month visas to foreign workers who would
be tied to their farms. These contract workers would have to
leave the US at least 30 days every 3 years.
Unions
Unions are organizations of workers whose purpose is to raise
wages and improve conditions for members who pay the dues
that support the union. Unions put pressure on employers
in four major ways with strikes that reduce the supply of a
good or commodity; activities that reduce the supply of labor
or preserve jobs, such as limits on immigration or clauses
in collective bargaining agreements that limit mechanization;
political activities to obtain favorable laws and their interpretation; and consumer boycotts to reduce the demand
for particular commodities. Employers counter these union
weapons by replacing workers who strike, engage in political
activities to win laws favorable to management rights, and by
advocating more immigration and other policies that increase
the supply of labor.
US union membership has been in a long-term decline, so
that only 11% of the 128 million wage and salary workers
were union members in 2012, down sharply from 20% in
1983 (www.bls.gov/news.release/union2.nr0.htm). There were
14.3 million union members in 2012, including seven million
private sector workers and 7.3 million public employees. Local
government workers had the highest unionization rate, 42%,
whereas agriculture had the lowest, 1.4%. By occupation,
education workers had the highest unionization rate, 35.4%,
and farming had the lowest rate, 3.4%.
137
Pre-UFW Unions
The American Federation of Labor (AFL) began as a national
organization of craft unions in 1886. The AFL's member
unions, such as carpenters or bricklayers, organized workers
into unions that reected worker crafts or occupations. In
1903, several AFL unions announced plans to organize farm
workers, but their union drive soon sputtered, in part because
the AFL unions feared that organizing farm workers would
upset farmers, who could use their power in Congress and
state legislatures to restrict all union activities.
The Industrial Workers of the World (IWW) or Wobblies
was a revolutionary union founded in 1905 by Eugene
Debs and other radical labor leaders who felt betrayed by
the AFL unions. Their goal was to replace what the IWW
called a wage slave system of employers and employees
with worker-run cooperatives. The IWW wanted to organize
all workers into one big union that included skilled as
well as unskilled workers and minorities such as Chinese and
Japanese farm workers, who were excluded from most AFL
unions.
The IWW successfully organized many of the wheat harvesters in the Midwestern states early in the twentieth century.
A peak of 250 000 mostly white workers migrated from Texas
to Canada, harvesting wheat and other grains from south to
north. Most traveled by riding freight trains without paying,
and migrants without an IWW red card were sometimes
prevented from riding the rails. A typical IWW plan of action
at a particular farm involved an IWW organizer or job delegate getting a job and helping the workers to organize a strike.
138
and strikes and helping workers to present demands to employers. CAWIU-led strikes were often violent, in part because
growers and their foremen were often deputized to help local
law enforcement.
There were 37 strikes involving 48 000 farm workers in 14
crops in California in 1933, culminating in an October cotton
harvesters strike. Harvest-time strikes during the spring and
summer usually resulted in wage increases, so that by fall,
workers were prepared to strike again to get a wage increase for
picking cotton, the crop that employed most of the workers.
Cotton farmers met in September to set a piece-rate wage of
pay 60 cents per 100 pounds of cotton picked, up from 40
cents in 1932 but less than the US$1.50 of 1929. Cotton
harvesters were expecting wages to rise to at least US$1, and
the CAWIU called a strike on 4 October 1933 to support its
demand for a US$1 per 100 pound piece rate. Growers evicted
10 00020 000 strikers and their families from on-farm labor
camps, and most moved into CAWIU-run tent camps.
The strike was condemned by farmers but were supported
by local leaders. A Tulare newspaper editorialized that the
strike would vanish into thin air overnight if the outside agitators were rounded up and escorted out of the county, as they
should be (Jamieson, 1945, p. 103). Farmers tried to break up
striker rallies, and two workers were killed in Pixley, CA, USA.
State ofcials urged local authorities to disarm the growers,
who instead issued more gun permits, prompting the reporters
who arrived to cover the strike to turn against growers for
refusing mediation.
The strike threatened the cotton crop. The Governor
appointed a UC fact nding missions that recommended a
75-cent piece rate. Banks persuaded farmers to pay 75 cents by
threatening to withhold nancing for the 1934 cotton crop,
and the Governor announced that workers who did not go to
work by 16 October 1933 would be denied state relief in the
winter months. The 75-cent wage appeared to be at least a
partial victory for the CAWIU, and it prompted farmers to
form a new organization, the Associated Farmers of California,
which persuaded most rural counties to enact antipicketing
ordinances that were used to prosecute CAWIU organizers.
The Associated Farmers, nanced largely by nonfarm
banks, railroads, canneries, public utilities, and the Industrial
Association of San Francisco, provided funds to local law enforcement to monitor CAWIU leaders. It succeeded, and 14
CAWIU leaders were convicted of instigating violence and
were sent to prison in July 1934. The CAWIU showed that
farm workers could be organized to strike in support of higher
wages, but the CAWIU's policy of not signing contracts, and its
communist orientation, persuaded growers to organize themselves into effective antiunion associations.
139
fell from 3.4 pounds per person in 1968 to 2.2 pounds per
person in 197071. Chavez, hailed as the Latino Martin Luther
King, was featured on the cover of Time magazine on 4 July
1969 under the headline, The Grapes of Wrath.
Grape grower Lionel Steinberg signed a contract with the
UFW on 10 April 1970, ending La Causa. Other grape growers
followed, signing contracts that offered harvesters US
$1.75 h1, and the UFW soon had 150 contracts covering
20 000 workers. The contracts included clauses restricting
mechanization and pesticide usage, and the UFW announced
plans to follow in the footsteps of construction and longshoremen unions by being the organizing institution in what
had been a casual labor market, with UFW hiring halls allocating work according to each worker's seniority with the UFW.
The UFW had a rival, the Teamsters union that represented
truck drivers as well as many of the workers employed in
canneries and processing sheds. When the UFW sent its werepresent-your-workers letters to lettuce growers in 1970, most
responded that their eld workers were already represented by
the Teamsters. The UFW attacked the Teamsters and the
growers, emphasizing that many workers did not know the
Teamsters represented them and that secret contracts were
signed to avoid the UFW.
The UFW was an early supporter of the Democratic candidate for governor in 1974, Jerry Brown. After he won the
November 1974 election, Brown made the enactment of a
farm labor relations law his top priority. The Agricultural
Labor Relations Act (ALRA) was signed into law on 5 June
1975 so that the rst elections could be held during the peak
harvest period, and 15 artichoke workers employed by Molera
Agricultural Group near Castroville made history by casting
votes in the rst Agricultural Labor Relations Board (ALRB)supervised election in September 1975. The UFW and the
Teamsters competed vigorously in these rst ALRA elections.
There were elections on ve or more farms every day in the fall
of 1975, a total of 418 in the rst 5 months the ALRA was in
effect. The UFW won 198 or 55% of the 361 elections in which
a winner was certied, and the Teamsters 115% or 32%.
Unionization was expected to transform to farm labor
market, double farm wages in California and the rest of the
US, and close the farmnonfarm wage gap. However, experienced observers were more skeptical about unionization.
Fuller and Mason (Fuller and Mason, 1977 p. 80) concluded
that farm worker unionization will continue to be more exceptional than dominant (1977, p. 79), but added that farm
worker unions representing a small share of farm workers
could nonetheless become politically inuential with respect
to laws and programs affecting all farm workers.
Rising farm wages and the introduction of fringe benets
for unionized farm workers raised labor costs and spurred
efforts to develop labor-saving machines including some developed by the University of California researchers. The UFW
and the California Rural Legal Assistance organization sued the
UC in 1978, charging that researchers were using tax monies to
develop machines that displaced farm workers and small
farmers. Stopping mechanization research became the UFW's
No. 1 legislative priority (Business Week, 30 January 1978)
and was largely achieved as rising unauthorized migration
weakened the UFW and reduced wage increases (Martin and
Olmstead, 1985).
140
disputes by dropping charges that particular employers violated the ALRA in exchange for contracts. For example, the
UFW settled a long-running dispute with lettuce grower Bruce
Church Inc (BCI) in May 1996 by signing a 5-year collective
bargaining agreement, but BCI soon stopped growing lettuce.
The UFW won a mandatory mediation amendment to the
ALRA in 2002 that allows either employers or unions to request mediation to negotiate a rst contract. If the mediator
fails to help the parties reach agreement, he can recommend a
contract that the ALRB can impose on the parties (Martin and
Mason, 2003).
Unions play a relatively small role in the farm labor market
of California and most other major farming states. Four major
explanations have been advanced for the relative paucity of
unions in agriculture: union leadership failures, politics, farm
employer changes, and immigration. The union leadership
failure is the most common explanation, with most analyses
asserting that Cesar Chavez was a charismatic leader able to
articulate the hopes of farm workers, but Chavez and the UFW
were unable to negotiate and administer union contracts to the
satisfaction of employers and experienced farm workers. As
workers left for nonfarm jobs, the UFW was unable to organize
newcomer farm workers (Pawel, 2009; Ganz, 2009).
The second explanation involves the politics surrounding
the ALRB, the state agency that administers the ALRA. Democratic governors made key appointments to the ALRB between
1975 and 1982, Republicans between 1983 and 1998,
Democrats between 1999 and 2004, Republicans between
2005 and 2011, and Democrats since then. This it's-all-politics theory holds that the effectiveness of a self-help labor relations law depends on which party makes appointments to
the ALRB, the agency that enforces the law (Majika and Majika,
1982).
The third explanation emphasizes that union successes of
the 1960s and 1970s were mostly with employers who hired
farm workers directly and had brand names that made them
vulnerable to union-led boycotts of their farm and nonfarm
products. Boycott-vulnerable corporations such as Seven-Up,
Shell Oil, and United Brands sold their California farming
operations in the 1980s, and the UFW found it harder to deal
with the independent growers who replaced them. There was
also an increase in the use of intermediaries such as contractors, and the combination of independent growers and
intermediaries such as FLCs reduced union power.
The fourth explanation is immigration. The UFW had its
maximum impacts on farm wages between the mid-1960s and
the early 1980s, when legal and unauthorized immigration
was low. (Illegal) migration began rising in the 1980s, rose
more in the 1990s, and peaked during 200207, when an
estimated 500 000 unauthorized foreigners a year, including
300 000 Mexicans, settled in the US. These migrants increased
the supply of farm workers and made it hard for unions to win
wage and benet increases via collective bargaining (Martin,
2009).
141
Conclusions
Agriculture is a peculiar industry with a unique labor market.
The three R-functions of all labor markets are dealt with differently in agriculture. Farmers often rely on intermediaries
such as contractors to assemble crews of workers and move
them from farm to farm, many farm operators use piece-rate
wage systems to give workers an incentive to work fast without
close supervision, and farm employers have more often cooperated to ensure that they collectively have enough seasonal
workers to ll farm jobs rather than individually developing
mechanisms to identify and retain the best workers on their
particular farm.
Approximately three-fourths of US hired farm workers were
born abroad, usually in Mexico, and half of all farm workers
are not authorized to work in the US. Farm employers believe
that US workers shun especially seasonal farm jobs and want
the government to make it easier for them to hire foreigners as
legal guest workers. Twice in the past, between 1917 and 1921
and again between 1942 and 1964, the US government
allowed farmers to recruit Mexican Braceros to ll seasonal
farm jobs. A separate guest worker program, H-2 between
1952 and 1986 and H-2A since 1987, is used mostly by farm
employers in the eastern states to recruit foreign workers to ll
seasonal jobs. US farmers have been asking Congress to relax
regulations governing the H-2A program for the past two
decades, especially rules that require them to try to recruit US
workers, to provide guest workers with free housing, and to
pay them a super minimum wage known as the AEWR.
Guest workers change the farm labor market by altering
recruitment, remuneration, and retention, with agents handling recruitment in worker countries of origin, guest workers
who are aware that termination means losing the right to be in
142
the US having extra motivation to perform work to the satisfaction of the employer, and retention not an issue because
guest workers must leave the US when their jobs end or visas
expire. Farm worker unions change the farm labor market in
opposite ways. Unions often want a voice in recruitment, and
some have tried to operate hiring halls to which employers
turn when they need workers. Unions generally favor wageleveling pay systems and often establish higher-thanminimum wages for the workers covered by the contract. Finally, union contracts usually include seniority and benet
provisions that make it worthwhile for a worker to remain
with one farm.
The farm labor market today is at a crossroads. Farm employers and farm worker advocates agree that government
policies, especially immigration policies, are likely to shape
recruitment, remuneration, and retention. Employers would
like more farm workers to be legal guest workers, whereas
worker advocates favor legalizing currently unauthorized
workers and encouraging farmers to raise wages and take other
steps to retain them.
References
Brenner, M., 2001. In the kingdom of big sugar. Vanity Fair. Available at: http://
www.vanityfair.com/business/features/2001/02/oridas-fanjuls-200102 (accessed
30.01.13).
Carter, C., Hueth, D., Mamer, J., Schmitz, A., 1981. Labor strikes and the price of
lettuce. Western Journal of Agricultural Economics 6 (1), 114. Available at:
http://ideas.repec.org/a/ags/wjagec/32084.html (accessed 30.01.13).
Congressional Research Service, 1980. Temporary Worker Programs: Background
and Issues. Prepared for the Senate Committee on the Judiciary. Available at:
http://ufdc.u.edu/UF00087217/00001 (accessed 30.01.13).
Daniel, C.E., 1981. Bitter Harvest: A History of California Farmworkers 18701941.
Berkeley: University of California Press.
Fisher, L., 1952. The Harvest Labor Market in California. Cambridge, MA: Harvard
University Press.
Fisher, L., 1953. The Harvest Labor Market in California. Cambridge: Harvard
University Press.
Fuller, V., Mason, B., 1977. Farm labor. Annals of the American Academy of
Political and Social Science 429, 6380. Available at: http://ann.sagepub.com/
content/429/1/63.abstract (accessed 01.09.13).
Ganz, M., 2009. Why David Sometimes Wins: Leadership, Organization, and
Strategy in the California Farm Worker Movement. Oxford University Press.
Available at: http://global.oup.com/academic/product/why-david-sometimes-wins9780195162011;jsessionid=33942B6864B63BFF6BD00B0DA0D67C1B?
cc=us&lang=en& (accessed 01.09.13).
Goldfarb, R., 1981. A Caste of Despair. Iowa State University Press. Available at: http://
books.google.com/books/about/Migrant_farm_workers.html?id=nClHAAAAMAAJ
(accessed 01.09.13).
Jamieson, S., 1945. Labor Unionism in American Agriculture. Washington: US
Department of Labor. Bureau of Labor Statistics Bulletin 836. Available at: http://
www.jstor.org/stable/1053346
Lloyd, J., Martin, P., Mamer, J., 1988. The Ventura citrus labor market. Berkeley:
University of California, Division of Agriculture and Natural Resources Giannini
Information Series 88-1.
Majika, L., Majika, T., 1982. Farmworkers, Agribusiness, and the State. Philadelphia:
Temple University Press.
Mamer, J., Rosedale, D., 1980. The Management of Seasonal Farm Workers under
Collective Bargaining. UCCE Leaet 21147.
Martin, P., 2003. Promise Unfullled: Unions, Immigration, and Farm Workers.
Ithaca: Cornell University Press. Available at: www.cornellpress.cornell.edu/book/?
GCOI=80140100792940&CFID=9652803&CFTOKEN=f1155d49f162eed55AABB7F9-C29B-B0E5-30D66D992EBABD0B&jsessionid=84301cb0683d577084
9b171b6b4e272f564cTR (accessed 01.09.13).
Martin, P., 2005. AgJOBS: New solution or new problem. UC Davis Law Review 38
(3), 973991. Available at: http://lawreview.law.ucdavis.edu/articles/Vol38/
vol38_no3.html (accessed 30.01.13).
Martin, P., 2009. Importing Poverty? Immigration and the Changing Face of Rural
America. Yale University Press. Available at: http://yalepress.yale.edu/yupbooks/
book.asp?isbn=9780300139174 (accessed 30.01.13).
Martin, P., Mason, B., 2003. Mandatory mediation changes rules for negotiating
farm labor contracts. California Agriculture 57 (1), 1317.
Martin, P.L., Olmstead, A.L., 1985. The agricultural mechanization controversy.
Science 227 (4687), 601606.
Martin, P., Perloff, J., 1997. Hired farm labor. In: Siebert, J. (Ed.), California
Agriculture. Issues and Challenges. UC-DANR, pp. 151174.
Pawel, M., 2009. The Union of Their Dreams: Power, Hope, and Struggle in Cesar
Chavez's Farm Worker Movement. Bloomsbury Press. Available at: http://
unionoftheirdreams.com/home.php (accessed 30.01.13).
Rasmussen, W., 1951. A History of the Emergency Farm Labor Supply Program,
194347. USDA Monograph vol. 13.
Rural Migration News, 2000. California: Pesticides, Transportation, Wages. vol. 6.
No 1. Available at: http://migration.ucdavis.edu/rmn/more.php?id=417_0_3_0
(accessed 30.01.13).
Rural Migration News, 2010. H-2A Cases, H-2B. vol. 16. No 4. Available at: http://
migration.ucdavis.edu/rmn/more.php?id=1572_0_4_0 (accessed 30.01.13).
Rural Migration News, 2012. California: Heat Bills, QCEW, FELS. vol. 18. No 4.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=1714_0_3_0
(accessed 30.01.13).
Steven Street, R., 1998. Tattered Shirts and Ragged Pants: Accommodation, Protest,
and the Coarse Culture of California Wheat Harvesters and Threshers, 1866
1900. Pacic Historical Review 67 (4), 573608.
Scruggs, O., 1960. The First Mexican Farm Labor Program. Arizona and the West 2
(Winter), 319326. Available at: www.jstor.org/action/showPublication?
journalCode=arizwest (accessed 01.09.13).
Relevant Website
www.doleta.gov/agworker/naws.cfm
NAWS. National Agricultural Worker Survey.
Introduction
Food and ber is produced on farms in a land-intensive and
biological production process by three major types of workers:
farm operators, unpaid family workers, and hired workers.
Around the world, 59% of the estimated 1.1 billon people
employed on farms in 2000 were farm operators and members
of their families, and 450 million or 41% are hired or wage
workers (Pigot, 2003, p. 38).
The employment of all three types of workers on farms falls
with economic development, but the employment of farmers
and unpaid family members tends to fall fastest. In the US,
hired workers were approximately 60% of average employment on farms in 2010, and farmers and unpaid family
members approximately 40%. The consolidation of farms
into fewer and larger units that specialize in the production
of one or a few crop or livestock commodities promises to
further increase the farm worker share of average employment
on US farms.
Consolidation of farm production on fewer and larger
farms, with hired workers doing an ever rising share of farm
work, is occurring around the world. Hired workers do most of
the farm work in the production of labor-intensive horticultural crops in Western European countries, and many are
migrants from poorer countries, as with Poles employed on
German farms, Ukrainians employed on British farms, and
Romanians employed on Italian farms. In Japan and Korea,
migrants from the Philippines and Vietnam often work on
farms that produce labor-intensive crops, as the wives of
farmers, as trainees, and as guest workers. In many developing
countries, workers from lower wage neighboring countries do
much of the work on larger farms and plantations, from
Malaysia and Thailand in southeast Asia to South Africa to
Costa Rica. This article focuses on the US, which has some of
the worlds largest labor-intensive farms that hire workers, but
the trend toward producing labor-intensive crops on so-called
factories in the elds and employing workers who migrate
from lower wage areas within their country or another country
is universal.
In the US, agriculture is dened for employment purposes
in Section 3(f) of the Fair Labor Standards Act (www.dol.gov/
whd/regs/statutes/FairLaborStandAct.pdf) as farming in all its
branchesincluding the cultivation and tillage of the soil,
dairying, the production, cultivation, growing, and harvesting
of any agricultural or horticultural commoditiesthe raising
of livestock, bees, fur-bearing animals, or poultry, and any
practices (including any forestry or lumbering operations)
performed by a farmer or on a farm as an incident to or in
conjunction with such farming operations, including preparation for market, delivery to storage or to market or to carriers
for transportation to market. One practical consequence of
this denition is that workers who pack produce on the farm
where they work are considered farm workers if the farmer
packs only his own fruit. By contrast, farmers who pack their
doi:10.1016/B978-0-444-52512-3.00101-7
143
144
Farm Employment
In the US and many other industrial countries, hired workers
dominate average agricultural employment. During the
1990s, when USDAs National Agricultural Statistics Service
(NASS) collected data on farmers, unpaid family workers,
and hired farm workers, there were an average 2 million
farmers and unpaid family workers and 1.3 million hired
workers employed on US farms, meaning that farmers and
unpaid family members accounted for 60% of average farm
employment.
The employment of all three types of workers on farms
have trended downward, but the employment of farmers and
unpaid family members fell fastest, so that hired workers were
approximately 60% of average employment on farms in 2010.
The labor force projections in Table 1 suggest that the number
of farm operators and unpaid family members will continue
declining, whereas the number of hired workers stabilizes, so
that the share of average employment contributed by hired
workers rises to 62% by 2020.
The most detailed source of data on farm employment is
from the COA that the US and most other countries conduct
periodically (www.agcensus.usda.gov/index.php). In the US,
all places that normally sell at least US$1000 worth of farm
commodities are surveyed in the years ending in two and
seven. Some 482 000 US farms reported almost US$22 billion
in labor expenses for workers hired directly by the farm
operator in the 2007 COA, and another US$4.5 billion for
contract labor, which involves workers brought to farms
by labor contractors and other intermediaries. Total labor expenses of US$26 billion were a seventh of farm production
expenses.
Farmers reported hiring 2.6 million workers in the 2007
COA, including 35% or 910 000 workers who were hired
for 150 days or more on their farms. This 2.6 million jobson-farms number must be interpreted carefully because it does
not include workers brought to farms by contractors and other
Table 1
intermediaries, and it double counts individuals who are reported by two farmers.
There are several ways to convert the total number of farm
jobs into average employment or year-round equivalent jobs in
order to compare farm and nonfarm employment. For example, average employment is approximately 1.5 million in US
food manufacturing (North American Industry Classication
System (NAICS) 311), which means that adding up the employment of wage and salary workers each month in industries
ranging from meatpacking to fruit and vegetable freezing and
canning and dividing by 12 months generates an average 1.5
million employees. Hired farm workers are not included in the
Current Employment Statistics program (www.bls.gov/ces), so
their average employment must be estimated.
Average employment of hired workers on farms can be
estimated by dividing the farmers expenditures on hired
workers by average hourly earnings to calculate the number of
year-round or 2000 h-jobs on farms. The NASS surveys farm
employers quarterly to obtain employment and earnings data
on hired workers (http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID=1063). In 2007,
NASS reported that farmers paid hired workers an average US
$10.21 an hour, the same year that farmers reported US$26.4
billion in labor expenses. Dividing labor expenses by average
hourly earnings, as in Table 2, suggests 1.2 million full-time
equivalent (FTE) or 2000 h a year jobs on US farms in 2007,
about the same as average employment in 2002 using that
year's labor expenses and average hourly earnings.
The Quarterly Census of Employment and Wages (www.bls.
gov/cew) collects data on the employment and earnings of
workers in establishments covered by Unemployment Insurance (UI). The QCEW has several advantages over the COA,
including detailed data by commodity and geographic area, but
its coverage of farm workers is not complete. All farm workers in
Table 2
2002
2007
200
22
9.1
8.80
2 500
1 201 923
297
26
11.4
10.21
2 547
1 224 290
US: Total and hired worker employment (thousands): 2000, 2010, and 2020
Agriculture
Wage and salary
Operator and family
US total
2000
2 396
1 354
1 042
143 236
2010
2 135
1 282
853
143 068
2020
2 005
1 236
769
163 536
Change (%)
200010
201020
11
5
18
0
6
4
10
14
Source: Reproduced from Sommers, D., Franklin, J., 2012. Overview of projections to 2020. Monthly Labor Review 135 (1), 320. Available at: http://www.bls.gov/opub/mlr/2012/01/
(accessed 04.02.13) and Henderson, R., 2012. Industry employment and output projections to 2020. Monthly Labor Review 135 (1), 6583. Available at: www.bls.gov/opub/mlr/2012/
01/ (accessed 04.02.13).
60%
50%
40%
Immigration reform and control act enacted
National agriculture workers survey beings
SAW
Unauthorized
30%
20%
10%
2009
2008
2007
2006
2005
2004
2003
2002
2001
2000
1999
1998
1997
1996
1995
1994
1993
1992
1991
1990
1989
1988
1987
1986
0%
1985
145
Figure 1 Special agricultural workers (SAWs) and unauthorized crop workers, 19892009. Reproduced from NAWS (http://www.doleta.gov/
agworker/naws.cfm).
146
Table 3
All
US-born
Foreign-born
52
78
36
28
30
59
23
30
6
100
77
37
68
97
44
23
23
1
45
78
36
13
3
65
23
32
7
23
13
88
17
1
78
45
22
14
98
20
0
56
27
23
12
83
15
1
88
52
9.13
194
18
73
44
9.74
180
26
66
76
8.89
200
14
78
31
Abbreviations: FVH, fruit, vegetable, and horticultural speciality; HS, high school.
Source: Reproduced from NAWS interviews 200709.
workers, versus a quarter of US-born workers, had employerprovided health insurance in their current job.
More than three-fourths of foreign-born workers, and twothirds of US-born workers, plan to continue working in agriculture for at least ve more years. A third of the foreign-born,
versus two-thirds of the US-born, say they could nd a nonfarm job within a month.
Table 4 examines two groups of farm workers whose share
of crop workers changed over time. SAW-legalized farm
workers, including a few workers legalized under the general
legalization program in 198788 and Central American programs in the 1990s, fell from 32% of all crop workers to 15%
between 198991 and 19982000; the share of SAWs has
since stabilized at just more than 10%. Foreign-born newcomers, who are workers in the US less than a year before they
were interviewed, rose sharply during the 1990s to almost a
quarter of all crop workers in 19982000. Since then, the share
of newcomers has fallen to less than 10% between 2007 and
2009.
As would be expected, SAW-legalized workers are much
older than newcomers, as they had to do farm work as unauthorized foreigners in 198586 to qualify for legalization.
The average age of SAW-legalized workers was 49 in 200709,
versus 25 for newcomers. Three-fourths of the SAW-legalized
workers did not move, but a quarter returned to Mexico in the
past year, usually over the Christmas holidays. More than 90%
of the newcomers to the US farm workforce moved from
Mexico to the US in the year before they were interviewed.
SAW-legalized workers are older and have less education
than foreign-born newcomers, on average 5 versus 6 years (7%
of both groups had graduated from high school in 200709),
but are much more likely to speak some English and to have
incomes above the poverty line. By contrast, approximately
95% of foreign-born newcomers had below-poverty level incomes. A third of foreign-born newcomers were employed by
labor contractors, versus less than a fourth of SAW-legalized
workers, including only an eighth in 200709. Foreign-born
newcomers had fewer days of farm work than SAW-legalized
workers, in part because not all were in the US for the full year
before being interviewed.
Approximately 90% of both SAW-legalized and foreignborn newcomer workers are employed in FVH commodities, a
pattern that has not changed over the past two decades. The
share of both SAW-legalized and foreign-born newcomer
workers lling harvest and postharvest jobs has been falling,
and was half or less in 200709.
SAW-legalized workers earned an average 1.5 times the
federal minimum wage in 198991, but their average premium over the minimum wage fell in the subsequent periods.
Foreign-born newcomers earned a 30% premium over the
federal minimum wage in 198991, and they averaged only
10% above the federal minimum wage in 200709. A third of
SAW-legalized workers, but only an eighth of newcomers,
believe they could get a nonfarm job in a month.
In a hired farm workforce that involves 2.5 million individuals working for wages on US farms sometime during a
typical year, making the hired farm workforce equivalent to the
average employment of janitors and cleaners, farm worker
averages can obscure important changes. For example, almost
all foreign-born farm workers were born in Mexico, but
Table 4
147
Foreign-born newcomers
19982000
200709
198991
19982000
200709
32
15
12
23
100
86
32
2
3
63
100
84
49
2
2
87
12
37
3
13
74
23
7
7
41
13
25
100
88
40
1
4
77
36
31
13
2
16
1
88
25
1
1
36
94
2
14
1
88
25
1
1
34
94
3
7
8
76
86
59
17
76
87
39
26
88
87
45
1
58
93
72
1
60
77
44
1
70
93
51
4.91
3.80
77
5.98
5.15
76
1
13
7.87
7.25
90
4
12
5.51
3.80
191
45
6.93
5.15
193
11
40
9.82
7.25
226
26
37
20
Abbreviations: FVH, fruit, vegetable, and horticultural speciality; HS, high school; SAW, special agricultural worker.
Source: Reproduced from NAWS interviews 19892009.
However, half of crop and nursery workers remain unauthorized, helping to explain the keen interest of farm employers in immigration reforms that could lead them to re
experienced but unauthorized workers to avoid nes unless
their currently unauthorized workers were legalized. The prospect of new requirements that employers use the Internetbased E-Verify system to check the legal status of newly hired
workers has encouraged most farmers to demand easier access
to legal guest workers to ll farm jobs. However, there is not
yet any agreement on a package of new measures to keep
unauthorized workers from getting US jobs and allowing farm
employers to more easily hire guest workers.
148
149
In Fall 2000, worker advocates and farm employers negotiated AgJOBS to repeat the IRCA approach to unauthorized
migration and agriculture, viz, legalize the current unauthorized farm wrokers and make it easier for farm employers
to hire legal guest workers in the future. AgJOBS included
several important changes. Like the SAW legalization program,
AgJOBS would allow currently unauthorized farm workers to
legalize their status immediately. However, to earn a regular
immigrant status for themselves and their families, foreigners
legalized under AgJOBS would have to continue to do
farm work, a provision aimed at preventing an immediate
exodus of newly legalized farm workers to nonfarm jobs
(Martin, 2009).
There have been several iterations of AgJOBS. The most
recent version, S 1038 and HR 2414 introduced in May 2009,
would have allowed up to 1.35 million unauthorized farm
workers who did at least 150 days or 863 h of farm work in the
24-month period ending 31 December 2008 to apply for Blue
Card probationary status (Rural Migration News, 2009a). Blue
Card holders could work and travel freely within the US and
enter and leave the US, and could earn an immigrant status for
themselves and their families by continuing to do farm work
over the next 35 years. AgJOBS has three continued farm
work options: (1) performing at least 150 days (a day is at
least 5.75 h) of farm work a year during each of the rst 3 years
after enactment; (2) doing at least 100 days of farm work a
year during the rst 5 years; or (3) working at least 150 days in
any 3 years, plus 100 days in the fourth year (for workers who
do not do 150 days in the rst 3 years).
For 6 years, farm employers of Blue Card holders would
have to provide their employees with written records of their
farm work and submit a copy to DHS or face nes of up to US
$1000. DHS would check documentation of the farm work of
Blue Card holders and, after they paid fees and nes, Blue Card
holders and their family members could become immigrants.
AgJOBS would change the H-2A program in three major
ways to make it easier for farmers to recruit and employ legal
guest workers (Rural Migration News, 2009a). First, farm
employers could attest that they need guest workers and are
paying prevailing wages rather than have Department of Labor
(DOL) supervise their efforts to recruit US workers, a process
called certication. Attestation would effectively shift control
of the border gate from the US Department of Labor to
employers.
Second, rather than provide free housing to H-2A and outof-area US workers as is required currently, AgJOBS would
allow farm employers to pay a housing allowance of US$12
an hour, depending on the local costs to rent two-bedroom
units that are assumed to house four workers, if state governors certied that there is sufcient rental housing for the
guest workers in the area where they will be employed. Third,
the Adverse Effect Wage Rate (AEWR), the minimum wage that
must be paid to legal guest workers, would be frozen at last
year's levels and studied, effectively reducing the AEWR by US
$12 an hour and offsetting the cost of the housing allowance.
Despite bipartisan support, AgJOBS has not been enacted.
Meanwhile, farmers aware that (1) half of their workers are
unauthorized, (2) federal I-9 audits of their employment records can remove a large share of their workers, and (3) more
states are enacting laws requiring employers to use E-Verify
150
151
152
a year. However, the average earnings of seasonal farm workers, now approximately US$10 000 a year, would rise to more
than US$14 000 a year, or from below the 2011 poverty line of
US$10 890 for an individual to above the line.
153
154
1968, when more than 90% of meat production workers belonged to unions and the average meatpacking wage of US
$3.45 an hour was 15% above the average manufacturing
wage of US$3 an hour (Craypo, 1994, p. 71). During the
1980s, many of the unionized plants in urban areas closed
amidst a wave of strikes to protest requests for wage concessions. By 1986, average meatpacking wages of US$8.24 an
hour were 18% below the average manufacturing wage of US
$9.75. Meatpacking wages continued to fall, and by 1990 the
US$8.73 an hour wage was 24% below the US$10.85 average
manufacturing wage (Craypo, 1994, p. 71).
Meatpacking Workers
Meatpacking has long attracted workers with relatively little
education and sometimes little English, but meatpacking
wages were comparable to those of other manufacturing industries when meat processors were in urban areas. Few
meatpacking workers followed plants from urban to rural
areas, so when the industry moved, it had to nd a new
workforce.
Meat processing facilities in rural areas generally do not
have to compete with other factories for workers, and often
recruit workers from out of the area, especially to staff second
or night shifts. Refugee resettlement in the 1970s and 1980s
brought Asians to the Midwest, and the 1986 IRCA facilitated
the geographical and occupational mobility of newly legalized
Mexicans. Many saw moving from seasonal farm to year-round
meat processing jobs as a step up the US job ladder.
There is little systematic data on employer preferences for
particular types of workers. Poultry plant managers in the late
1980s told interviewers that Asians and Hispanics had a better
work ethic than local Blacks and Whites. Grifth also noted
that economic growth offered local workers other job opportunities, encouraging many to quit meatpacking jobs. Many
immigrant workers moved to meatpacking jobs on their own,
but some plants offered cash bonuses of several hundred
dollars to current workers and others who referred persons
who stayed on the job 60 or 90 days. Networks evolved to
bring US-born as well as Mexican-born Hispanic workers from
South Texas and other areas with high unemployment rates to
midwestern meatpacking plants.
Once a core group of Asians or Hispanics is employed in a
plant, network hiring can take over recruitment, with current
workers bringing friends and relatives to ll vacant jobs
(Grifth, 1988, p. 35). Network hiring shifts most recruitment
and training costs to currently employed workers, who bring
only those who can do the work and often act as the mentors
of newly hired workers. The Los Angeles Times on 1012
November 1996 proled one network that moved workers
along the so-called chicken trail from South Texas to Missouri
(Katz, 1996). Hudson Foods, based just outside Noel, Missouri, paid South Texas recruiter B. Chapman US$175 for each
worker who was referred and hired in its chicken processing
plant. The reporter was selected by Chapman, traveled to Noel,
and lived with 135 other migrant poultry workers in a converted motel, paying US$45 per week in rent.
Hudson employed 200 workers to process 1.3 million
chickens a week. Worker turnover was very high; Hudson
Enforcement
Meatpacking drew the attention of immigration enforcement
agencies during the late 1990s, when an estimated 25% of
meatpacking workers were unauthorized. Operation Vanguard
subpoenaed employment records from meatpacking plants,
compared information provided by newly hired workers on
I-9 forms with government databases, and instructed employers to ask employees who appeared to be unauthorized to
clear up discrepancies in their records before INS agents came
to the plant to interview them. When employees were informed of INS suspicions that they were unauthorized, most of
the workers quit.
Vanguard was attacked by meatpackers, farmers, unions,
and Hispanic groups, prompting INS headquarters to order its
suspension in 2000. The subsequent lack of enforcement
contributed to the jump in the Hispanic share of employment
in meatpacking between 2000 and 2005. However, beginning
in 2006, meatpacking plants were often targeted in raids
seeking unauthorized workers. The Immigration and Customs
Enforcement agency used 1000 agents to inspect workers at six
plants owned by Swift on 12 December 2006, arresting almost
1300 of the 7000 workers employed on the day shift in these
plants. Crider Inc., a poultry processor in Stillmore, Georgia,
lost three-fourths of its 900-strong workforce when ICE agents
mounted a raid on Labor Day weekend in 2006. In the aftermath of the raids, many meatpackers enrolled in E-Verify, the
Internet-based database that allows employers to check the
legal status of newly hired workers.
The result was a reversal of the growing share of Hispanics
in meatpacking between 2005 and 2010. EEOC data, which
report the sex, race, and ethnicity of employees (www.eeoc.
gov/eeoc/statistics/employment/jobpat-eeo1/index.cfm) in most
US establishments, show that the share of Hispanic workers in
food manufacturing and meat packing rose rapidly between
2000 and 2005 but fell between 2005 and 2010. In 2000,
Hispanics were 38% of all employees in animal slaughtering
and 48% of animal slaughtering laborers. The Hispanic share
of animal slaughtering workers rose by approximately 10%
points between 2000 and 2005, and then fell to 2000 levels or
below by 2010.
Reasons for the rising share of Hispanics among laborers in
meatpacking include network hiring and recruitment during
periods of low unemployment. Reasons for the falling share of
Hispanics since 2005 include well publicized workplace raids
in 200607 and I-9 audits since the 200809 recession that
increased unemployment and made year-round meatpacking
jobs that often pay US$12 an hour more attractive, and more
employers enrolling in E-Verify, which may discourage unauthorized workers from applying for jobs.
Community Impacts
The arrival of Hispanic workers can quickly change the face
of rural areas that sometimes have not experienced signicant immigration for a century. The new residents have been
welcomed in most areas, especially those losing people and
jobs. Hispanic immigrant meatpacking workers buy and rent
homes and shop at local stores, helping to stabilize local
economies.
There are also new tensions with demographic change.
Many local residents complain about the side effects of the
changing labor force, including more students with limited
English prociency in local schools and more uninsured patients seeking health care at local clinics and emergency rooms.
Many meat processing plants provide health insurance and
other benets after 60 or 120 days of employment but, with
high turnover, a signicant share of the workers in a particular
plant may not have employer-provided health insurance.
Two extremes mark the reactions of meat processors to
these externalities from hiring migrant workers. Some recognize that they are hiring workers from outside the area with
little English and formal schooling, and some have formed
partnerships with local community colleges and high schools
to offer classes in English, nance, and other life skills to their
workers. For example, Tyson Foods has an education assistance plan that reimburses 75% of the cost of tuition, books,
and fees (up to US$3500 a year) for coursework that helps
to meet the companys business needs. In Grand Island,
Nebraska, Swift & Co. built a two-classroom school near its
plant in 2002 so that workers could attend high school classes
before and after their work shifts; the local school district
provided a teacher and a teacher's aide.
The other end of the spectrum is marked by processors who
say that their major economic contribution is the facility they
provide for local farmers and the payroll they provide to local
workers. Meatpackers who do not make impact payments,
sponsor sports events, and inform community leaders of their
plans may contribute to the backlash against immigration in
some communities. Some cities and counties have voted
against zoning or other changes needed to open or reopen
meat processing facilities.
Many rural counties in the Midwest are losing people,
forcing residents to choose between depopulation and diversity. Over the past 50 years, census-dened rural counties
without a city of at least 2500 people lost more than a third of
residents in 11 Great Plains states, with farm-based counties
away from interstate highways losing the most residents. Of
155
Conclusions
Farm operators, unpaid family workers, and hired workers are
the three major types of workers employed on US farms. Over
the past quarter century, the share of average employment
contributed by hired workers has been rising, so that hired
workers are now about 60% of average employment on US
farms. These hired workers are concentrated in three interrelated ways, by commodity, size of farm, and geography, so
that most hired workers are employed on large farms in
California and a few other states that produce labor-intensive
fruit and vegetable commodities. Dairies and nurseries are also
important employers of farm workers.
Over half of the hired workers on US farms have been
unauthorized since the mid-1990s, and almost all new entrants to the farm workforce are unauthorized. Farm work is
more often a less-than-10-year job than a career, and older
hired workers who nd nonfarm jobs are typically replaced by
youthful newcomers from rural Mexico, giving especially seasonal agriculture something of a revolving-door labor market.
This revolving door is threatened by immigration reforms
that may make it more difcult for newcomers to enter from
abroad. Farm employers want new and modied guest worker
programs to make it easier to hire the foreign workers who are
over two-thirds of US farm workers, whereas worker advocates
argue that there must be strong recruitment, housing, and
wage requirements to protect foreign and US workers. Farm
employers and worker advocates reached a compromise in
2000 known as AgJOBS to legalize currently unauthorized
farm workers and make it easier for farm employers to hire
guest workers in the future, but they have been unable to
persuade Congress to enact AgJOBS.
Instead, the federal government has gradually tightened
border and interior enforcement, and some states have implemented immigration control laws, in ways that have generated
farm labor shortage complaints. Most complaints of labor
shortage reect special circumstances, such as particularly light
or late harvests in remote areas that do not attract workers, but
farmers fear that they could face labor shortages that would
result in sharply higher wages. For this reason, farm employers
have a keen interest in immigration reform proposals.
Given immigration policy uncertainties, many farmers are
hedging their bets. Most oppose federal laws requiring employers to use E-Verify to check new hires and the enactment
156
of state laws penalizing employers and unauthorized workers unless these enforcement efforts are accompanied by
employer-friendly guest worker program. Some employers are
investing in housing so that they can employ H-2A guest
workers, and some are investing in mechanical aids to enlarge
the pool of available workers and labor-saving mechanization
to adjust to fewer and more expensive workers. History is
unlikely to repeat itself and ood the farm labor market with
new workers, as in the late 1980s, but it is not clear whether
and how fas farm labor costs under status quo and immigration
reform scenarios will change.
References
Calvin, L., Marti, P., 2010. The U.S. produce industry and labor: Facing the future in
a global economy. Economic Research Report No. (ERR-106), November. USDA.
Available at: http://www.ers.usda.gov/Publications/ERR106 (accessed 04.02.13).
Craypo, C., 1994. Meat packing: Industry restructuring and union decline. In: Paula,
V. (Ed.), Contemporary Collection Bargaining in the Private Sector. Madison, WI:
Industrial Relation Research Association, pp. 6396.
General Accounting Ofce, 1998. Community Development: Changes in Nebraska's
and Iowa's Counties with large meatpacking workforces GAO/RCED-98-62.
Grifth, D., 1988. The Impact of the 1986 IRCA on the US poultry industry.
A comparative analysis. Washington, DC: Mimeo.
Katz, J., 1996. The chicken trail: New migrant trails take latinos to remote towns.
Los Angeles Times. Available at: http://articles.latimes.com/1996-11-12/news/mn63879_1_latino-migrants/3 (accessed 04.02.13).
Khan, A., Martin, P., Hardiman, P., 2004. Expanded production of labor-intensive
crops increases agricultural employment. California Agriculture 58 (1), 3539.
Available at: http://californiaagriculture.ucanr.org/landingpage.cfm?article=ca.
v058n01p35&fulltext=yes (accessed 04.02.13).
MacDonald, J., Ollinger, M., 2000. Consolidation in Meatpacking: Causes and
concerns. Agricultural Outlook. JuneJuly, 2326 and Structural Change in U.S.
Chicken and Turkey Slaughter. Agricultural Economic Report 787. Washington,
DC: Economic Research Service, USDA.
Martin, P., 1994. Good intentions gone awry: IRCA and U.S. agriculture. American
Academy of Political and Social Science 534, 4457. Available at: http://www.
jstor.org/stable/1048497 (accessed 04.02.13).
Martin, P., 1998. The endless debate: Immigration and US Agriculture. In: Duignan,
P., Gann, L. (Eds.), The Debate in the United States over Immigration. Stanford:
Hoover Institution, pp. 79101. Available at: www-hoover.stanford.edu (accessed
04.02.13).
Martin, P., 2003. Promise Unfullled: Unions, Immigration, and Farm Workers.
Ithaca: Cornell University Press. Available at: http://www.cornellpress.cornell.
edu/book/?GCOI=80140100792940&CFID=9652803&CFTOKEN=
f1155d49f162eed5-5AABB7F9-C29B-B0E5-30D66D992EBABD0B&jsessionid=
84301cb0683d5770849b171b6b4e272f564cTR (accessed 04.02.13).
Martin, P., 2005. AgJOBS. New solution or new problem. UC Davis Law Review 38
(3), 973991. Available at: http://lawreview.law.ucdavis.edu/articles/Vol38/
vol38_no3.html (accessed 04.02.13).
Martin, P., 2006. Immigration reform: Implications for agriculture. ARE Update 9 (4).
Available at: http://giannini.ucop.edu/are-update/9/4/immigration-reform-implic/
(accessed 04.02.13).
Martin, P., 2009. Importing Poverty? Immigration and the Changing Face of Rural
America. Yale University Press. Available at: http://yalepress.yale.edu/yupbooks/
book.asp?isbn=9780300139174 (accessed 04.02.13).
Martin, P., 2012. Agriculture and migration after Arizona. ARE Update 16 (1), 68.
Available at: http://giannini.ucop.edu/are-update/16/1/agriculture-and-migration
(accessed 04.02.13).
Martin, P., Huffman, W., Emerson, R., Edward Taylor, J., Rochin, R. (Eds.), 1995.
Immigration Reform and US Agriculture. Berkeley, CA: Division of Agriculture
and Natural Resources Publication.
Martin, P., Martin, D., 1993. The Endless Quest: Helping America's Farm Workers.
Boulder: Westview Press.
Martin, P., Mines, R., Diaz, A., 1985. A prole of California farmworkers. California
agriculture. Available at: http://californiaagriculture.ucanr.org/landingpage.cfm?
article=ca.v039n05p16&abstract=yes (accessed 04.02.13).
Martin, P., Midgley, E., 2006. Immigration: Shaping and reshaping America, vol.
61. Washington DC: Population Reference Bureau. Available at: http://www.prb.
org/Publications/PopulationBulletins/2006/ImmigrationShapingandReshaping
America.aspx (accessed 04.02.13).
Migration News, 2007a. Senate. Immigration reform stalls. vol. 14. No 3. July.
Available at: http://migration.ucdavis.edu/mn/more.php?id=3294_0_2_0
(accessed 04.02.13).
Migration News, 2007b. DHS: No match enforcement. vol. 14. No 4. October.
Available at: http://migration.ucdavis.edu/mn/more.php?id=3315_0_2_0
(accessed 04.02.13).
Migration News, 2012b. DHS. Border, interior. vol. 19. No 4. October. Available at:
http://migration.ucdavis.edu/mn/more.php?id=3784_0_2_0 (accessed 04.02.13).
Mines, R., 2010. Indigenous farmworkers. Mimeo. Available at: http://rickmines.
wordpress.com/indigenous-farmworkers/ (accessed 04.02.13).
Oliveira, V., 1989. Trends in the hired farm work force, 1945-87. Washington: US
Department of Agriculture, Economic Research Service, Agricultural Information
Bulletin 561. Available at: naldc.nal.usda.gov/download/CAT89917698/PDF
(accessed 04.02.13).
Pigot, M., 2003. Decent work in agriculture. Prepared for ILO symposium, April 30.
Available at: http://www.ilo.org/wcmsp5/groups/public/ed_dialogue/actrav/
documents/publication/wcms_111457.pdf (accessed 04.02.13).
Rural Migration News, 1996. House rejects guest workers. vol. 2. No 2. April.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=111_0_3_0
(accessed 04.02.13).
Rural Migration News, 2008. California. Heat deaths, drought, data. vol. 14. No 4.
October. Available at: http://migration.ucdavis.edu/rmn/more.php?id=1339_0_3_0
(accessed 04.02.13).
Rural Migration News, 2009a. AgJOBS: Provisions, eligibility. vol. 15. No 3. July.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=1466_0_4_0
(accessed 04.02.13).
Rural Migration News, 2009b. California. Sales, strawberries vol. 15. No 4. October.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=1491_0_5_0
(accessed 04.02.13).
Rural Migration News, 2010a. AgJOBS, Immigration reform. vol. 16. No 1. January.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=1508_0_4_0
(accessed 04.02.13).
Rural Migration News, 2010b. DHS: Border, interior, services. vol. 16. No 2. April.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=1533_0_4_0
(accessed 04.02.13).
Rural Migration News, 2011. H-2A Reform, Cases H-2B. vol. 17. No 4. October.
Available at: http://migration.ucdavis.edu/rmn/more.php?id=1643_0_4_0
(accessed 04.02.13).
Wells, M., 1996. Strawberry Fields: Politics, Class and Work in California
Agriculture. Ithaca, NY: Cornell University Press.
Relevant Websites
http://www.doleta.gov/agworker/naws.cfm
National Agricultural Workers Survey (NAWS).
www.youtube.com/watch?v=BNbQ0xdLXqc
Agricultural Law
TJ Centner, The University of Georgia, Athens, GA, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Ad valorem taxation A tax based on the fair market value
of the real estate. The value is calculated on the property's
potential for its highest and best use.
Appropriation doctrine State legislative delineation of
rights and priorities to water resources.
Conservation easement An easement that sets forth
conservation objectives such as preserving wildlife habitats,
riparian lands, forests, or farmland.
Point-source pollution Water pollution from a single
point such as a pipe or concentrated animal feeding
operation.
Preferential assessment The modication of ad valorem
taxation under which qualifying land is assessed according
to its current use value rather than fair market value.
Introduction
The hard economic times of the 1930s contributed to ideas
that farmers and farm communities needed legal expertise. In
1933, V. O. Braun, a lawyer from Owosso, Michigan, published a book titled, Agricultural and Business Law for the Farmer.
Twenty years later, faculty from land grant universities in the
north-central region recognized the changing structure of
agriculture and published proceedings from a seminar titled,
Legal Aspects of the Family Farm Corporation. The communications and ideas of this faculty led to discussions of
having more structured venues for communicating information dealing with agricultural law.
Meanwhile, other legal experts developed materials and
published information on agricultural law. In 1979, the Agricultural Law Journal (discontinued) was initiated to provide
scholarly articles about agricultural legal issues. Articles in law
reviews and other publications provided a foundation for
agricultural law in the 1980s. A multivolume treatise, Harl,
Agricultural Law, provided in-depth coverage of agricultural law
topics. The authors and their literature shaped the issues, legislation, and jurisprudence forming agricultural law.
Agricultural law includes numerous legal topics and agricultural law practices have changed over the years. The early
issues centered on property and business arrangements. In the
1970s, many agricultural lawyers spent considerable amounts
of time on property taxation and estate planning. Farm nancial issues in the 1980s drew attention to nancial matters
including bankruptcy. The industrialization of agriculture and
concerns about environmental quality in the 1990s meant that
agricultural law expanded to encompass issues such as water
pollution from concentrated animal feeding operations
(CAFOs). Issues on genetically modied organisms, animal
welfare, agricultural labor, and food safety have also become
important. The potential breadth of an agricultural attorney is
unlimited. Agricultural law can be described as the application
doi:10.1016/B978-0-444-52512-3.00254-0
157
158
Agricultural Law
Agricultural Law
known as preferential assessment. Preferential assessment involves the assessment of qualifying land at its use value rather
than fair market value. Generally, the adoption of preferential
assessment requires an amendment to the state constitution
and the adoption of legislation delineating use value qualications. Under preferential assessment, landowners may be
required to sign contractual agreements to keep their lands in
agricultural production for a number of years. Legal counselors
provide property owners advice about the advantages and potential problems of entering such agreements.
Agricultural lawyers are also involved with efforts to preserve farmland. They work with landowner clients to determine whether to participate in state programs involving
preferential assessment, farmland preservation, conservation
easements, and transferrable development rights. Agricultural
lawyers may also be involved in helping communities develop
zoning ordinances and agricultural districts that are supportive
of continued agricultural production.
In cases where owners want to protect agricultural land,
legal counsel may draft a conservation easement to preclude
the future development of the property. A conservation easement sets forth conservation objectives to preserve wildlife
habitats, riparian lands, forests, or farmland. An easement may
delineate purposes for which the property may not be used
and its restrictions are perpetual. Under the applicable state
law, an organization holds the conservation easement and is
granted the power to constrain the rights of the landowner.
By voluntarily placing a conservation easement on property
to preserve farmland, landowners qualify for tax benets. Because the property cannot be developed, its real estate taxes
may be lower than comparable properties without an easement. The value of a donation of a conservation easement is
deductible from the donor's income under federal income tax
law. The value of property subject to a conservation easement
may also be taken into account for estate tax purposes.
Another institution used to preserve farmland involves a
state or local program for transferable development rights
(TDRs). Under a TDR program, a rural landowner sells development rights to private developers and the farmland is
limited in its future uses. By purchasing development rights,
developers are granted rights to develop properties at higher
densities in nonrural areas. Under this arrangement, agricultural producers receive compensation without having to sell
or develop their lands.
Legal counselors may be called on to assist clients in
forming farm corporations that comply with their state's legislation against corporate farms. Several states in the upper
Midwest have delineated prohibitions on the corporate ownership of farmland with exceptions for family farms and active
agricultural producers. Justications for limiting corporations
from owning farmland include a dislike for industrialized
agribusiness and absentee ownership as well as concerns about
environmental damages and rural depopulation.
159
160
Agricultural Law
Agricultural Nuisances
With the expansion of residential areas into the countryside in
the 1950s, conicts between agricultural practices and nonfarm residential property users became a problem. Persons
living in suburbia did not like the noises, dust, and smells that
accompany aspects of agricultural production. Many of the
objections centered on practices involving animal manure.
Agricultural lawyers were called on to defend producers
against lawsuits based on nuisance. If a jury found that an
agricultural practice was a nuisance, the producer could be
enjoined from continuing the practice. This resulted in producers not being able to protably continue with their farming
operations. Moreover, producers were hesitant to make investments in their operations because of uncertainties about
future complaints from neighbors.
To counter injunctive relief available in nuisance lawsuits,
state legislatures adopted antinuisance laws. These laws became known as right-to-farm laws because by precluding injunctive relief under nuisance law, they enable producers to
continue farming despite the objectionable activities. A majority of the right-to-farm laws adopted a coming-to-thenuisance exception under which a person who moved next to
an established farm could not claim the farm's activities were a
nuisance. In this manner, right-to-farm laws enabled producers to continue with activities despite the fact that the
neighbors felt the activities were a nuisance. Right-to-farm laws
in some states also offer antinuisance protection to qualifying
agricultural businesses.
Because right-to-farm laws delineate a state's antinuisance
rules, they preempt attempts by local governments to regulate
agricultural nuisances. However, local governments may continue to regulate agricultural activities under zoning or local
health laws unless state legislation says otherwise. Although
right-to-farm laws operate to protect producers against some
nuisance lawsuits, legal counsel may be required to evaluate
whether the law applies to the facts of a given situation. Each
state's right-to-farm law contains specialized provisions delineating qualications before the protection applies. Moreover, amendments to state right-to-farm laws have resulted in
very different provisions for each state.
Another issue under right-to-farm laws is whether the
provisions of a state law constitute an unconstitutional taking.
In 1998, an Iowa right-to-farm law was found to create an
easement that constituted an unconstitutional taking of private property (Centner, 2000). The court felt that the Iowa
legislature went too far in attempting to preserve farmland,
and in a subsequent lawsuit, this was related to the protection
of property rights provided by the Iowa Constitution. Safeguards and regulatory provisions incorporated in right-to-farm
laws of other states should thwart similar constitutional
challenges.
Business Arrangements
Another prominent area of agricultural law deals with business
arrangements used by producers and related rms in the
production and marketing of agricultural products. Legal
counselors give advice on contractual agreements, help clients
form business entities, oversee documents used in securing
nancing, assist indebted operators with bankruptcy, and
provide advice on estate planning.
Producers generally seek assistance from legal counsel
whenever entering a major contractual obligation to ascertain
that the agreement accomplishes its intended purpose without creating any unnecessary complications. Important contracts include agreements for forming businesses, purchasing
businesses, buying and selling property, mortgages, leases,
loans, easements, lien releases, and security agreements that
pledge collateral as security for borrowing money. Counsel can
explain the meaning of legal terms, add provisions to offer
protection against potential problems, suggest the removal
of onerous or unnecessary provisions, and offer advice on
alternatives.
Agricultural producers raising large numbers of animals,
especially hogs and poultry, often sign production or marketing contracts with business rms known as integrators. The
contracts are written by the integrators with detailed provisions affecting production activities. Under a production
contract, the producer feeds and cares for the animals and is
paid pursuant to a contractual pricing formula determined by
the performance of the animals. Under a marketing contract,
the producer agrees to sell or deliver animals to an integrator
according to pricing terms set in the contract. Agricultural
lawyers may be needed to offer advice on the terms of these
contracts, although producers may have few options for alternative marketing outlets for their animals (Looney and
Poole, 1999).
Agricultural law practitioners help clients make decisions
about whether to operate as a sole proprietorship or to form a
Agricultural Law
business entity. Producers may nd it advantageous to form a
business entity to raise funds, have family members or friends
as partial owners, limit liability for losses and accidents, and
transfer assets on death. Each state has separate legislation
governing business entities that include corporations, Subchapter S corporations, cooperatives, partnerships, limited
partnerships, and limited liability companies.
A disadvantage of some business entities is income taxation
at the rm level. Legal counsel can explain how each business
entity might t the needs of a client's farming situation. Favorable state legislation regarding limited liability companies
suggests that this form of business is well suited for many
small businesses. A limited liability company allows income
to pass through to owners so that there is only a single level
of income tax and liability is limited to the assets of the
company.
A major reason for forming a business entity is liability
for accidents. Farming is a dangerous occupation given the
chemicals and equipment used in producing food and animals. Any farm or business that employs nonfamily workers or
has people coming onto the property should be concerned
about being held liable for damages from an accident. For
example, a worker may suffer severe injuries from operating a
piece of farm equipment. This suggests that the operator may
want to consider forming some type of business entity that
would own the land and equipment and employ the worker.
The producer could own other assets outside the business
entity, such as a house, bank accounts, stocks, and bonds. By
structuring the business entity as owner of machinery and
property and the employer of workers, a producer may successfully shield assets outside the entity from liability related
to a major accident.
Over the years, agricultural lawyers have been involved
with helping producers form agricultural cooperatives, and
assisting clients in their dealings with their cooperatives. Distinct legal provisions for this form of business and controversies on paying out dividends to members have meant that
specialized legal counselors are needed to assist producers as
well as cooperatives.
Counselors help agricultural producers and agribusiness
rms grapple with problems connected with credit and security interests (Meyer, 2010). Producers often seek counsel to
assist with documents involved in securing nancing for the
purchase of seeds, fertilizer, equipment, and other production
inputs. Agricultural producers depend on the advice of agricultural lawyers before signing these contractual arrangements
to ascertain that terms are reasonable and do not delineate any
adverse provision that may interfere with future business
arrangements.
When borrowing money to purchase personal property,
borrowers sign a security agreement listing collateral as security for the repayment of the loan. Security agreements have
signicant ramications concerning ownership and rights in
property. Legal advice is important when delineating terms of
a security agreement because of the options available for listing collateral. Collateral may include accounts, goods, stock,
livestock, equipment, inventory, and farm products. Special
rules apply to farm products as opposed to other types of
collateral so different nancial arrangements may be needed to
safeguard the interests of a client.
161
162
Agricultural Law
Agricultural Law
Water Resources
The production of food and ber products is dependent on the
availability of water resources. Both water quantity and quality
affect the viability of crop and animal production. In more and
more situations, agricultural producers need legal advice on
how to comply with legal requirements dealing with water
resources. Additional legal advice may examine the future
availability of sufcient water and how to address issues of
water quality.
Owing to the provisions of the US Constitution, the federal
government is involved in water issues that affect agricultural
producers. Provisions regarding treaties with Indian tribes,
compacts between and among states, and the Commerce
Clause have justied Congressional action in enacting regulations governing water allocations, ood control, irrigation
projects, and pollution. Simultaneously, each state has its own
water law. Legal counsel may be called on to assist producers
in determining rights to water and the legality of using water
from a water body.
State water law may incorporate principles of the riparian
doctrine, delineate an appropriation doctrine governing water
rights, or use a combination of both. The riparian doctrine was
adopted by most states in the eastern part of the US. Water
usage is part of land ownership and applies to landowners
adjacent to surface waters. There is a division between natural
use and articial uses of water. A landowner may use unlimited quantities of water for natural uses but only reasonable
quantities for articial water uses such as impoundments and
irrigation.
Conicts involving insufcient quantities of water in states
following the riparian doctrine have led state legislatures to
adopt water-permitting systems. This means that water usage
for irrigating crops is governed by the riparian doctrine
amended by state appropriation provisions. Counsel may be
163
Environmental Issues
Producers have a responsibility in disposing of their byproducts and wastes responsibly so that they do not adversely
affect others. Given damages that may be caused by pollutants,
numerous environmental laws have been enacted and many
apply to agricultural production (Centner, 2004). In pursing
their activities, agricultural producers must desist from practices that release pollutants in violation of federal, state, and
local environmental laws and regulations.
Turning to water quality, agriculture is listed by the US
Environmental Protection Agency (EPA) as the major polluter
of streams and lakes in the country. Under the US Clean Water
Act, EPA has adopted numerous regulations that address the
impairment of water quality by agricultural activities. Federal
law distinguishes point sources of pollutants from nonpoint
sources. Any point-source discharge of pollutants into federal
waters needs a permit. Nonpoint-source pollution is regulated
by the states.
A major issue involves pollutants from CAFOs. CAFOs are
listed as point sources of pollution so that any CAFO with a
discharge of pollutants into federal waters needs a National
Pollution Discharge Elimination System permit. As a result of
litigation commencing in 1989, EPA agreed to develop rules
for CAFO discharges that would comply with the Clean Water
Act. In 2003, 2008, and 2012, EPA adopted revised regulatory
provisions for CAFOs. Agricultural lawyers continue to advise
CAFO operators on the requirements delineated by the regulatory and judicial changes to the federal provisions.
164
Agricultural Law
Other Issues
Agricultural lawyers have become involved with and provide
advice on numerous other issues affecting agriculture.
These efforts are important in helping agricultural producers
develop and maintain viable business operations, respond to
social expectations, and adjust their operations to changes in
technology and the marketplace. Issues include food safety,
genetically modied seeds, organic production, controlling
diseases, migrant labor, animal welfare, energy, and local food
production.
Food safety has become an important concern for many
people, and numerous federal, state, and local regulations
have been enacted to help guarantee safe food supplies. Some
laws prescribe requirements that help guard against unwholesome foods and others provide for the inspection of
food items and businesses processing food products. Federal
agencies with food safety oversight include the Food and Drug
Administration (part of the US Department of Health and
Human Services) and the Food Safety and Inspection Service
(part of the US Department of Agriculture). Many states have
their own food safety provisions and inspection programs.
Outbreaks of food-caused illnesses show the need for food
safety regulations. Although governments are in charge of
prosecuting persons and rms that violate laws in placing
unwholesome foods in the marketplace, legal counselors may
be called to offer advice to persons injured by unwholesome
food items. Counselors also help clients meet the regulatory
requirements. This may include determining if a regulation
applies to a client's activities, helping farm businesses comply
with applicable regulations, or responding to allegations of a
failure to comply with safety requirements.
A special food safety issue involves the sale of raw (unpasteurized) milk. To safeguard public health, federal law
Agricultural Law
165
166
Agricultural Law
Conclusory Comments
Although this article has focused on legal issues in the US,
several topics may be expected to be important internationally
(Cardwell, 2004; Rogers, 2008). Agricultural lawyers in most
countries assist producers with legal documents concerning
land, contracts, and nancing arrangements. They also may
assist in restructuring operations to take advantage of support
programs and marketing opportunities. In other cases, counselors are involved in land reform.
Agricultural lawyers might be involved in three policy
issues that continue to affect world food supplies and the
provision of food to the hungry. Food safety, food security,
and trade impediments are matters that governments can address to facilitate better living conditions.
People all over the world are concerned about food safety.
The agricultural law community can help governments develop appropriate regulatory provisions to reduce risks of
contamination during the production and marketing of food
products. Moreover, persons involved in marketing unwholesome food products need to be held accountable for
damages.
Food security continues to be a problem not only in the
developing world, but also for many people in the developed
world. The availability of sufcient food supplies may be exacerbated by climate change. The legal community needs to
foster programs and ideas to help get food to persons who are
hungry.
Legal counselors may also need to become involved in
opposing regulations that constitute barriers to international
trade. Countries are able to adopt phytosanitary measures relating to food safety and animal health with respect to imported pests and diseases. However, protectionist interest
groups sometimes convince governments to adopt regulations
such as domestic subsidies for agricultural products, import
quotas, and standards that differentially impact foreign suppliers. A major source of disagreement involves import restrictions on food items produced from genetically modied
organisms. Are the restrictions a justiable precautionary approach to a risky technology or an unjustiable barrier to
trade? Another potential barrier may be an environmental
Agricultural Law
References
Cardwell, M.N., 2004. The European Model of Agriculture. Oxford: Oxford University
Press.
Centner, T.J., 2000. Anti-nuisance legislation: Can the derogation of common law
nuisance be a taking? Environmental Law Reporter 30, 1025310260.
Centner, T.J., 2004. Empty Pastures: Conned Animals and the Transformation of
the Rural Landscape. Champaign, IL: University of Illinois Press.
Centner, T.J., Ferreira, S., 2012. Governments' ability to take actions to confront
incursions of diseases a case study: Citrus canker in Florida. Plant Pathology
61, 821828.
Centner, T.J., Newton, G.L., 2011. Reducing concentrated animal feeding operations
permitting requirements. Journal of Animal Science 89, 43644369.
167
Endres, A.B., 2004. State authorized seed saving: Political pressures and
constitutional restraints. Drake Journal of Agricultural Law 9, 323357.
Endres, J.M., Grossman, M.R., 2004. Air emissions from animal feeding operations:
Can state rules help? Penn State Environmental Law Review 13, 151.
Geyer, L.L., 1997. A comparison of farmer bankruptcy and insolvency statutes or
selling the farm. Drake Law Review 45, 331356.
Grossman, M.R., 2010. Climate change and the law. American Journal of
Comparative Law 58, 223255.
Hamilton, N.D., 2011a. Moving toward food democracy: Better food, new farmers,
and the myth of feeding the world. Drake Journal of Agricultural Law 16,
117145.
Hamilton, N.D., 2011b. Farming uncertain climate future: What COA 15 means for
agriculture. University of Illinois Law Review 2011, 341359.
Looney, J.W., Poole, A.K., 1999. Adhesion contracts, bad faith, and economically
faulty contracts. Drake Journal of Agricultural Law 4, 177195.
Meyer, K.G., 2010. A garden variety of UCC issues dealing with agriculture.
University of Kansas Law Review 58, 11191177.
Rogers, C., 2008. Agricultural Law. West Sussex: Tottel Publishing Haywards
Health.
Schutz, A.B., 2011. Toward a more multi-functional rural landscape: Community
approaches to rural land stewardship. Fordham Environmental Law Review 22,
633689.
Uchtmann, D.L., 2007. American Agricultural Law Association: Past, present and
future. Drake Journal of Agricultural Law 12, 116.
Relevant Websites
http://www.agandfoodlaw.com/2009/01/about-this-blog.html
Agricultural and Food Law and Policy Blog.
http://aglaw-assn.org/index.html
American Agricultural Law Association.
http://apps.americanbar.org/dch/committee.cfm?com=GP206000
American Bar Association Agricultural Committee.
http://www.law.drake.edu/academics/agLaw/
Drake Agricultural Law Center.
http://www.martindale.com/Agricultural-Law-law-rms-countries.htm
Martindale Agricultural Law Firms.
http://new.nationalaglawcenter.org/
National Agricultural Law Center.
http://law.psu.edu/academics/research_centers/agricultural_law_center/current_issues
Penn State Agricultural Law.
http://law.uark.edu/academics/llm/
University of Arkansas LL.M. Program.
Agricultural Mechanization
AL Olmstead, University of California, Davis, CA, USA
PW Rhode, University of Michigan, Ann Arbor, MI, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Biological innovation Improvements in seed, fertilizer,
and cultural practices directed to adapting plants to new
environments, combating pest threats, and increasing yields
and labor productivity; also improvements in breeding
stock, feeding practices, and health directed to increasing
livestock productivity.
Combine A mobile harvesting machine that combined the
cutting and threshing operations into one device. The early
combines were mammoth machines often powered by
about 40 equines.
Cotton gin A machine perfected by Eli Whitney in 1793 to
separate the seed and ber in Upland cotton.
Cradle A scythe with a small wooden frame attached at
the rear of the cutting blade used to harvest small grains.
The frame caught cut grain and stalks helping to prevent the
grain from shattering. In North America this device replaced
the sickle and scythe in the late eighteenth century. It in turn
was replaced by the mechanical horse-drawn reaper
beginning in the late 1830s.
General purpose tractor This machine which rst
appeared in 1924 spaced the wheels so that the tractor could
168
doi:10.1016/B978-0-444-52512-3.00236-9
Agricultural Mechanization
169
170
Table 1
Agricultural Mechanization
Method
Acres/day
Scythe
Cradle (late eighteenth century)
Reaper (1833)
Self-raker (1854)
Self-binder (1881)
1/31/2
1
1.52
22.5
1012
Source: Compiled from Hayami, Y., Ruttan, V., 1985. Agricultural Development: An
International Perspective, revised ed. Baltimore: Johns Hopkins University Press, p. 81.
Agricultural Mechanization
Tractors
As one has seen, the quest to apply mechanical power to the
farm long predated the gasoline tractor. Farm steam engines
probably rst made their appearance in cotton gins, and mobile engines were adapted to power threshing machines in the
late 1840s. A number of early inventors constructed massive
steam plows. In 1858, Joseph Fawkes exhibited a steam plow
at the Illinois State Fair. In the decade following the Civil War,
many manufactures ventured into constructing prototypes.
Philander H. Standish of Martinez, California was an important pioneer. On May 10, 1868, Standish patented a steam
engine plow, and according to contemporary accounts actually
plowed 100 acres with it. In 1868, a Standish steam traction
engine named The Mayower drew huge crowds at the
California State Fair. But for all the interest, the monster
machine never was a mechanical or nancial success.
An alternative was offered by the English cable system of
plowing. The cable system consisted of two stationary steam
engines located at opposite sides of a eld. Steel cables attached to the engines pulled the plow across the eld with the
engines alternating the pulling. This method required ve to
eight men: a foreman, two engineers, one or two teamsters,
and two plowmen. The cable plows were expensive, and the
steel cables, which needed replacement roughly every year,
cost between $600 and $900 each. The expense limited the
market to a few experimenters with very large estates. A signicant problem with the early steam traction engines was
their reliance on the models built for steam threshing that
made them unsuitable for plowing. The traction gears were not
strong enough to pull the drawbar, the drive wheels were not
large enough, the machines were difcult to operate, and the
plows too often snagged in uneven terrain.
The 1870s and early 1880s were a period of experimentation, with no individual or model dominating. Gradually,
through trial and error, various technological changes were
made to increase the practicality of mobile steam plows. Two
industry leaders emerged, both of which were located in
Stockton, California and both of which were active in the early
combine harvester industry. Daniel Best and the Holt Brothers
both produced models with horizontal boilers. These weighed
over 10 tons, could plow approximately 40 acres a day, and ca.
1890 sold for approximately $4500. Because they were so large
and so expensive, their primary market was the large California
wheat ranches. By 1890, eastern and Midwestern producers
such as J. I. Case of Racine, Wisconsin were manufacturing
steam traction engine plows. The Case machine was
suitable for plowing, harrowing, hauling, running threshing
machines and sawmills, rolling streets, and pulling combines
as well as plows (Wik, 1953).
Steam traction engines could be built to run off of virtually
any type of fuel. In the East, farmers often used coal and wood,
but in the West the price of these fuels was generally so high
that manufacturers constructed straw-burning engines. By the
turn of the century, steam traction plows were established as
an alternative to horse-drawn plowing in the West. In the East,
steam plowing did not become popular until the early years of
the twentieth century, with the advent of stronger and lighter
weight engines. Everywhere, improved designs increased steam
pressure and enhanced reliability.
171
Agricultural Mechanization
30000
Works stock
5000
Tractors
4500
25000
4000
3500
20000
3000
2500
15000
2000
10000
1500
1000
5000
172
500
0
1910
0
1915
1920
1925
1930
1935
1940
1945
1950
1955
1960
Figure 1 Number of draft animals and tractors in the US (191060). Reproduced from Olmstead, A.L., Rhode, P.W., 2001. Reshaping the
landscape: The impact and diffusion of the tractor in American agriculture, 191060. Journal of Economic History 61 (3), 670.
Agricultural Mechanization
173
174
Agricultural Mechanization
lift system, the use of mounted tools, from plows to cultivators, soared. Since 1900, the manufacture of tillage equipment has followed a trend common to many industries. Seven
or eight full-line companies, that is, producers of tractors
as well as implements, have captured most of the market.
These companies were, in order of importance (ca. 1935),
International Harvester, Deere, Case, Oliver, Allis-Chambers,
Minneapolis-Moline, Massey-Harris, and Avery. In 1937, these
eight rms produced approximately 95% of the tractor plows
sold in the US, nearly 80% of the disk and spring-tooth harrows, about three-fourths of the spike-tooth harrows, around
two-thirds of the sulky plow and two-horse walking plows,
and somewhat less than half of the one-horse walking plows.
As smaller tractors became popular after 1915, two- and
three-bottom gang plows rose in signicance. At rst, horsetype plows often were adapted to two- and three-plow tractors,
but the hitching arrangements and their ability to withstand
the increased stress left much to be desired. For example, the
rst tractor plows were attached only with chains and were
impossible to back up. More rigid hitches remedied this failing. Other improvements, such as heat-treated parts and
stronger frames, made the plows more durable. Although the
changes in design were relatively minor, the quality improvements were dramatic. A study by leading agricultural engineers
judged the tractor plow of 1932 was about twice as good as
that of 191014. With the advent of power lifts on tractors
around 1930, plows mounted directly onto the tractor were
adapted. The carriage or wheeled frame could be discarded,
and lifting and adjustment performed mechanically. The
introduction of impediments for the Ferguson three-point
linkage system and hydraulic lift further increased efciency
(Bainer et al., 1953, ch. 6). Tractor manufacturers saw the need
to better match their machines and the equipment they towed,
and many leading rms began to offer specially designed
tillage equipment as early as the 1920s. This led to the integration of many equipment makers and tractor companies
into full-line rms.
Besides improved plows, several other pieces of primary
tillage equipment came into vogue in the late nineteenth
century. One was the lister or middlebuster, which was
essentially two moldboard plows set back-to-back to throw
soil to both sides. Much like plows, listers were available in
walking, riding, and tractor-mounted models. Disk plows also
appeared by at the end of the nineteenth century. The disks
were set at an angle both to the ground and the direction of
motion. For tractor gangs, four to six disks were the most
common. Replacing the share, moldboard, colter, and jointer
of the moldboard plow with a rotating disk was rst conceived
as a means of reducing draft. But disks lacked the suction of
the moldboard plow and needed greater mass to maintain
penetration. The heavier frames and added weights increased
the disk's draft. Disk plows do not turn the soil as thoroughly
as moldboards. The choice of whether to use a disk or a plow
often depended on the type of soil.
Three types of harrows were employed on American farms:
the spike-tooth, the spring-tooth, and the disk harrow. The
oldest of these is the spike-tooth harrow, which traces its ancestry back as far as the plow. The rst spike-tooth harrows
were purportedly of a triangular or A conguration, reminiscent of the ancient Roman harrows. The triangular models
Agricultural Mechanization
Table 2
175
Method
Quantity ()
Hand (1788)
Whitney (1793 Saw Gin)
Whitney (1800 Model)
Improved (1866 Gin)
2
80
350
3000
Source: Compiled from Lebergott, S., 1984. The Americans. New York: W.W. Norton,
p. 170.
176
Agricultural Mechanization
Agricultural Mechanization
Perspectives
To this juncture, our story has emphasized the role of
mechanization in reshaping the productivity and structure of
American agriculture. Other forces arising from better and
more intensive applications of chemistry, biology, and genetics to agriculture have also played a major role. Social
scientists long argued that in the US relatively cheap land and
expensive labor led farmers, inventors, rms, and governments to concentrate on mechanization rather than other
forms of technical change (which for simplicity the authors
have called biological innovations). By this reasoning, biological innovations such as hybrid corn only became prominent after the 1930s well after the closing of the frontier
and when, according to the standard account, an increasing
scarcity of land and a rapid decline in commercial fertilizer
prices made such innovations protable. Proponents of this
view explicitly argued that mechanical technologies were almost exclusively labor saving they increased the output per
worker. Biological technologies were primarily land saving
they increased output per acre (Cochrane, 1979, pp. 201
202). This stylization seemed to t the long sweep of
American development, because until the 1930s output per
worker had risen considerably, but output per acre for major
crops had changed little. Although still repeated, this general
view has recently been discredited.
For many reasons, trends in output per acre understate the
contributions of biological innovations. Agricultural production is an inherently biological process that uses organisms
to transform sunlight and soil nutrients into food and ber.
Evolving pests and diseases constantly threaten the efciency
of this transformation process. Machines may become obsolete, and they can wear out; but a new machine of the outdated
design will work more or less like the equipment it replaced.
This is not true for biological technologies. Farmers and scientists have long understood the Red Queen effect: one has to
run fast just to stay in one spot. A once productive plant variety
can become worthless as pathogens evolve to penetrate its
defenses. Moreover, the introduction of invasive species from
foreign lands can dramatically cut yields. In addition, yields
often suffered as agriculture moved westward. Introducing
production to new environments required biological learning
that involved adapting plants to meet new, often hostile,
conditions.
The once strict association of machines with only saving
labor and of biological advances with only saving land is very
questionable. As noted above, the tractor saved over 160
million acres of crop and pastureland by the 1940s, and better
cotton varieties increased slave picking productivity by four
times in the half century before the Civil War. These are not
isolated examples. What sense does it make to say that better
tillage equipment are machines so they save labor, but if a
farmer replaces some of this equipment with improved
herbicides, this saves land? Once one abandons the old
paradigm and reexamines American agricultural development,
a record of biological innovation emerges that went hand in
177
References
Bainer, R., Kepner, R.A., Barger, E.L., 1953. Engineering Elements of Farm
Machinery. Ann Arbor, MI: Edwards Brothers.
Brodell, A.P., 1952. Harvesting Small Grains and Soybeans and Methods of Storing
Straw. Washington, DC: USDA US Bureau of Agricultural Economics, FM-91.
Christensen, T.P., 1939. First cream separator. Hoards' Dairyman 84, 338.
Cochrane, W.W., 1979. Development of American Agriculture: A Historical Analysis.
Minneapolis, MI: University of Minnesota Press.
Davidson, J.B., 1931. Agricultural Machinery. New York: John Wiley & Sons.
Edwards, E.E., 1949. Europe's contribution to the American dairy industry. Journal of
Economic History 9 (Supplement: The Tasks of Economic History), 7884.
Forste, R.H., Frick, G.E., 1979. Dairy. In: Schertz, L.P. (Ed.), Another Revolution in
U.S. Farming? Washington, DC: USDA, pp. 119147.
Fussell, G.F., 1966. The English Dairy Farmer: 15001900. London: Frank Cass & Co.
Gray, L.C., 1941. History of Agriculture in the Southern United States to 1860.
New York: Peter Smith vol. II.
Gray, R.B., 1954. Development of the Agricultural Tractor in the United States.
Beltsville, MD: USDA Information Series No. 107.
Hutchinson, W.T., 1930. Cyrus Hall McCormick: Seedtime, 18091856. New York:
The Century Co.
Jensen, J.M., 1986. Loosening the Bonds: Mid-Atlantic Farm Women, 17501850.
New Haven, CT: Yale University Press.
Jensen, J.M., 1988. Butter making and economic development in mid-Atlantic
America, 17501850. Signs 13 (4), 813829.
Lakwete, A., 2003. Inventing the Cotton Gin: Machine and Myth in Antebellum
America. Baltimore, MD: Johns Hopkins University Press.
McKibben, E.G., Griffen, R.A., 1938. Changes in farm power and equipment:
tractors, trucks and automobiles. Works Progress Administration. National
178
Agricultural Mechanization
Quick, G., Buchele, W., 1978. The Grain Harvesters. St. Joseph, MI: American
Society of Agricultural Engineers.
Rogin, L., 1933. Introduction of Farm Machinery in Relation to the Productivity of
Labor in the Agriculture of the United States During the Nineteenth Century.
Berkeley: University of California Press.
Street, J.H., 1957. The New Revolution in the Cotton Economy: Mechanization and
Its Consequences. Chapel Hill, NC: University of North Carolina Press.
US Bureau of the Census, 1947. Census of Agriculture: 1945. Washington, DC:
GPO.
Weiss, T. 1991. Long term changes in US agricultural output per worker, 1800
1900. NBER Working Paper No. 23. Cambridge, MA: National Bureau of
Economic Research.
Wik, R.M., 1953. Steam Power on the American Farm. Philadelphia, PA: University
of Pennsylvania Press.
Williams, R.C., 1987. Fordson, Farmall, and Poppin' Johnny: A History of the Farm
Tractor and its Impact on America. Urbana, IL: University of Illinois Press.
Glossary
Common agricultural policy instruments That alter
international competitiveness include both border and
domestic measures. Border measures include import
and export taxes and subsidies, as well as quantitative
restrictions such as import or export quotas or bans.
All of these measures drive a wedge between the
prices observed in domestic and international markets.
This wedge has the same magnitude for producers
and consumers at least at the border, in contrast to
price-distorting domestic consumer and producer taxes
or subsidies or quantitative restrictions on consumption
or production, which affect just one of those two sides
of the market for internationally tradable goods. Domestic
subsidies or taxes on or border measures affecting inputs
into farming also will alter producer incentives and, in the
process, distort the demand for and prices of inputs. These
contrast with government-provided or governmentsubsidized investments in agricultural R&D, rural
infrastructure, or rural education and health, which can
increase returns to producers without directly distorting
product or input prices.
The nominal rate of assistance (NRA) Measures market
distortions imposed by governments that create a gap
between the current domestic price of a product and
the price that would exist under free markets. Under
the small-country assumption, this rate is computed
as the percentage by which government policies have raised
gross returns to farmers above what they would have
been had the government not intervened (or the percentage
by which government policies have lowered gross
returns, if NRAo0). It therefore includes the effect
of not only output-price-distorting policy instruments
Introduction
Throughout history the agricultural and food sector has been
subjected to perhaps more heavy-handed governmental
interventions than any other sector. Agricultural trade-related
policies account for an estimated 70% of the global welfare
cost of all merchandise trade distortions, even though the
agricultural sector contributes only 6% of global trade and 3%
of global income (Anderson et al., 2010, Table 2.3).
For advanced economies, the most commonly articulated
reason to restrict food trade has been to protect domestic producers from import competition as they come under competitive pressure to shed labor. Such measures harm not only
domestic consumers and exporters of other products but also
foreign producers and traders of food products. For decades,
doi:10.1016/B978-0-444-52512-3.00120-0
179
180
The resulting disarray in world agriculture has manifested itself in overproduction of agricultural products in
high-income countries and underproduction in low-income
countries. This disarray also means that there has been less
international trade in such products than would have been the
case under free trade. The end result is thinner and thus more
volatile markets for these weather-dependent products.
Agricultural policies became newsworthy during 200812
because international food prices spiked upwards three times in
that period. Biofuel policies have partly caused these price
spikes, and in turn, the effects of biofuel policies have been
exacerbated by the trade-policy responses of numerous countries at a time of low global grain stocks. Responses by
food-surplus developing countries have typically involved
restrictions on exports, while those by food-decit developing
countries have involved a lowering of import barriers. The ostensible motivation of policymakers has been to prevent a
decline in national food security: each country has aimed to
protect its domestic consumers (and indirectly, to protect the
current government from losing power). Together, however,
these measures have amplied international price spikes so that
each countrys measures have harmed other countries consumers (Carter et al., 2011; Martin and Anderson, 2012).
Changes in food prices create winners and losers, especially
among the poor. It has been argued for decades that such distortions have added to global inequality and poverty, because
three-quarters of the worlds poorest people depend, directly
or indirectly, on agriculture as their major source of income
(World Bank, 2007). Protectionist policies of high-income
countries have been partly responsible for international income
inequality and poverty in developing countries, but so too has
the antiagricultural bias of many developing countries policies,
according to a recent set of economy-wide empirical studies
(Anderson et al., 2010).
The agricultural policies of rich countries have not been
motivated by their effects on global poverty but rather by
domestic political concerns. Agricultural policy remains important in rich countries despite the relatively small and stilldeclining share of agriculture in GDP and employment. For
example, the common agricultural policy (CAP) in the European Union (EU) continues to absorb 40% of the entire EU
budget. That importance is reected in the priority these
countries trade negotiations place on farm policies in the
current round of World Trade Organization (WTO) negotiations on which the future growth of global income and the
trade of all goods and services depend.
Some agricultural- and trade-policy developments of the
past half-century have happened quite suddenly and been
transformational. Such events include decolonization in Africa
and elsewhere around 1960; the creation of the CAP in Europe
in 1962; the introduction of exible exchange rates from the
1970s; liberalization, deregulation, privatization, and democratization in many countries from the mid-1980s; the
opening of markets in China in 1979, in Vietnam in 1986, and
in Eastern Europe (following the fall of the Berlin Wall) in
1989; and the demise of the Soviet Union in 1991. However,
less well known are the inuences of policies that change
gradually in the course of economic development, as incomes
grow and comparative advantages evolve. Even these patterns
are subject to disruption though: since the 1980s many
production in each of the focus countries and just under twothirds of global agricultural production, valued at undistorted
prices over the period covered. Of the worlds 30 most valuable agricultural products, the indicators cover 77% of global
output (ranging from two-thirds for livestock to three-quarters
for oilseeds and tropical crops and ve-sixths for grains and
tubers). These products represent 85% of global agricultural
exports. Such comprehensive coverage of countries, products,
and years offers a reliable picture of long-term trends and
uctuations in policy indicators for individual countries and
commodities, as well as for country-groups, regions, and the
world as a whole. This data set reveals distinct patterns of price
distortions across countries and over time, as well as policy
turning points. After dening the indicators, these patterns are
summarized here under four headings: sectoral distortion
variation across countries; intrasectoral variation across farm
products; year-to-year variations in rates of distortion; and
policy-instrument choices.
181
182
60
50
High-income countries
High-income, incl. decoupled payments
Developing countries
40
Percentage
30
20
10
0
195559 196064 196569 197074 197579 198084 198589 199094 199599 200004 200510
10
20
30
Figure 1 Nominal rates of assistance to agriculture in high-income and developing countries, 19552010 (%). Five-year weighted averages, with
decoupled payments included in the dashed line. Reproduced from Anderson, K. (Ed.), 2009. Distortions to Agricultural Incentives: A Global
Perspective, 19552007. London: Palgrave Macmillan and Washington, DC: World Bank (Chapter 1), updated from estimates in Anderson, K.,
Nelgen, S., 2013. Updated National and Global Estimates of Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.org/
agdistortions (accessed 29.04.14).
183
Developing countries
60
NRA ag tradables
NRA nonag tradables
40
RRA
Percentage
20
0
196569
197074
197579
198084
198589
199094
199599
200004
200510
20
40
60
(a)
High-income countries
80
60
NRA ag tradables
NRA nonag tradables
RRA
40
Percentage
20
0
195559 196064 196569 197074 197579 198084 198589 199094 199599 200004 200510
20
40
60
(b)
Figure 2 Developing and high-income countries' nominal rates of assistance (NRAs) to agricultural and nonagricultural tradable sectors, and
relative rates of assistance (RRAs), 19552010 (%). Calculations use farm production-weighted averages across countries. RRA is dened as
RRA 100 100 NRAagt =100 NRAnonagt 1, where NRAagt and NRAnonagt, respectively, are the percentage NRAs for the tradable
segments of the agricultural and nonagricultural sectors. Reproduced from Anderson, K. (Ed.), 2009. Distortions to Agricultural Incentives: A
Global Perspective, 19552007. London: Palgrave Macmillan and Washington, DC: World Bank (Chapter 1), updated from estimates in Anderson,
K., Nelgen, S., 2013. Updated National and Global Estimates of Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.
org/agdistortions (accessed 29.04.14).
184
Trade-reduction index
50
Percentage
40
30
20
10
High-income countries
Europes transition econs
Developing countries
0
196064 196569 197074 197579 198084 198589199094 199599 200004 200510
(a)
Welfare-reduction index
100
90
80
Percentage
70
60
50
40
30
High-income countries
20
10
0
196064 196569 197074 197579 198084 198589 199094 199599 200004 200510
(b)
Figure 3 (a) Trade-reduction indexes (TRIs) and (b) Welfare-reduction indexes (WRIs) among high-income, transition, and developing countries
for tradable farm products, 19602010 (%). Reproduced from Lloyd, P.J., Croser, J.L., Anderson, K., 2010. Global distortions to agricultural
markets: New indicators of trade and welfare impacts, 1960 to 2007. Review of Development Economics 14 (2), 141160, based on time-series
estimates in Anderson, K., Croser, J.L., 2009. National and Global Agricultural Trade and Welfare Reduction Indexes, 1955 to 2007. Available at:
www.worldbank.org/agdistortions (accessed 29.04.14), and updated using Anderson, K., Nelgen, S., 2013. Updated National and Global Estimates
of Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.org/agdistortions (accessed 29.04.14).
185
Japan
Iceland
Korea
Norway
Switzerland
Sudan
Morocco
Turkey
Slovenia
Canada
EU15
Romania
Colombia
Poland
Zambia
Lithuania
Estonia
Senegal
US
China
Russia
Philippines
Mexico
Latvia
Czech Rep
Chile
Vietnam
Rep South Africa
Hungary
Brazil
Slovakia
Australia
Ukraine
Nigeria
New Zealand
Ghana
Thailand
Dominican Republic
India
Malaysia
Bulgaria
Kenya
Indonesia
Tanzania
Cameroon
Ethiopia
Madagascar
Pakistan
Mozambique
Uganda
Sri Lanka
Egypt
Bangladesh
Argentina
Ecuador
Nicaragua
Zimbabwe
Cote d'Ivoire
50
50
100
150
Figure 4 Relative rates of assistance by country, 200510. Reproduced from Anderson, K. (Ed.), 2009. Distortions to Agricultural Incentives: A Global
Perspective, 19552007. London: Palgrave Macmillan and Washington, DC: World Bank (Chapter 1), using Anderson, K., Nelgen, S., 2013. Updated
National and Global Estimates of Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.org/agdistortions (accessed 29.04.14).
Year-to-Year Variation
Around the long-run trend for each country, much uctuation
is seen from year to year in individual product NRAs. This
tendency has not diminished since the mid-1980s for developing countries, and it has even increased for high-income
countries. The negative correlation of a commoditys NRA with
movements in its international price is largely responsible for
this pattern. On average, barely half of the change in an
186
35
China
30
India
25
Indonesia
Developing countries
Coconut
Cotton
20
Sugar
15
Milk
10
Maize
Wheat
Pigmeat
0
5
199599
200004
200509
Poultry
2010
Beef
10
Rice
15
Figure 5 Agricultural nominal rates of assistance in China, India, and
Indonesia, 19952010 (%). Compiled from estimates in Anderson, K.,
Nelgen, S., 2013. Updated National and Global Estimates of
Distortions to Agricultural Incentives, 1955 to 2011. Available at:
www.worldbank.org/agdistortions (accessed 29.04.14).
200509
198084
Soybean
Coffee
50
(a)
50
150
High-income countries
Rice
Sugar
Cotton
Milk
Pigmeat
Poultry
Beef
Maize
Soybean
Wheat
200510
198084
Rapeseed
Barley
(b)
50
50
150
187
Developing countries
90
70
50
30
10
10
196569
197074
197579
198084
198589
199094
199599
200004
200509
30
50
(a)
Import-competing
Exportables
Total
195559 196064 196569 197074 197579 198084 198589 199094 199599 200004 200510
30
50
(b)
Import-competing
Exportables
Total
Figure 7 Nominal rates of assistance (NRAs) to exportable, import-competing, and all covered agricultural products in (a) developing and
(b) high-income and European transition economies, 19552010 (%). Five-year weighted averages for covered products only. The total also
includes nontradables. The straight line in the upper segment of each graph represents an ordinary-least-squares regression based on annual NRA
estimates. Reproduced from Anderson, K. (Ed.), 2009. Distortions to Agricultural Incentives: A Global Perspective, 19552007. London: Palgrave
Macmillan and Washington, DC: World Bank (Chapter 1), updated using Anderson, K., Nelgen, S., 2013. Updated National and Global Estimates of
Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.org/agdistortions (accessed 29.04.14).
188
60
50
Percent
40
30
20
10
0
1960
1965
1970
1975
1980
Export tax
Import subsidy
1985
1990
1995
2000
2005
Import tax
Export subsidy
Figure 8 Contributions of various instruments to the border component of the welfare reduction index (WRI) for developing countries, 1960
2010 (%). Derived from estimates reported in Croser, J.L., Anderson, K., 2011. Changing contributions of different agricultural policy instruments
to global reductions in trade and welfare. World Trade Review 10 (3), 297323, updated using Anderson, K., Nelgen, S., 2013. Updated National
and Global Estimates of Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.org/agdistortions (accessed 29.04.14).
changes in the relative importance of different policy instruments occur. This is evident from the estimated contributions
to total agricultural WRIs of various policy instruments during
the upward price spikes around 1974 and 2008 and the
downward spike around 1986 (Figure 8). In some cases, trade
taxes even temporarily disappeared; in other cases, trade subsidies emerged or expanded. Even when aggregated overall
developing countries, the contribution of export taxes and
import subsidies to the overall WRI rises and falls with international prices, whereas the opposite is true of import taxes
and export subsidies.
Income Redistribution
Distortions in agricultural and food markets result from policies designed to alter the distribution of income from what
would otherwise emerge under unfettered market outcomes.
Income distribution may change for structural or cyclical reasons. For example, overall economic development is typically
associated with some sectors growing and some declining
198084
189
200510
350
350
Decoupled payments
300
300
Production measures
250
Border measures
200
Percentage
Percentage
250
150
200
150
100
100
50
50
0
ANZ
NA
EU
EFTA Ja/Ko
ANZ
NA
ECA
EU
EFTA Ja/Ko
Figure 9 Comparison of earlier (198084) and more recent (200510) contributions of various policy instruments to the producer component of
the welfare reduction index (WRI) for selected high-income and transition countries (%). ANZ, Australia and New Zealand; EFTA, European Free
Trade Area; EU, European Union of 27 member countries; Ja/Ko, Japan and (South) Korea; and NA, North America. ECA is a term used by the
World Bank to denote the transitional economies of Central and Eastern Europe and Central Asia. Reproduced from Croser, J.L., Anderson, K.,
2011. Changing contributions of different agricultural policy instruments to global reductions in trade and welfare. World Trade Review 10 (3),
297323, updated using Anderson, K., Nelgen, S., 2013. Updated National and Global Estimates of Distortions to Agricultural Incentives, 1955 to
2011. Available at: www.worldbank.org/agdistortions (accessed 29.04.14).
Democratization
Many developing countries have experienced democratization
over recent decades. The implications for agricultural policies
190
Olper et al. (forthcoming) exploit the time-series and crosssectional variation in the World Banks database to show that
democratization reduced agricultural taxation and increased
agricultural subsidization because most political transitions
occurred in poor countries with many farmers.
Summary
The reduction of antiagricultural policies in developing
countries during the past decade has been caused by economic
growth, by the shift in the politicaleconomic equilibria induced by such growth, and by changes in governance and
media structures. As rural infrastructure improves and communications costs fall, farmers become more aligned and
politically more effective. This development again contributes
to a shift in the power balance in favor of rural interests.
Moreover, as economies develop, the role of agribusiness and
food companies often with cooperative roots expands.
These more concentrated and better capitalized organizations
often form powerful lobby coalitions with farmers interest
groups. Reduced taxation of agriculture in many developing
countries that experienced income growth during recent decades is consistent with the identied forces sourced with a
political-economic lens. The reduction of antiagricultural
policies over the past two decades has been reinforced by
political reforms (democratization) and by the growth of
commercial media.
191
192
From our assessment, it is clear that much progress has occurred in the past decade or so in improving our understanding of why governments distort incentives facing
agriculture. Certainly, more empirical testing of hypotheses
suggested by theorists could be carried out, but considerable
light has already been shed on most of the stylized facts raised
by the World Banks documentation of the evolution of global
price distortions since the 1950s. That understanding suggests
that there is room for cautious optimism about the prospects
for future agricultural policy reform. Admittedly, it is troubling
that some developing countries have moved from negative to
positive RRAs and that agricultural protection and market
distortion have recently increased in three of the most important developing countries, namely China, India, and
Indonesia. In high-income countries, too, although the World
Bank data reveal declining trends for NRAs, these trends do not
necessarily reect actual changes in their distorting policy instruments. Instead, higher world food prices largely explain the
reductions in measured NRAs in the past 5 years. But many
other countries RRAs do appear to have converged toward
zero (that is, where their assistance to agricultural and nonagricultural tradables is approximately equal), and other highincome countries have been lowering their RRAs nontrivially
since the late 1980s.
Global and regional institutions appear to have played an
important role in contributing to these reforms. Of particular
importance to the decline in the RRA for the EU has been the
institution of the General Agreement on Tariffs and Trade (and
now the WTO). However, the recent shift in agricultural policies focusing on renewable energy (particularly in the USA,
the EU, and Brazil) has major implications for world food
prices and security. Ongoing research should make as transparent as possible the continued pursuit of protectionist
measures by various countries in the form of biofuels policies,
which tend to raise world food prices, in contrast to traditional
agricultural policies, which historically have depressed these
prices.
Prospects for policy reform will be inuenced by the
changing landscape of organized economic interests. Interactions between farmers and landowners, agribusiness, food
and retail companies, environmentalists and other groups
clearly inuence agricultural policy negotiations and debates
in all countries. The vertical relationships between farmers and
agribusinesses are often critical in sustaining policy reforms.
Capturing opportunities to form new coalitions among the
interests of farmers, downstream agribusiness, food consumers, and environmental groups will largely dictate sustainable policy reforms that promote the provision of local
public goods, agricultural productivity, and markets for environmental services. Certainly the many complex factors that
contribute to distortion of agricultural and food markets can
impede as well as promote progress, but hopefully continued
Acknowledgments
This article draws on the authors recent survey in the June
2013 issues of the Journal of Economic Literature. We thank John
Nichols for his helpful comments on an earlier draft and Signe
Nelgen for assistance with the gures and tables. Anderson
acknowledges nancial support from the Australian Research
Council and Rural Industries Research and Development
Corporation.
References
Akiyama, T., Baffes, J., Larson, D.F., Varangis, P. (Eds.), 2001. Commodity Market
Reforms: Lessons of Two Decades. Washington, DC: World Bank.
Alatas, V., Banerjee, A., Hanna, R., Olken, B.A., Tobias, J., 2012. Targeting the poor:
Evidence from a eld experiment in Indonesia. American Economic Review 102
(4), 12061240.
Anania, G., Bohman, M.E., Carter, C.A., McCalla, A.F. (Eds.), 2004. Agricultural
Policy Reform and the WTO: Where Are We Heading? London: Edward Elgar.
Anderson, J.E., Neary, J.P., 2005. Measuring the Restrictiveness of International
Trade Policy. Cambridge, MA: MIT Press.
Anderson, K., 1995. Lobbying incentives and the pattern of protection in rich and
poor countries. Economic Development and Cultural Change 43 (2), 401423.
Anderson, K. (Ed.), 2009. Distortions to Agricultural Incentives: A Global Perspective,
19552007. London: Palgrave Macmillan; Washington, DC: World Bank.
Anderson, K. (Ed.), 2010. The Political Economy of Agricultural Price Distortions.
Cambridge and New York: Cambridge University Press.
Anderson, K., Cockburn, J., Martin, W. (Eds.), 2010. Agricultural Price Distortions,
Inequality, and Poverty. Washington, DC: World Bank.
Anderson, K., Hayami, Y., Honma, M., 1986. The growth of agricultural protection.
In: Anderson, K., Hayami, Y. (Eds.), The Political Economy of Agricultural
Protection: East Asia in International Perspective. Sydney: Allen and Unwin, in
association with the Australian National University, Australia-Japan Research
Centre, pp. 1730.
Anderson, K., Kurzweil, M., Martin, W., Sandri, D., Valenzuela, E., 2008. Measuring
distortions to agricultural incentives, revisited. World Trade Review 7 (4), 675704.
Anderson, K., Nelgen, S., 2012. Trade barrier volatility and agricultural price
stabilization. World Development 40 (1), 3648.
Anderson, K., Nelgen, S., 2013. Updated National and Global Estimates of
Distortions to Agricultural Incentives, 1955 to 2011. Available at: www.worldbank.
org/agdistortions (accessed 29.04.14).
Anderson, K., Swinnen, J.F.M., 2010. How distorted have agricultural incentives
become in Europes transition economies? Eastern European Economics 48 (1),
79109.
Anderson, K., Valenzuela, E., 2008. Estimates of Distortions to Agricultural
Incentives, 1955 to 2007. Available at: www.worldbank.org/agdistortions
(accessed 29.04.14).
Baldwin, R., Robert-Nicoud, F., 2007. Entry and asymmetric lobbying: Why governments
pick losers. Journal of the European Economic Association 5 (5), 10641093.
Bates, R.H., Block, S., 2010. Agricultural trade interventions in Africa. In: Anderson,
K. (Ed.), The Political Economy of Agricultural Price Distortions. Cambridge and
New York: Cambridge University Press, pp. 304331 (Chapter 12).
Besley, T., Burgess, R., 2001. Political agency, government responsiveness and the
role of the media. European Economic Review 45 (46), 629640.
193
Carter, C.A., Rausser, G.C., Smith, A., 2011. Commodity booms and busts. Annual
Review of Resource Economics 3, 87118.
Dixit, A.K., 1996. The Making of Economic Policy: A Transaction Cost Politics
Perspective. Cambridge, MA: MIT Press.
Downs, A., 1957. An Economic Theory of Democracy. New York: Harper and Row.
Drabek, Z., Bacchetta, M., 2004. Tracing the effects of WTO accession on policymaking in sovereign states: Preliminary lessons from the recent experience of
transition countries. The World Economy 27 (7), 10831125.
Evenett, S.J., Primo Braga, C., 2006. WTO accession: Moving the goalposts? In:
Newfarmer, R. (Ed.), Trade, Doha and Development: A Window into the Issues.
Washington, DC: World Bank, pp. 227241 (Chapter 19).
Gardner, B.L., 1983. Efcient redistribution through commodity markets. American
Journal of Agricultural Economics 65 (2), 225234.
Gardner, B.L., 1987. Causes of US farm commodity programs. Journal of Political
Economy 95 (2), 290310.
Gawande, K., Hoekman, B., 2006. Lobbying and agricultural trade policy in the
United States. International Organization 60, 527561.
Gawande, K., Hoekman, B., 2010. Why governments tax or subsidize agricultural
trade. In: Anderson, K. (Ed.), The Political Economy of Agricultural Price
Distortions. Cambridge and New York: Cambridge University Press, pp. 241277
(Chapter 10).
de Gorter, H., Nielson, D.J., Rausser, G.C., 1992. Productive and predatory public
policies: Research expenditures and producer subsidies in agriculture. American
Journal of Agricultural Economics 74 (1), 2737.
Huang, J., Rozelle, S., Martin, W., Liu, Y., 2009. Distortions to agricultural
incentives in China. In: Anderson, K., Martin, W. (Eds.), Distortions to
Agricultural Incentives in Asia. Washington, DC: World Bank, pp. 117161
(Chapter 3).
Kherallah, M., Delgado, C., Gabre-Madhin, E., Minot, N., Jonson, M., 2002.
Reforming Markets in Africa. Baltimore and London: John Hopkins University
Press.
Krueger, A.O., Schiff, M., Valds, A., 1988. Agricultural incentives in developing
countries. World Bank Economic Review 2 (3), 255272.
Krueger, A.O., Schiff, M., Valds, A., 1991. The Political Economy of Agricultural
Pricing Policy. Vol. 1, Latin America; vol. 2, Asia; and vol. 3, Africa and
the Mediterranean. Baltimore: Johns Hopkins University Press for the World
Bank.
Kuzyk, P., McCluskey, J.J., 2006. The political economy of the media: Coverage of
the US-Canadian lumber trade dispute. World Economy 29 (5), 637654.
Lloyd, P.J., Croser, J.L., Anderson, K., 2010. Global distortions to agricultural
markets: New indicators of trade and welfare impacts, 1960 to 2007. Review of
Development Economics 14 (2), 141160.
Lpez, R.A., 2008. Does protection for sale apply to the US food industries?
Journal of Agricultural Economics 9 (1), 2540.
Martin, W., Anderson, K., 2012. Export restrictions and price insulation during
commodity price booms. American Journal of Agricultural Economics 94 (2),
422427.
McCluskey, J., Swinnen, J., 2010. Media economics and the political economy
of information. In: Coen, D., Grant, W., Wilson, G. (Eds.), The Oxford
Handbook of Government and Business. Oxford: Oxford University Press,
pp. 643662.
McMillan, M., 2001. Why kill the golden goose? A political-economy model of
export taxation. Review of Economics and Statistics 83 (1), 170184.
Oberholzer-Gee, R., Waldfogel, J., 2005. Strength in numbers: Group size and
political mobilization. Journal of Law and Economics 48 (1), 7391.
Olper, A., Falkowski, J., Swinnen, J., forthcoming. Political reforms and rent distribution: Evidence from agricultural policies. LICOS Discussion Paper. Leuven,
Belgium: Katholieke Universiteit Leuven. World Bank Economic Review 27.
Olper, A., Swinnen, J., 2013. Mass media and public policy: Global evidence from
agricultural policies. World Bank Economic Review 27 (3), 413436.
doi:10.1093/wber/lht008.
Olson, M., 1965. The Logic of Collective Action: Public Goods and the Theory of
Groups. Cambridge, MA: Harvard University Press.
Orden, D., Blandford, D., Josling, T., 2010. Determinants of United States farm
policies. In: Anderson, K. (Ed.), The Political Economy of Agricultural Price
Distortions. Cambridge and New York: Cambridge University Press, pp. 162190
(Chapter 7).
Organization for Economic Co-operation and Development (OECD), 2009.
Agricultural Policies in Emerging Economies: Monitoring and Evaluation. Paris:
Organisation for Economic Co-operation and Development.
Organisation for Economic Co-operation and Development (OECD), 2012. Producer
and Consumer Support Estimates. Available at: http://www.oecd.org (for 1986
2011) (accessed 25.11.12).
194
Rausser, G., 1992. Predatory versus productive government: The case of U.S.
agricultural policy. Journal of Economic Perspectives 6 (3), 133157.
Rausser, G.C., de Gorter, H., 1989. Endogenizing policy in models of agricultural markets. In: Maunder, A., Valds, A. (Eds.), Agriculture and
Governments in an Interdependent World. Oxford: Oxford University Press,
pp. 259274.
Rausser, G.C., Swinnen, J.F.M., Zusman, P., 2011. Political Power and Economic
Policy: Theory, Analysis, and Empirical Applications. Cambridge and New York:
Cambridge University Press.
Rausser, G.C., Zilberman, D., Just, R., 1984. The distributional effects of land
controls in agriculture. Western Journal of Agricultural Economics 9 (2),
215232.
Rodrik, D., 1995. Political economy of trade policy. In: Grossman, G.M., Rogoff, K.
(Eds.), Handbook of International Economics, vol. 3. Amsterdam: North-Holland,
pp. 14571494.
Strmberg, D., 2001. Mass media and public policy. European Economic Review 45
(46), 652663.
Strmberg, D., 2004. Mass media competition, political competition, and public
policy. Review of Economic Studies 71 (1), 265284.
Swinnen, J.F.M., 1994. A positive theory of agricultural protection. American Journal
of Agricultural Economics 76 (1), 114.
Swinnen, J.F.M. (Ed.), 2008. The Perfect Storm: The Political Economy of the
Fischler Reforms of the Common Agricultural Policy. Brussels: Center for
European Policy Studies.
Swinnen, J.F.M., Banerjee, A.N., de Gorter, H., 2001. Economic development,
institutional change, and the political economy of agricultural protection: An
econometric study of Belgium since the 19th Century. Agricultural Economics 26
(1), 2543.
Swinnen, J.F.M., Olper, A., Vandemoortele, T., 2012. Impact of the WTO on
agricultural and food policies. The World Economy 35 (9), 10891101.
Swinnen, J., Vandeplas, A., Maertens, M., 2011. Liberalization, endogenous
institutions, and growth: A comparative analysis of agricultural reforms in Africa,
Asia, and Europe. World Bank Economic Review 24 (3), 412445.
Tovar, P., 2009. The effects of loss aversion on trade policy: Theory and evidence.
Journal of International Economics 78 (1), 154167.
Varshney, A., 1995. Democracy, Development, and the Countryside: Urban-Rural
Struggles in India. Cambridge and New York: Cambridge University Press.
World Bank, 2007. World Development Report 2008: Agriculture for Development.
Washington, DC: World Bank.
Relevant Websites
www.apo-tokyo.org
Asian Productivity Organization.
www.fao.org/mafap
Food and Agriculture Organization.
www.oecd.org/chile/producerandconsumersupportestimatesdatabase.htm
Organization for Economic Co-operation and Development.
www.worldbank.org/agdistortions
World Bank.
Glossary
Agroforest Complex agroforestry system with a forest-like
structure; synonymous to complex multistrata agroforestry
system.
Complex multistrata agroforestry system (CMSAF) Treedominated land use system with two or more strata of trees
or shrubs and a substantial degree of structural complexity
within at least one of the strata.
Homegarden Intimate, multistorey combination of
various trees and crops, sometimes in association with
domestic animals, around homesteads.
doi:10.1016/B978-0-444-52512-3.00030-9
195
196
Rustic cacao
Planted beneath thinned
primary or old secondary
forest
16
ecological intensication. These questions will be briey reviewed in the Section on Production and Intensication.
0
Meters
16
Planted shade
Ranges from traditional
polyculture through
commercial to a specialized,
single-species shade
0
Meters
8
Technified cacao
No shade component
0
Meters
Figure 2 Gradient of cocoa production systems with varying degrees
of complexity. Reproduced from (with kind permission from the Royal
Swedish Academy of Sciences) Rice, R.A., Greenberg, R., 2000.
Cacao cultivation and the conservation of biological diversity. Ambio
29, 167173.
shade trees, and fruit trees, such as the exotic jackfruit (Artocarpus heterophyllus) and caj (Spondias mombin), the latter
introduced from the Amazon. These fruit trees are particularly
prominent because they are preferred by farm workers and can
regenerate spontaneously, especially during phases of extensive management or temporary abandonment (Sambuichi
et al., 2012). Bananas (Musa spp.) are also often present. There
is also a recent trend of enriching the cabrucas with other
commercial tree species, such as rubber trees (Schroth et al.,
2011b).
There is a wide variety of cocoa production systems in West
and Central Africa, with a clear eastwest gradient of decreasing shade use. According to Gockowski and Sonwa
(2008), medium to heavy shade (i.e., CMSAF) is used by more
than 50% and 60% of cocoa farms in Nigeria and Cameroon,
respectively, but less than 30% of cocoa farms in Ghana and
Cte d'Ivoire. Within Ghana, Ruf (2011) reported a trend of
decreasing shade use on cocoa farms from the older, eastern
cocoa regions to the newer, western cocoa regions. This
changing attitude toward shade is apparently related to the
adoption of cocoa varieties that are less shade tolerant as well
as related to forest laws that restrict the farmers' rights to
selling farm timber. The use of shade has also been in decline
in Cte d'Ivoire, in part related to the dominant role of migrant farmers from nonforest areas during the expansion of the
cocoa sector in the second half of the twentieth century (Ruf
and Schroth, 2004). Differences in the attitude toward, and
knowledge about, forest trees as cocoa shade between local
and migrant cocoa farmers have also been shown in Cameroon (Laird et al., 2007). In southern Cameroon, where CMSAF
are the dominant practice in cocoa farms, trees of other species
contributed 25% to total farm revenues (Gockowski et al.,
2010). A trend of increasing replacement of forest trees with
fruit trees with increasing proximity to the capital Yaound has
been observed. This suggests that farmers intensify and diversify their cocoa systems as they gain market access for a
wider range of products (Sonwa et al., 2007).
Coffee and tea are also sometimes grown in CMSAF, although the most complex types are perhaps less frequent than
those with cocoa. In the case of coffee, systems with a large
percentage of native forest trees in the canopy are also called
rustic systems or traditional polycultures, whereas systems
with a dominance of planted and managed fruit and timber
trees (including bananas and plantains) in the canopy are referred to as commercial polycultures (Moguel and Toledo,
1999). CMSAF with coffee can be found in several parts of
Mesoamerica, including the Sierra Madre de Chiapas in
southern Mexico, where Arabica coffee is often interspersed
with forest and fruit trees and sometimes with ornamental
palms (Figure 3). This forms a landscape mosaic made up of
coffee agroforests, natural forest, and cattle pasture (Schroth
et al., 2011a). In El Salvador, most of the forest cover consists
of coffee agroforests (Somarriba et al., 2004). A common
practice in Costa Rica and other parts of Central America is the
association of coffee with commercial timber trees, especially
laurel (Cordia alliodora) as well as fruit and leguminous shade
trees. In India's main coffee region, Kodagu in the Western
Ghats mountains, coffee is often grown under a highly diverse
canopy of native forest trees that were retained when coffee
was planted into partially cleared forest, as well as fruit trees
197
198
integrated into the shifting cultivation cycle in Indonesia, especially Eastern Kalimantan, where it has become the second
most important forest product of the country after timber. The
rattan seeds or seedlings are added to slash-and-burn plots
with dryland rice and they grow as part of a commercial fallow
vegetation when the food crop elds are abandoned. Canes
can be harvested after 710 years for 50 or more years, until
the plot is slashed and burned again for a new cycle. This
practice is now threatened by the expansion of oil palm as well
as periodic droughts to which rattan is poorly adapted
(Michon, 2005).
Rattan and rubber agroforests in Indonesia, and to a lesser
extent rubber agroforests in the Amazon, can be considered
long-cycle rotational systems that involve periodic events of
clearfelling and replanting in fact a type of economically
enriched fallow. Their invention is a remarkable case of farmer
innovation. Through the integration of tree crops into their
slash-and-burn systems, farmers in Indonesia and the Amazon
solved several problems at the same time. The planting of tree
seeds or seedlings with food crops required a little extra labor
during the rst few years, when the seedlings were most vulnerable. In contrast to the practice used in industrial plantations of planting tree crops with cover crops, it also ensured
food security while the tree crops were not yet productive.
Furthermore, the agroforests had a much higher density of
useful trees than natural forest, where the tree crops were native (e.g., several hundred rubber trees per hectare in agroforests as compared with less than ve per hectare in natural
forest in the Amazon), thereby again increasing the productivity of labor as well as land. And nally, by associating tree
crops with native vegetation, these economically enriched
fallows regenerated the fertility of the site, enabling a new cycle
of food and tree crops when the old tree crops had been
exhausted.
Other CMSAF that are planted in slash-and-burn plots can
become permanent through regeneration in canopy gaps, as in
natural forest. Remarkable among these are the agroforests
based on damar trees (S. javanica), a resin producing dipterocarp species that occupy more than 50 000 ha in southern
Sumatra (Michon, 2005). Permanent damar agroforests were
invented by farmer extractivists in southern Sumatra in response to the overexploitation of damar trees in the native
forest when market demand for their resin increased in the
early twentieth century. The new practice resulted in a remarkable case of reagroforestation of a slash-and-burn landscape (Michon et al., 2000). Dipterocarp trees are considered
difcult to regenerate but are successfully planted by the local
farmers in slash-and-burn plots with rice, coffee (C. canephora),
pepper (Piper nigrum), and fruit trees. The coffee is cultivated
for 8 years, and then the damar and fruit trees grow together
with natural regrowth. Resin tapping begins after 2025 years
and after 4050 years, when the agroforests reach their full
production. Dead trees are replaced under the canopy, but
there is usually no replanting of the whole plot. Although
most of the large trees in mature agroforests are damar trees,
these are associated with many other useful tree species such as
durian (D. zibethinus) and timber trees. The large durian trees
that produce a popular and commercially important fruit as
well as timber are also a common or dominant component of
other types of Indonesian agroforests, sometimes with other
199
200
Height (m)
Primary
Hevea
Damar
Durian
45
35
25
15
5
45
35
25
15
5
10
30
50
10
30
50
Figure 6 Height proles of mean foliage cover in primary forest and agroforests based on rubber, damar, and durian in Sumatra. Reproduced
from (with kind permission from Island Press) Schroth, G., Harvey, C.A., Vincent, G., 2004c. Complex agroforests their structure, diversity, and
potential role in landscape conservation. In: Schroth, G., et al. (Eds.), Agroforestry and Biodiversity Conservation in Tropical Landscapes. Island
Press, Washington, DC, pp. 227260 and Thiollay, J.-M., 1995. The role of traditional agroforests in the conservation of rain forest bird diversity
in Sumatra. Conservation Biology 9, 335353.
Forest-Enrichment Systems
Homegardens represent the intensive end of CMSAF, characterized by a dominance of cultivated species, whereas forestenrichment systems are the extensive end and transition into
extractively used natural forests (wild harvesting). In these
systems, useful plants are integrated into more or less disturbed natural forest, for example, in clearings or along water
courses, but in contrast to the systems discussed earlier, the
natural forest vegetation remains dominant. Hunter-gatherers
in the Amazon appear to have enriched forest around campsites with useful palms and other trees for several thousand
years (Politis, 2001), which is similar to the practice in Indonesia, whereas the transfer of forest species to areas around
campsites was an early form of plant domestication (Michon
and de Foresta, 1999). More recent practices in the Amazon
include the sowing of aai palms in riparian forests (Schroth
and da Mota, 2007, Figure 7) or the enrichment of natural
rubber groves with rubber seeds or seedlings to counteract the
decline of the tapped mature trees (Dean, 1987). The planting
of clusters of rattan palms into thinned forest can be found in
Kalimantan, Indonesia (Michon, 2005). If natural forest with
high densities of useful trees whose regeneration was facilitated by human disturbance were included in the concept of
CMSAF, then this would reportedly be applied to some 11% of
the Brazilian Amazon, where such human-modied forests are
thought to prevail (Scoles and Gribel, 2011). Examples include the oligarchic forests dominated by aai palms in fact
transitional systems between extractivism and agroforestry in
the Amazon estuary (Muniz-Miret et al., 1996); forest fallows
with high densities of tucum palms (Astrocaryum tucuma syn.
Astrocaryum aculeatum) that produce valuable fruits in the
central Amazon (Schroth et al., 2004a); and probably forests
with high density of Brazil nut trees (Scoles and Gribel, 2011).
Environmental Functions
The environmental functions of CMSAF have mostly been
studied at the scale of the plot or farm and with a short-term
focus, but ultimately to determine their true relevance to global environmental issues, they need to be considered at the
scale of the landscape and over timescales of years or decades.
In view of the ongoing forest loss in many tropical countries,
of particular interest is whether CMSAF replace forest or help
conserve forest, or even help to restore forest functions where
these have previously been lost. From an environmental point
of view, especially in view of global climate change and
201
202
(541 Mg ha1) at that site, whereas food crop elds only had
85 Mg ha1, or 16% of the biomass of primary forest
(Duguma et al., 2001). Because aboveground carbon stocks are
concentrated in large trees, they should be highest in farms
that retain large remnant forest trees soon after clearing and
should decrease as these forest trees die or are sold off. The
conservation and regeneration of large forest trees in CMSAF is
thus an important measure for conserving the carbon stocks
(and also the biodiversity) of agroforests. In a global review
of carbon stocks in coffee production systems, Mndez et al.
(2012) found average carbon stocks in the vegetation
decreasing in the sequence: traditional coffee polycultures
that contained large forest trees4commercial polycultures
that associate coffee with a range of fruit trees4coffee
monocultures with a simple shade stratum of legume
trees4unshaded coffee monocultures. Belowground C stocks
of tree crops are often approximately 2030% of aboveground
C stocks but can vary considerably and reach values of 1 and
higher for species that are often pruned, for example, for the
extraction of hearts of palm (Schroth et al., 2002). When farms
are very extensively managed or even temporarily abandoned,
tree cover and presumably their biomass per hectare can increase. For example, an increase in tree density (and presumably carbon stocks) has been found by recent inventories
in cocoa agroforests in southern Bahia, Brazil, compared with
inventories carried out in the 1960s. This has been interpreted
as an effect of the cocoa crisis and reduced management intensity of the past 20 years (Sambuichi et al., 2012). Such
increases may, however, be temporary and be lost when conditions improve and farm management intensies.
In permanent agroforests that were established on slashand-burn plots, total system biomass should increase over
time approaching that of natural forest, although probably
never reaching it owing to the absence of very large trees that
can take several hundred years to grow. In rotational systems,
such as certain rubber and rattan agroforests, however, the
system biomass is periodically reset through slashing, burning, and replanting and is best characterized through a time
average, similar to that of monocyclic forest plantations. In
Indonesia, Hairiah et al. (2001) reported carbon stocks of
89 Mg ha1 in old rubber agroforest and a time average of
46 Mg C ha1 in a rubber agroforest cycle between two slashand-burn events, compared with 306 Mg C ha1 in primary
forest. Schroth et al. (2011a) reported C stocks of 143
(SD 63) Mg ha1 for eight old rubber agroforests in Brazil;
primary forest was not measured at that site.
As CMSAF often form the transition between more intensively managed agricultural land and natural forest, they may
also contribute to the conservation of forest carbon stocks by
reducing the use of re at the agricultureforest interface. For
example, in northern Thailand, the presence of tea agroforests
in watersheds has reportedly reduced the use of re in the
same watersheds for fear of affecting the valuable tea plantings
if re went out of control. It has also been suggested that the
presence of rubber agroforests on forest boundaries in the
Tapajs region of the Amazon may have protected forest edges
by encouraging a more careful use of re, to which rubber trees
are very sensitive, in slash-and-burn plots (Schroth et al.,
2004c). Other edge effects that commonly contribute to tree
mortality and the degradation of forest boundaries, such as
20
y = 1.605x + 13.821
R 2 = 0.2664, P = 0.041
15
10
0
0
4
6
Vegetation complexity
10
203
millions of hectares. Although these areas usually have restrictions on the types of land use that are permitted, the
practice of slash-and-burn agriculture and cattle pasture within
protected areas is quite common. Especially where CMSAF are
traditional forms of land use in these reserves, they can be
environmentally and socially more sustainable alternatives to
slash-and-burn agriculture and pasture. For example, in the
biosphere reserves of the Sierra Madre de Chiapas, Mexico,
coffee agroforests are an important land use activity, especially
at higher elevations (Cortina-Villar et al., 2012), whereas in the
Tapajs-Arapiuns Extractive Reserve in the Brazilian Amazon,
rubber agroforestry and a more recent adaptation, agroforests
based on timber and nontimber trees, are alternatives to the
production of cassava our in slash-and-burn agriculture
(Schroth et al., 2011a; Schroth and da Mota, 2013). CMSAF
may also have value for tourism, but apart from some birdwatching tourism in shade coffee farms mostly in northern
Latin America, this potential has been little explored.
204
tree crop plantings and have lost many species and varieties
(Kumar and Nair, 2004). Signicant traditional shade coffee
areas in Mesoamerica, northern South America and the
Caribbean have been lost through conversion into lightly or
unshaded systems (Perfecto et al., 1996). In Kodagu, India,
traditionally high shade levels in coffee farms have been reduced with the introduction of irrigation and crop diversication (especially pepper) and farmers increasingly use exotic
trees (Grevillea robusta) instead of diverse native trees for shade
(Garcia et al., 2010).
Michon (2005) suggested that the apparently low protability of many Indonesian agroforests which leads to their
replacement by simpler land use systems is in part due to their
management for diversication rather than intensication.
However, extensive management and consequently low
productivity is also characteristic of many CMSAF that are not
particularly diversied from an economic point of view
but are dominated by a single crop species (e.g., rubber or
cocoa). Apparently, CMSAF lose ground as market conditions
encourage greater specialization and more intensive management of a single or small number of currently most protable crops. This is what will be seen if rubber agroforests are
replaced by monocultures of clonal rubber trees in Indonesia
or if homegardens are replaced by coconut plantations in
Kerala, India. Cultural and societal changes such as increased
urbanization and changing food preferences, certainly, also
play a role (Kumar and Nair, 2004). Agricultural policies have
also for many years encouraged monoculture practices, such as
the replacement of traditional shade coffee and cocoa systems
with less shaded systems, although farmers have not always
followed these recommendations (Johns, 1999).
Considering the uctuations of commodity prices on
international markets and the numerous environmental risks
to which producers of tree crops are exposed, switching to
monoculture practices may not always be in the best long-term
interests of local farmers, who may not have the nancial and
technical means to engage in such drastic changes of their
traditional land use systems. Ruf and Schroth (2013) present a
series of case studies illustrating a current trend toward diversication among tree crop farmers in regions that had
previously been dominated by a single (often pioneer) tree
crop such as cocoa, coconut, or coffee. This trend is motivated
in part by severe price shocks affecting commodities such as
coffee and cocoa during the past two decades and in part by
environmental pressures such as pests and diseases, declining
soil fertility, and climate variability. This diversication may
take place at the plot, farm, or landscape level and does not
necessarily result in CMSAF, but suggests that interest in diversied farming systems is again on the rise, counteracting to
some extent the overspecialization that was a hallmark of the
Green Revolution.
Where CMSAF are in decline not because of their diversication but because of their low productivity and protability, research is needed into ways to increase their output
while still preserving essential elements of these traditional,
site-adapted systems. The following examples are intended to
illustrate that the conservation, intensication, and promotion
of CMSAF are multidimensional tasks which need to consider
the dynamics of markets and society, in addition to agronomic
and ecological questions, without attempting to be exhaustive.
205
350
30 years, sandy soil (1)
30 years, sandy soil (2)
40 years, terra preta
300
250
200
150
100
50
0
0
20
40
60
80
100
120
Measured trees
Figure 10 Productivity of individual rubber trees in three rubber agroforests in the Tapajs region of the Brazilian Amazon. Closed symbols show
the productivity per tree at the beginning of the tapping season, and open symbols show the average productivity of the highest producing tree
over the tapping season. Reproduced from (with kind permission from Elsevier) Schroth, G., Moraes, V.H.F., da Mota, M.S.S., 2004d. Increasing
the protability of traditional, planted rubber agroforests at the Tapajs river, Brazilian Amazon. Agriculture, Ecosystems and Environment 102,
319339.
for improving the fruit quality and productivity of an Amazonian palm species, A. aculeatum syn. A. tucuma, that regenerates abundantly in disturbed sites (such as agroforests,
crop elds, and fallows) but is very difcult to germinate and
plant.
Futures of CMSAF
Change is normal in agricultural systems. Some CMSAF, such
as homegardens, are thousands of years old and may have
been sites of early plant domestication. Other CMSAF were
invented by tropical farmers within the past hundred years,
responding to an increased demand for commodities that extractive systems were not able to support or taking advantage
of new crops and integrating them into their traditional land
use systems. Some CMSAF reect strategies of occupying land
and taking it into production at relatively low cost, whereas
others are carefully built and managed systems where a variety
of crops occupy different ecological niches within a farming
system. During the second half of the twentieth century, many
CMSAF came under pressure from agronomists who favored
intensive, monoculture production systems in the style of the
Green Revolution. More recently, under the pressure of years
of low commodity prices and increased risks from global climate change, the advantages to tropical farmers of producing
several different outputs than depending on a single product
has been more commonly recognized among farmers and
agricultural policy makers (Ruf and Schroth, 2013). However,
globalization and increasing global demands for commodities
such as rubber and oil palm provide farmers with strong incentives to specialize and intensify their production systems, at
least where inputs are affordable and markets and policies are
206
References
Cassano, C.R., Schroth, G., Faria, D., Delabie, J.H.C., Bede, L., 2009. Landscape
and farm scale management to enhance biodiversity conservation in the cocoa
producing region of southern Bahia, Brazil. Biodiversity and Conservation 18,
577603.
Correia, M., Diabat, M., Beavogui, P., et al., 2010. Conserving forest tree diversity
in Guine Forestire (Guinea, West Africa): the role of coffee-based agroforests.
Biodiversity and Conservation 19, 17251747.
Cortina-Villar, S., Plascencia-Vargas, H., Vaca, R., et al., 2012. Resolving the
conict between ecosystem protection and land use in protected areas of the
Sierra Madre de Chiapas, Mexico. Environmental Management 49, 649662.
Dean, W., 1987. Brazil and the Struggle for Rubber. Cambridge: Cambridge
University Press.
Dhakal, B., Pinard, M.A., Gunatilleke, N., et al., 2012. Impacts of cardamom
cultivation on montane forest ecosystems in Sri Lanka. Forest Ecology and
Management 274, 151160.
Duguma, B., Gockowski, J., Bakala, J., 2001. Smallholder cacao (Theobroma cacao
Linn.) cultivation in agroforestry systems of West and Central Africa: challenges
and opportunities. Agroforestry Systems 51, 177188.
Estrada, A., Raboy, B.E., Oliveira, L.C., 2012. Agroecosystems and primate
conservation in the tropics: a review. American Journal of Primatology 00, 116.
Faria, D., Paciencia, M.L.B., Dixo, M.B.O., Laps, R.R., Baumgarten, J., 2007. Ferns,
frogs, lizards, birds and bats in forest fragments and shade cacao plantations in
two contrasting landscapes in the Atlantic forest, Brazil. Biodiversity and
Conservation 16, 23352357.
Feintrenie, L., Levang, P., 2009. Sumatra's rubber agroforests: advent, rise and fall
of a sustainable cropping system. Small-scale Forestry 8, 323335.
Fraser, J.A., Junqueira, A.B., Clement, C.R., 2010. Homegardens on Amazonian dark
earths, non-anthropogenic upland, and oodplain soils along the Brazilian middle
Madeira river exhibit diverging agrobiodiversity. Economic Botany 65, 112.
Garcia, C.A., Bhagwat, S.A., Ghazoul, J., et al., 2010. Biodiversity conservation in
agricultural landscapes: challenges and opportunities of coffee agroforests in the
Western Ghats, India. Conservation Biology 24, 479488.
Gockowski, J., Sonwa, D.J., 2008. Biodiversity and smallholder cocoa production
systems in West Africa. Sustainable Tree Crops Program Working Paper Series
6, 121.
Gockowski, J., Sonwa, D.J., 2011. Cocoa intensication scenarios and their
predicted impact on CO2 emissions, biodiversity conservation, and rural
livelihoods in the Guinea rainforest of West Africa. Environmental Management
48, 307321.
Gockowski, J., Tchatat, M., Dondjang, J.-P., Hietet, G., Fouda, T., 2010. An
empirical analysis of the biodiversity and economic returns to cocoa
agroforests in Southern Cameroon. Journal of Sustainable Forestry 29,
638670.
Gouyon, A., de Foresta, H., Levang, P., 1993. Does 'jungle rubber' deserve its
name? An analysis of rubber agroforestry systems in southeastern Sumatra.
Agroforestry Systems 22, 181206.
Hairiah, K., Sitompul, S.M., van Noordwijk, M., Palm, C., 2001. Carbon stocks of
tropical land use systems as part of the global C balance: effects of forest
conversion and options for clean development activities. In: van Noordwijl, M.,
Williams, S., Verbist, B. (Eds.), ASB Lecture Note 4A. Bogor: International Centre
for Research in Agroforestry, pp. 149.
Hall, J.M., Gillespie, T.W., Mwangoka, M., 2011. Comparison of agroforests and
protected forests in the East Usambara Mountains, Tanzania. Environmental
Management 48, 237247.
Jagoret, P., Michel-Dounias, I., Snoeck, D., Ngnogu, H.T., Malzieux, E., 2012.
Afforestation of savannah with cocoa agroforestry systems: A small-farmer
innovation in Central Cameroon. Agroforestry Systems 86, 493504.
Johns, N.D., 1999. Conservation in Brazil's chocolate forest: the unlikely persistence
of the traditional cocoa agroecosystem. Environmental Management 23, 3147.
de Jong, W., 2001. The impact of rubber on the forest landscape in Borneo. In:
Angelsen, A., Kaimowitz, D. (Eds.), Agricultural Technologies and Tropical
Deforestation. Wallingford: CAB International, pp. 367381.
Kumar, B.M., Nair, P.K.R., 2004. The enigma of tropical homegardens. Agroforestry
Systems 61, 135152.
Kusters, K., Ruiz-Perez, M., de Foresta, H., et al., 2008. Will agroforests vanish?
The case of damar agroforests in Indonesia. Human Ecology 36, 357370.
Laird, S.A., Awung, G.L., Lysinge, R.J., 2007. Cocoa farms in the Mount Cameroon
region: biological and cultural diversity in local livelihoods. Biodiversity and
Conservation 16, 24012427.
Leakey, R.R.B., Tchoundjeu, Z., Schreckenberg, K., Shackleton, S.E., Shackleton, C.
M., 2005. Agroforestry tree products (AFTPs): Targeting poverty reduction
and enhanced livelihoods. International Journal of Agricultural Sustainability 3,
123.
Leakey, R.R.B., Weber, J.C., Page, T., et al., 2012. Tree domestication in
agroforestry: progress in the second decade. In: Nair, P.K.R., Garrity, D.P. (Eds.),
Agroforestry The Future of Global Land Use. Dordrecht: Springer, pp. 133.
Matocha, J., Schroth, G., Hills, T., Hole, D., 2012. Integrating climate change
adaptation and mitigation through agroforestry and ecosystem conservation. In:
Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry The Future of Global Land Use.
Dordrecht: Springer, pp. 105126.
Mndez, V.E., Castro-Tanzi, S., Goodall, K., et al., 2012. Livelihood and
environmental trade-offs of climate mitigation in smallholder coffee agroforestry
systems. In: Wollenberg, E., Nihard, A., Tapio-Bistrm, M.L., Grieg-Gran, M.
(Eds.), Climate Change Mitigation and Agriculture. London: Earthscan,
pp. 370381.
207
Glossary
Agroforestry A managed land use that combines elements
of agriculture and forestry, sometimes described as a twotiered farming system.
Earthow A downslope viscous ow of soil and rock
material saturated with water under the pull of gravity.
Earthows are a shear above a failure plane in underlying
rock. They can be deep owing with the failure plane deeper
than the rooting depth of trees.
Gully An eroding landform created by running water.
Gullies in hill sides can be very large and difcult to
stabilize, notably where the bedrock is exposed.
Subterranean gullies are called tunnel gullies.
Loess A type of silty or loamy soil arising from wind
deposition of the parent material, which because of its loose
Introduction
Soil is one of the most precious resources. The loss of soil,
particularly through the land degradation processes of wind
and water erosion, is one of the most serious environmental
problems the world is faced with, as it reduces the means of
producing food. Approximately 80% of the worlds agricultural land was reported, almost 20 years ago, to suffer
moderate to severe soil erosion and 10% to suffer slight to
moderate erosion (Pimentel et al., 1995). These statistics are
unlikely to have improved since 1995, as farm sizes have increased, woody vegetative boundaries have been removed, and
more sloping land has been brought into pastoral and arable
cultivation to feed and fuel an increasing world population.
Erosion rates on sloped arable land are of an order higher than
rates on forested slopes (Cerdan et al., 2010; Pimentel et al.,
1995). Land-use change following deforestation of sloped
land is generally from forest to arable agriculture, with its accelerated risk of soil erosion. The negative effects of soil erosion include water pollution and siltation, crop yield
depression, organic matter loss, and reduction in water storage
capacity (e.g., Pimentel et al., 1995; Bakker et al., 2004; Cerdan
et al., 2004; Boardman and Poesen, 2006), which may lead to
fundamental social challenges, such as land abandonment and
the decline of rural communities (Bakker et al. 2005).
208
doi:10.1016/B978-0-444-52512-3.00247-3
209
210
(a)
(b)
Figure 1 (a) Severe slipping on soft mudstone in eastern North Island, New Zealand. (b) Young space planted willows reducing the risk of
further erosion on an unstable slope. Photos McIvor, I.
Earthow Erosion
Earthow is a ow of soil and underlying regolith, generally
characterized by retention of a pastured cover and often broken by tension cracks and smaller secondary movements. Such
ows do not result in a separate slip scar and debris. Earthows range from shallow to deep (1 to 470 m), from fastmoving to a very slow and discontinuous creep, and from
retaining a continuous turf mat to having a broken surface
with secondary movements. They may even have gullies cutting through them, increasing their instability. Earthows
move when the whole regolith is wetted up and the frictional
resistance is at a minimum. This is generally later in winter and
not usually in response to intense rainstorms.
The control measures applied depend on the type of
earthow. The measures rely on removing surface water to
minimize inltration by surface smoothing and constructing
diversion banks, tying together the surface with willow roots,
pair planting willows where gullies are most likely to form,
and planting at the toe of the movement to hold up the toe
(essential when the toe is being undercut by a waterway).
Both poplars and willows are used for managing earthows (Figures 2 and 3). Willows are preferable to poplars
for halting earthows, as their roots form thick mats when in a
wet environment. This holds the poorly structured mudstone
better than poplar roots, which do not have this matting
characteristic.
Slump Erosion
Slump erosion occurs where there is a backward rotation of a
signicant area of land. This erosion type is relatively uncommon, as most occur as a secondary feature following a
ow or large slip leaving an exposed headwall which then
collapses with a backward tilt. Slump erosion events are usually sufciently large (Figure 4) that tree planting alone cannot
control them. They need to have surface dam water drained
the surface smoothed, and the area retired and close planted in
trees. Once in trees, the slumps need to be closely managed, as
continuing movement overturns or topples trees requiring
clearing to keep drainage open and replanting. Over time
movement reduces.
211
Efs
Earthflow
Erosion
(a)
(b)
Figure 2 (a) Mudstone earthow on pastoral land with protected poplar poles space planted to control the movement and (b) shallow earthow
on mudstone with movement halted by successful poplar planting. Photos Eyles, G.
Gully Erosion
212
form and severity is very dependent on the rock type. The very
severe to extreme gully erosion is restricted to argillites (crushed), mudstone, and ne siltstones with each rock type
having its characteristic gully shape.
Prevention is much more effective than repair as once the
erosion is into the bedrock it is very difcult to get trees (or
any other plant material) established. The large gullies cannot
be repaired. The whole catchment needs to be retired from
grazing and planted in closed canopy trees with the eroding
surfaces repeatedly planted with willow wands to create a
vegetated surface. These sites take many generations before
they are repaired.
The construction of debris dams (Lancaster and Grant,
2006) at intervals up the gully coupled with pair planting of
willows has successfully controlled erosion from small gullies.
The willow root mats grow across the gully bed and over the
surface of the dam covering and protecting the eroding surface
(Figure 7(b)). Tree pairs are spaced from 8 to 15 m up the
gully depending on severity. Discontinuous gullies (Figure 7
(a)) are very common in hill country. Large erosion events ll
the valley bottoms and smaller events begin to scour them.
Prevention is by pair or single planting of willows up the
valley bottom at 1520 m spacing and at weak points developing a planted block with 23 rows of willows planted at
1.5 m spacing across the valley bottom and in an area fenced
out from grazing.
Rill Erosion
Pasture renewal in easy hill country is often on a 5 to 10 year
cycle involving desiccation of the existing pasture followed by
surface disking, planting of a fodder crop, and then oversowing with an improved pasture spp. mix. Rill erosion when
the surface is exposed can lead to severe soil loss (Figure 8).
(a)
(b)
Figure 7 (a) A discontinuous gully and (b) gully control achieved by stabilizing the base level through construction of debris dams supported by
willows. Note the willow root mat grown over the dam structure. Photos G. Eyles.
213
(a)
(b)
Figure 9 (a) Effective control of hill country stream bank erosion can often be achieved by bank planting of willows. (b) Mature poplars providing
stability and shade for a now stable stream. Photos G. Eyles.
214
developed to conserve soil and livelihoods, in which windbreaks were a key component. In 1987, approximately
858 000 windbreaks in the United States, mostly in the north
central and Great Plains areas, spanned 281 000 km and protected 546 000 ha (Williams et al., 1997). Agroforestry approaches to combating wind erosion and desertication have
been reported for Egypt (El-Flah, 2009), the Sudan (Dafa-Alla
and Al-Amin, 2011), and Pakistan (Akram et al., 2006), with
varying degrees of success.
Degree of erosion
Water erosion
Slight erosion
Moderate erosion
High erosion
Severe erosion
Extreme erosion
Total
66.76
35.14
16.87
7.63
2.92
129.32
Wind erosion
Slight erosion
Moderate erosion
High erosion
Severe erosion
Extreme erosion
Total
71.6
21.74
21.82
22.04
28.39
165.59
Table 2
215
The main regions of China suffering from water and soil erosion
Region
Geographical scope
Geographical features
Situation of erosion
Heilongjiang
Jilin
Liaoning
Inner Mongolia
Beijing
Hebei
Shangdong
Liaoning
Shanxi
Henan
Anhui
Shanxi
Shaanxi
Gansu
Inner Mongolia
Ningxia
Henan
Henan
Inner Mongolia
Hebei
Shaanxi
Ningxia
Gansu
Sichuan
Yunnan
Guizhou
Hubei
Chongqing
Shaanxi
Gansu
Tibet
Guizhou
Yunnan
Guangxi
Jiangxi
Hunan
Fujian
Guangdong
Guangxi
Hainan
Inner Mongolia
Shaanxi
Gansu
Qinghai
Ningxia
Xinjiang
Shallow soil
Bare rock
Steep slopes
Unproductive soil
Bare rock
Steep slopes
Low mountain and hilly area
Broken topography
Steep slopes
Rock desertication
Loess plateau
approximately
5000 t km 2 year 1
Slope disintegration
grassland
provinces of Shaanxi, Gansu, Qinghai, Ningxia, Inner Mongolia, Shanxi, and Henan), and the state-owned forest area in
Northeast of China (including the provinces of Jilin, Heilongjiang, Inner Mongolia, Hainan, and Xinjiang). Since the
inception of the program 2.7 million ha of plantations have
been established, 3.2 million ha of forests have been established by aerial seeding, 12 million ha of newly enclosed
216
Table 3
Project name
Project prole
Duration: 19992010
Geographical scope: 25 Provinces and Xinjiang production and construction corps
Relevant laws and regulations: Recommendations for Further Improving Sloping Land
Conversion Policy (2002), The Regulations on Sloping Land Conversion (2002)
Primary target: Solving the problem of water and soil erosion in key regions
to 2011, the completed construction area covers 289 000 km2,
Present situation: From 1999
2
2
among which 92 000 km from returning farmland to forest, 170 000 km from afforestation in
barren hills, and 27 000 km2 from closed forest. The forest coverage in the construction area
has undergone a 3% increase
Duration: 19782050
Geographical scope: 13 Provinces
Relevant laws and regulations: Recommendations for Further Improving the construction of
the three north shelterbelt system (2009)
Primary target: Effectively controlling the hazards of sand storms and water and soil erosion.
Constructing a shelterforest network for elds in the plains
Present situation: By the end of 2012, the total area of afforestation covered 265 000 km2. The
forest coverage in construction area now reaches 12.4% of the land area
Duration: 200110
Geographical scope: 5 Provinces
Relevant laws and regulations: Project Planning of BeijingTianjin Sand Storm Source
Control (2002)
Duration: 201030
Geographical scope: 7 Provinces
Relevant laws and regulations: Planning of Loess Plateau Comprehensive Management (2010)
Primary target: Controlling the water and soil erosion and reducing the quantity of sediment
owing into the Yellow river
Present situation: The area of afforestation covers 78 000 km2. The forest coverage in
construction area increased from 11% in 1977 to 19.6% in 2012
Duration: 200815
Geographical scope: 8 Provinces
Relevant laws and regulations: Planning of Rocky Desertication Comprehensive Treatment
200615 (2008)
Primary target: Controlling and preventing the spread of stony deserts and water and soil
erosion. Conversion of the slope land
Present situation: By the end of 2011, the area2 of afforestation reached to 8000 km2. The area
of stone desertication reduced by 9600 km from 2005 to 2011
Duration: 19982020
Geographical scope: 17 Provinces
Relevant laws and regulations: Implementation Plan of Natural Forest Protection in Upper
Reaches of Yangtze River and Upper and Middle Yellow River (2000), Implementation Plan of
Nature Forest Protection in the Key State-Owned Forest Areas in the Northeastern China and
Inner Mongolia (2000)
Primary target: Prohibiting the cutting of natural forest in upper reaches of the Yangtze River
and upper and middle Yellow River. Reducing the forest harvest in the key state-owned forest
areas in the Northeastern China and inner Mongolia
Present situation: The forest coverage in construction area has a 3.7% increase
Duration: 19882020
Geographical scope: 26 Provinces
Relevant laws and regulations: Greening Standard of Plain Counties In Northern and Central
China (1987), Greening Standard of Plain Counties in Southern China (1987), Planning of
Reaching Nation Standard in Greening the Plain Counties (1988), Program Planning of Plain
Farmland Shelterbelt 200610 (2006)
(Continued )
Table 3
217
Continued
Project name
Project prole
Primary target: Perfect the plain farmland shelterbelt system and forest ecosystem. Greening
Duration: 19892020
Geographical scope: 17 Provinces
Relevant laws and regulations: First-Stage Project Planning of Yangtze River Basin Shelter
along the highways, railways, and waterways. Improving the quality of the forest in plain area.
Insure stable grain production
Present situation: By the end of 2010, the area of afforestation reached 71 000 km2. The forest
coverage in construction area increased from 7.3% in 1987 to 15.8% in 2010
Forest System Construction (1986), Second-Stage Project Planning of Yangtze River Basin
Shelter Forest System Construction 20012010 (2000)
Primary target: Improving the deteriorative ecoenvironment in the Yangtze River Basin
Present situation: From 2002 to 2011, the area of afforestation reached to 11 700 km2. By the
end of 2011, the forest coverage in construction area reached to 45.4%
Duration: 200420
Geographical scope: Qinghai Province
Relevant laws and regulations: Overall Planning of Ecological Protection and Construction in
nonforested land and open forest land has been set aside for
natural regeneration, 101 million ha of forest has been taken
into management and protection, and 621 500 foresters have
been resettled in other locations.
The Shelterbelt Forest System Project covers the Northwest,
Northeast, and the North of China; the middle and lower
reaches of the Yangtze River; the coastal area; the Pearl River
Basin; the Huai River Basin; Taihang Mountain area; and the
plain area. By establishing farmland shelterbelt forest and
planting trees on barren land, by the end of 2008, 24.5 million
ha of forest had been conserved by the program and the forest
coverage in the three northern regions had increased from
5.1% in 1978 to 10.5% in 2008. The program has overseen the
improvement of 270 000 km2 of sandy lands and the stabilization of 380 000 km2 of water and soil erosion areas. Since
2000, the river basin programs within this project have collectively established 4.3 million ha of plantation.
The Sloping Land Conversion Program involves 25 provinces (Beijing, Tianjin, Hebei, Shanxi, Inner Mongolia, Liaoning, Jilin, Heilongjiang, Anhui, Jiangxi, Heinan, Hubei,
Hunan, Guangxi, Hainan, Hongqing, Sichuan, Guizhou,
Yunnan, Xizang, Shanxi, Gansu, Qinghai, Ningxia, and Xinjiang) and Xinjiang Production and Construction Corps. According to the principle of highlighting the key points, the
upper reaches of the Yangtze River, the upper and middle
reaches of the Yellow River, BeijingTianjin sand source district, critical lake watersheds, the Hongshui River Basin, the
Hei River Basin, and the Tarim River Basin are the focal points
of the program. This program began in 2000 after massive
ooding was caused in part by land clearing and focuses on
Chinas largest source of soil erosion and ood risk arable
farms on steep slopes. The program is a land retirement program that aims to reduce soil erosion by returning cropland on
steep slopes back to forest or grassland. Farmers are recompensed for giving up farming this land. Between 2000 and
218
Table 4
Program
Environmental situation
Species used
Region
Wind erosion
Populus tremula
Wind erosion
Rocky Desertication
Comprehensive Treatment
Project
Soil conservation
Mu Us Sandland
Loess plateau
Hunan
219
220
Summary
Soil is one of the most precious resources. The loss of soil,
particularly through the land degradation processes of wind
and water erosion, is one of the most serious environmental
problems the world is faced with, as it is reducing the means of
producing food. Approximately 80% of the worlds agricultural land was reported, almost 20 years ago, to suffer
moderate to severe soil erosion and 10% to suffer slight to
moderate erosion (Pimentel et al., 1995). It is possible to alter
the impact of these forms of erosion through the development
and implementation of national policies and effective technologies, coupled with changes in land use and alternative
economic opportunities for affected local communities.
Without economic protection, soil degradation is most likely
to continue in some other locality. Restorative technologies
incorporating trees in the agricultural landscape have been
developed in New Zealand and China and other countries to
reduce soil loss. Where these technologies are being applied,
they are proving to be effective in reducing erosion to low
levels, thereby retaining both soil quantity and quality for the
future.
References
Abdi, O.A., Glover, E.K., Luukkanen, O., 2013. Causes and impacts of land
degradation and desertication: Case study of the Sudan. International Journal of
Agriculture and Forestry 3, 4051.
Akram, M., Kahlown, M., Akram, S., Zamir, A., 2006. Desertication control for
sustainable land use in the Cholistan Desert, Pakistan. In: Lee, C., Schaaf, T.
(Eds.), Future of Drylands (International Scientic Conference on Desertication
and Drylands Research, Tunis, Tunisia, 1921 June 2006). The Netherlands:
Springer, pp. 483492 (Published: 2008).
Bakker, M.M., Govers, G., Kosmas, C., et al., 2005. Soil erosion as a driver of landuse change. Agriculture, Ecosystems and Environment 105, 467481.
Bakker, M.M., Govers, G., Rounsevell, M.D.A., 2004. The crop productivityerosion relationship: An analysis based on experimental work. Catena 57,
5576.
Boardman, J., Poesen, J., 2006. Soil erosion in Europe: Major processes, causes
and consequences. In: Boardman, J., Poesen, J. (Eds.), Soil Erosion in Europe
2006. Chichester: Wiley, pp. 479487.
Cerdan, O., Govers, G., Le Bissonnais, Y., et al., 2010. Rates and spatial variations
of soil erosion in Europe: A study based on erosion plot data. Geomorphology
122, 167177.
Cerdan, O., Le Bissonnais, Y., Govers, G., et al., 2004. Scale effect on runoff from
experimental plots to catchments in agricultural areas in Normandy. Journal of
Hydrology 299, 414.
Dafa-Alla, M.D., Al-Amin, N.K., 2011. Design, efciency and inuence of a
multiple-row, mix-species shelterbelt on wind speed and erosion control in arid
climate of North Sudan. Research Journal of Environmental and Earth Sciences
3, 655661.
Das, R., Bauer, S., 2012. Bio-economic analysis of soil conservation technologies in
the mid-hill region of Nepal. Soil and Tillage Research 121, 3848.
Delgado, M.E.M., Canters, F., 2012. Modeling the impacts of agroforestry systems
on the spatial patterns of soil erosion risk in three catchments of Claveria, the
Philippines. Agroforestry Systems 85, 411423.
El-Flah, A.H., 2009. The use of various wind barriers in controlling wind erosion
in north-western parts of Egypt. Journal of Applied Sciences Research 5,
490498.
Kusimi, J.M., 2008. Assessing land use and land cover change in the Wassa West
District of Ghana using remote sensing. GeoJournal 71, 249259.
Lancaster, S.T., Grant, G.E., 2006. Debris dams and the relief of headwater streams.
Geomorphology 82, 8497.
Li, C.J., Lei, J.Q., Gao, P., et al., 2012. Research progress of soil forming process
of aeolian sandy soil under the effect of articial shelter-belt. Acta Pedologica
Sinica 49, 12271234.
Li, M., Liu, A., Zou, C., et al., 2012. An overview of the Three-North shelterbelt
project in China. Forestry Studies in China 14, 7079.
Meena, L.R., Mann, J.S., Karim, S.A., 2012. Agroforestry practices in arid and semiarid regions of India: Challenges and opportunities. Indian Journal of Forestry
35, 18.
Pimentel, D., Harvey, C., Resosudarmo, P., et al., 1995. Environmental costs of soil
erosion and conservation benets. Science 267, 11171123.
Reisner, Y., de Filippi, R., Herzog, F., Palma, J., 2007. Target regions for silvoarable
agroforestry in Europe. Ecological Engineering 29, 401418.
Rosser, B.J., Ross, C.W., 2011. Recovery of pasture production and soil properties
on soil slip scars in erodible siltstone hill country, Wairarapa, New Zealand. New
Zealand Journal of Agricultural Research 54, 2344.
Saha, R., Mishra, V.K., Khan, S.K., 2011. Soil erodibility characteristics under
modied land-use systems as against shifting cultivation in hilly ecosystems of
Meghalaya, India. Journal of Sustainable Forestry 30, 310312.
Sanchez-Bernal, E., Ortega-Baranda, V., Dominguez-Hernandez, F., et al., 2013.
Soil erosion control using agroforestry terraces in San Pedro Mixtepec, Oaxaca,
Mexico. International Journal of Agricultural Sciences 3, 423439.
Shi, P., Yan, P., Yuan, Y., Nearing, M.A., 2004. Wind erosion research and control
in china: Past, present and future. Physical Geography 28, 366386.
Sourabh, D., Lynrah, M.M., Tiwari, B.K., 2013. Technological innovations in shifting
agricultural practices by three tribal farming communities of Meghalaya, northeast
India. Tropical Ecology 54, 133148.
Su, Y.Z., Wang, X.F., Yang, R., et al., 2010. Effects of sandy desertied land
rehabilitation on soil carbon sequestration and aggregation in an arid region in
China. Journal of Environmental Management 91, 21092116.
Thapa, G.B., Yila, O.M., 2012. Farmers land management practices and status of
agricultural land in the Jos Plateau, Nigeria. Land Degradation & Development
23, 263277.
Tsonkova, P., Bohm, C., Quinkenstein, A., Freese, D., 2012. Ecological benets
provided by alley cropping systems for production of woody biomass in the
temperate region: A review. Agroforestry Systems 85, 133152.
Williams, P.A., Gordon, A.M., Garrett, H.E., Buck, L., 1997. Agroforestry in
North America and its role in farming systems. In: Gordon, A.M.,
Newman, S.M. (Eds.), Temperate Agroforestry Systems. Wallingford, UK: CABI,
pp. 984.
Xu, J., van Noordwijk, M., He, J., et al., 2012. Participatory agroforestry
development for restoring sloping land in DPR Korea. Agroforestry Systems 85,
291303.
Xu, W.D., Liu, G.T., Duan, P.S., Zou, C.J., 1998. Study on Picea mongolica forest
ecosystem in Baiyinaobao natural reserve, Inner Mongolia. Beijing: China
Forestry Publishing House (in Chinese).
Relevant Websites
http://www.fao.org/docrep/x5388e/x5388e02.htm
Food and Agriculture Organization of the United Nations.
http://www.jeb.co.in/journal_issues/201303_mar13/paper_12.pdf
Journal of Environmental Biology.
http://www.china.org.cn/environment/2007-08/20/content_1034358.htm
Law of the Peoples Republic of China on Water and Soil Conservation.
http://www.poplarandwillow.org.nz
New Zealand Poplar & Willow Research Trust.
http://www.ldeo.columbia.edu/res/div/ocp/drought/dust_storms.shtml
The Earth Institute at Columbia University.
http://www.globalchange.umich.edu/globalchange2/current/lectures/land_deg/
land_deg.html
University of Michigan.
221
Glossary
Coppicing Cutting trees close to the ground level to
produce regrowth from the remaining stump.
Deep capture The extraction of nutrients by tree roots
from soil depths beyond the reach of crop roots.
Pollarding Cutting back the crown of a tree but leaving
the main trunk with the objective of harvesting wood and
Introduction
Much of the worlds agricultural land is degrading rapidly, and
losing its productivity due to soil erosion and nutrient mining
associated with continuous cropping without nutrient inputs
and soil conservation. An estimated 24% of the worlds land
area has been degrading over the past 25 years, directly affecting the livelihoods of 1.5 billion people (Bai et al., 2008).
Approximately 19% of the degraded land is cropland (Bai
et al., 2008). According to the Global Assessment of Humaninduced Soil Degradation, soil erosion affects 83% of the
global degraded area (Bai et al., 2008). Soil degradation by
erosion alone affects 1966 million hectares worldwide (Lal,
2007). In Africa, the annual average nutrient (NPK) loss is
estimated at 958 kg ha1 year1 in 28 countries and 61
88 kg ha1 year1 in the remaining 21 (Chianu et al., 2012).
Recent global analyses show that N limitation is particularly
widespread in all ecosystems (LeBauer and Treseder, 2008; Liu
et al., 2010). The global average N recovery rate is 59%, indicating that nearly 41% of N inputs are lost in ecosystems (Liu
et al., 2010). Almost 80% of African countries experience N
decit or N stress problems, which, along with poverty, cause
food insecurity and malnutrition (Liu et al., 2010). In total,
29% of the global cropland area experiences P decits (MacDonald et al., 2011).
Conventionally in modern agriculture, increased productivity has been achieved mainly through application of synthetic inorganic fertilizers. However, the increasing price of
synthetic fertilizers and the inability of poor farmers to gain
access to them pose severe constraints on their widespread use.
Although organic matter may be an alternative source of nutrients, neither animal manure nor green biomass is usually
found in adequate quantities to meet the high application
rates (1040 Mg ha1 year1) required to meet the nutrient
222
doi:10.1016/B978-0-444-52512-3.00022-X
Table 1
223
Cereal yield response to fertilizer trees summarized from studies across sub-Saharan Africa
Cereal crop
Species
Increasef (%7SE)
Maize
Pigeon peaa,b
Tephrosiaa,b
Leucaenab,c
Sesbaniaa,b
Gliricidiad
Faidherbiae
Synthetic fertilizer
Gliricidiad
Faidherbiae
Sesbaniaa,b
Vachelliae
Faidherbiae
24
28
6
42
15
12
72
4
5
2
3
5
2.170.2
2.170.1
2.570.2
3.070.1
3.270.1
4.570.2
3.870.1
1.570.1
1.070.2
1.870.1
0.770.1
1.270.1
0.770.1
0.970.1
1.070.1
1.770.1
2.270.1
2.570.2
2.270.1
0.170.1
0.370.1
0.670.1
0.0470.1
0.470.1
89.8713.2
206.3742.6
94.5712.2
318.1782.5
295.9727.8
184.6733.9
383.8740.5
93.875.3
144.4722.8
180.44719.1
107.8714.4
149.3714.4
Sorghum
Millet
(69)
(177)
(78)
(262)
(127)
(88)
(384)
(10)
(14)
(24)
(11)
(13)
Relay cropping.
Improved fallow.
c
Alley cropping.
d
Intercropping.
e
Parkland.
f
Increase over the no-input control.
Abbreviation: N number of data points representing either sites or years within a study.
Note: The yield increase is the difference between the treatment and the control (no input) on the same site. The percent increase is increase in yield over the control in percentage
terms, and this was calculated as 100*(yield increase)/control yield.
b
224
Table 2
Crop
Country
Mean yield
(Mg ha1)
Yield increaseb
(Mg ha1)
(%)
References
Cabbagec
Zambia
43.1
53.6
32.6
57.6
68.3
79.8
57.1
51.1
55.0
49.7
40.8
59.7
80.8
7.6
5.0
3.0
10.0
0.32
0.41
0.24
26.1
36.6
15.6
40.6
40.2
51.7
29
28.4
32.3
26.7
17.8
27.9
48.9
6.7
4.1
2.1
9.1
0.10
0.19
0.02
154
215
92
239
143
184
103
125
142
116
78
88
153
784
481
249
106
43.1
84.2
9.4
Oniond
Cabbage
Onion
Cabbage
Rape
Paprika
Zambia
South Africa
Malawi
This represents fresh weight in the case of cabbage, rape, and onion, whereas dry weight in the case of paprika.
Increase over the no-input control.
c
Average of 31 farmers' elds.
d
Average of 12 farmers' elds.
Note: The yield increase is the difference between the treatment and the control (no input) on the same site. The percent increase is increase in yield over the control in percentage
terms, and this was calculated as 100*(yield increase)/control yield.
b
availability of macronutrients (extractable N, P, and K), cations and improvement in soil pH, increased organic matter
(SOM), enhanced biological activity, improved soil physical
properties, and better water relations.
225
Increase (%) in N and P stocks due to fertilizer and nutrient uptake by crop relative to crop monoculture or areas outside tree
Agroforestry (crop)
Tree species
Increase (%)
Country
Reference
N stocks
Cacao
Parkland
Albizia
Faidherbia
N uptake
Parkland (millet)
Alley cropping (maize)
510
15156
200
5090
100150
529
20
139.2
126.6
159.6
170.4
50114
100300
156
299
76
160
99
2.34.5
18134
30
44125
529
160.7
92
110
121
Ghana
Sahel
Niger
Sudan
Ethiopia
Malawi
Viet Nam
Niger
Nigeria
Nigeria
Nigeria
Nigeria
USA
Malawi
Zambia
Zambia
Zambia
Zambia
Ghana
Sahel
Niger
Ethiopia
Malawi
Malawi
Zambia
Zambia
Malawi
P stocks
P uptake
Cacao
Parkland
Intercropping
Intercropping
Tephrosia
Faidherbia
Albizia
Gliricidia
Leucaena
Leucaena
Albizia
Gliricidia
Sesbania
Tephrosia
Gliricidia
Leucaena
Albizia
Faidherbia
Gliricidia
Gliricidia
Leucaena
Gliricidia
226
227
228
Table 4
Changes in soil physical properties (020 cm) due to fertilizer trees (FT) in improved fallow and the control (sole maize) and the
% change (%D) at Msekera, Kagoro, and Kalunga sites in Zambia and Domboshawa in Zimbabwe
Variable
Tree species
Site
FT
Control
(%D)
Reference
Bulk density
(Mg m3)
Gliricidia
Msekera
Leucaena
Vachelia
Sesbania
Domboshawa
Msekera
Sesbania
Domboshawa
Msekera
1.39
1.40
1.35
1.33
1.35
1.59
1.36
83.3
65.0
38.0
80.0
4.4
16
3.7
5.5
435
20.0
0.13
4.4
9.5
21.0
8.0
12
5.2
16.0
7.1
30.0
21.0
7.0
21.0
14.0
7.0
56.4
10.9
61.1
10.7
0.6
0.8
1.0
0.9
2.2
2.9
0
21.0
1.53
1.42
1.53
1.41
1.42
1.66
1.41
61.2
55.0
32.0
61.2
2.9
4.0
2.9
2.9
5.0
4.0
0.08
2.1
2.9
7.0
5.0
5.0
2.1
7.0
5.0
15.0
9.0
3.0
15.0
9.0
3.0
15.8
1.0
7.6
5.7
1.2
1.2
1.2
1.2
3.2
3.2
57.0
57.0
9.2
1.4
11.8
5.7
4.9
4.2
3.5
36.1
18.2
18.8
30.7
51.7
300.0
27.6
89.7
600.0
400.0
62.5
109.5
227.6
200.0
60.0
140.0
147.6
128.6
42.0
76.5
133.3
133.3
40.0
55.6
133.3
257.0
990.0
703.9
87.7
50.0
33.3
16.7
25.0
31.3
9.4
100.0
63.2
Aggregate stability
(mm)
Inltration rate
(mm hr1)
Pigeon pea
Gliricidia
Leucaena
Vachelia
Sesbania
Sesbania
Pigeon pea
Tephrosia
Time to runoff
(min)
Drainage
(mm)
Penetrometer resist
(Mpa)
Vachelia
Sesbania
Tephrosia
Tephrosia
Sesbania
Gliricidia
Leucaena
Vachelia
Sesbania
Pigeon pea
Vachelia
Sesbania
Kagoro
Msekera
Kagoro
Kagoro
Domboshawa
Msekera
Kagoro
Kalunga
Msekera
Domboshawa
Msekera
Kalunga
Msekera
Domboshawa
Kalunga
Msekera
Domboshawa
Kalunga
Msekera
Msekera-1a
Msekera-1b
Msekera-2a
Msekera-2b
Kagoro
Kagoro
Kagoro
Kagoro
Msekera
Msekera
Domboshawa
Domboshawa
229
Provision of Products
Most N-xing trees provide various products including wood,
fruits, edible seeds, and fodder that are rich in protein and
increase pasture productivity.
230
Table 5
Potential annual harvestable fuelwood produced from fertilizer trees planted in contour strips, woodlots, or rotational fallows
Tree species
Age (years)
Quantity
(Mg ha1 yr 1)
Sufcient for N
families of 6
Country
References
Calliandra
Casuarina
Acacia crassicarpa
A. crassicarpa
Vachellia nilotica
Senegalia (Acacia) polycantha
Leucaena
Acacia crassicarpa
A. mangium
Senegalia (Acacia) polycantha
Vachellia nilotica
Gliricidia
Leucaena
Sesbania
Gliricidia
Sesbania
Sesbania
Alder
Casuarina
Leucaena
Tagasaste
Leucaena single row
Leucaena double row
4.5
4.5
5
4
7
7
7
5
5
5
5
5
3
3
3
13
Na
Na
Na
Na
Na
2.7
2.7
3.2
1.8
22.4
1924.0
1.2
10.1
12.7
51.0
40.0
39.0
27.0
30.0
9.7
8.0
7.0
7.3
2.0
7.0
11.0
10.0
11.0
21.2
18.2
1.1
0.6
7.7
8.2
0.4
3.5
4.4
17.5
13.7
13.4
9.3
10.3
3.3
2.7
2.4
2.5
0.7
2.4
3.8
3.4
3.8
7.3
6.2
Tanzania
Tanzania
Tanzania
Zambia
Rwanda
Kenya
better quality and yield than in the open areas (Treydte et al.,
2007). For example, grass productivity under faidherbia and
parkia canopies was two to six times higher than in open areas
in West African parklands (Boffa, 1999). Similarly, in Kenya
grass productivity under acacia (now Vachellia tortilis) canopies
was 1.52.3 times higher than outside the tree canopies
(Weltzin and Coughenour, 1990). At Pakchong in Thailand,
dry matter yield over 840 days was 3041.5 Mg ha1 in a
mixture of grass and leucaena compared to 2536.8 Mg ha1
in grass alone (Tudsri et al., 2002). Similarly, at Turrialba in
Costa Rica, production of star grass was 16.9 Mg ha1 year1
with Erythrina compared to 11.7 Mg ha1 year1 in grass
monoculture (Kass et al., 1997).
In the parklands in the Sahel, pods of faidherbia provide a
valuable source of dry season fodder. Parkia, locally called
Nr, is also a valuable source of fodder in the Sahel, where its
branches are lopped by farmers and fed to livestock in the dry
season when grass is scarce. Supply of protein, which is the
most important nutrient for cattle production on rangelands,
can also be improved through fodder supplements from the
legume genera Acacia, Vachellia (Acacia), Leucaena, etc. (Lefroy
et al., 1992; Mapiye et al., 2011). As a result, meat and milk
production is signicantly improved. An analysis of results
from experiments in Latin America and Australia indicated
470% increase in live weight gain and beef production using
leucaena pastures (Jones, 1994).
Trade-offs
Under certain circumstances, the benets of fertilizer trees
could be offset by tree-crop competition for light, nutrients
and other resources, soil acidication, or gaseous emissions
231
soil, Seneviratne and Van Holm (1998) found over 5900 times
more N2O emission from soil without mulch than from plots
that received gliricidia mulch. In the same experiment, N2O
emission from urea fertilizer was over 25 000 times higher
than from plots that received gliricidia mulch (Seneviratne and
Van Holm, 1998).
Conclusions
This review suggests that diversication of agro-ecosystems
with fertilizer trees can optimize indigenous soil N supply and
increase productivity of the land. Fertilizer trees have an added
advantage: ensuring a multifunctional agriculture that provides timber, fodder, shade, soil improvement, and watershed
management. Unlike synthetic N sources, fertilizer trees ensure
greater internal nutrient recycling and water availability, thus
contributing to greater nutrient use efciency. Therefore, they
can make a major contribution to sustainable agriculture by
minimizing external inputs, particularly N fertilizers, increasing resource and land use efciency, and slowing down
erosion. The savings on synthetic fertilizer costs and GHG
mitigation potential could also be substantial. Unlike synthetic fertilizers, fertilizer trees may play a signicant role in
reducing N leaching, which is particularly important during
periods of reduced ground cover by herbaceous plants, such as
between cropping seasons. The advantage of organic inputs
over synthetic fertilizers is that much of the N from organic
inputs not used by the crop is usually incorporated into various SOM pools, or assimilated by the associated trees, thus
remaining in the system for other uses. N from inorganic pools
not taken by the crop is subjected to higher levels of leaching
and denitrication. Thus, the accumulation of N in SOM pools
over time is more sustainable compared to synthetic N fertilizer, which releases nutrients rapidly. The potential of inorganic fertilizers to ameliorate the physical and biological
degradation of poorly buffered soils is limited. Synthetic fertilizers, however, will remain a necessary input to agriculture
to feed the increasing human population. Therefore, the focus
of this article is not just whether fertilizer trees are better or
worse than mineral fertilizers, because both play an important
(and complementary) role in food production. The authors
strongly believe that smallholder farmers would benet if
development planners were to emphasize the merits of different fertility replenishment approaches and take advantage
of the synergy between fertilizer trees and mineral fertilizers
rather than focusing on the organic versus inorganic debate.
Although the rate of adoption of fertilizer trees has been
lower than anticipated in many regions of the world, there have
been notable successes in other parts. In the traditional production systems, the adoption of fertilizer trees has been driven
by local tradition, economic factors, and land ownership. These
traditional systems are being degraded and losing their productivity, but they may be a source of inspiration in the design of
new land management practices where fertilizer trees can play a
greater role in increasing food, forage, and bre production.
However, a longer-term vision and signicant investment in
research and development are needed. Screening of candidate
tree species and development of innovations appropriate to
specic conditions are important where these do not exist.
232
Where appropriate innovations already exist, barriers to adoption and risks that the adoption presents need to be identied.
Acknowledgment
We thank our colleagues and collaborators whose work has
provided primary data for this publication. We also thank the
Canadian International Development Agency (CIDA), Swedish
International Development Agency (Sida), US Agency for
International Development (USAID), Irish Aid, and Flanders
International Cooperation Agency (FICA) for the nancial
support for much of the work that laid the foundation.
References
Abril, A., Bucher, E.H., 2001. Overgrazing and soil carbon dynamics in the western
Chaco of Argentina. Applied Soil Ecology 16, 243249.
Aguiar, A.C.F., Bicudo, S.J., Sobrinho, J.R.S.C., et al., 2010. Nutrient recycling
and physical indicators of an alley cropping system in a sandy loam soil in
the pre-Amazon region of Brazil. Nutrient Cycling in Agroecosystems 86,
189198.
Ajayi, O.C., Place, F., Akinnifesi, F.K., Sileshi, G.W., 2011. Agricultural success from
Africa: the case of fertilizer tree systems in southern Africa (Malawi, Tanzania,
Mozambique, Zambia and Zimbabwe). International Journal of Agricultural
Sustainability 9, 129136.
Akinnifesi, F.K., Kang, B.T., Sanginga, N., Tijani-Eniola, H., 1997. Nitrogen use
efciently and N-competition between Leucaena hedgerows and maize in alley
cropping systems. Nutrient Cycling in Agroecosystems 47, 7180.
Akinnifesi, F.K., Ajayi, O.C., Sileshi, G., et al., 2010. Fertiliser trees for sustainable
food security in the maize-based production systems of East and Southern Africa.
A review. Agronomy for Sustainable Development 30, 615619.
Anim-Kwapong, G.J., 2006. Nitrogen value of pruning residues of some neotropical
Albizia species with potential as shade for cacao. Tropical Science 46, 4549.
Anoka, U.A., Akobundu, I.O., Okonkwo, S.N.C., 1991. Effect of Gliricidia sepium
(Jacq.) Steud and Leucaena leucocephala (Lam.) de Wit on the development of
Imperata cylindrical (L.) Raeuschel. Agroforestry Systems 16, 112.
Argel, P.J., Lascano, C.E., Ramrez, L., 1998. Leucaena in Latin American farming
systems: Challenges for development. Paper Presented at the Workshop
Leucaena: Adaptation, Quality and Farming Systems, 914 February 1998,
Hanoi, Vietnam. ACIAR: Canberra.
Bai, Z.G., Dent, D.L., Olsson, L., Schaepman, M.E., 2008. Proxy global assessment
of land degradation. Soil Use and Management 24, 223234.
Bayala, J., Sileshi, W.G., Coe, R., et al., 2012. Cereal yield response to conservation
agriculture practices in dry lands of West Africa: a quantitative synthesis. Journal
of Arid Environments 78, 13225.
Beer, J., Muschler, R., Kass, D., Somarriba, E., 1998. Shade management in coffee
and cacao plantations. Agroforestry Systems 38, 139164.
Boffa, J.M., 1999. Agroforestry parklands in sub-Saharan Africa. FAO Conservation
Guide 34. Agroforestry Systems 52 (2), 169170.
Buresh, R.J., Tian, G., 1998. Soil improvement by trees in sub-Saharan Africa.
Agroforestry Systems 38, 5176.
Chianu, J.N., Chianu, J.N., Mairura, F., 2012. Mineral fertilizers in the farming
systems of sub-Saharan Africa: A review. Agronomy for Sustainable Development
32, 545566.
Chikowo, R., Mapfumo, P., Nyamugafata, P., Giller, K.E., 2004. Woody legume
fallow productivity, biological N2-xation and residual benets to two successive
maize crops in Zimbabwe. Plant and Soil 262, 303315.
Chirwa, T.S., Mafongoya, P.L., Chintu, R., 2003. Mixed planted-fallows using
coppicing and noncoppicing tree species for degraded Acrisols in eastern
Zambia. Agroforestry Systems 59, 243251.
Chirwa, T.S., Mafongoya, P.L., Mbewe, D.N.M., Chishala, B.H., 2004. Changes in
soil properties and their effects on maize productivity following Sesbania sesban
and Cajanus cajan improved fallow systems in eastern Zambia. Biology and
Fertility of Soils 40, 2027.
Chirwa, P.W., Ong, C.K., Maghembe, J.A., Black, C.R., 2007. Soil water dynamics
in cropping systems containing Gliricidia sepium, pigeonpea and maize in
southern Malawi. Agroforestry Systems 69, 2943.
Dick, J., Skiba, U., Munro, R., Deans, D., 2006. Effect of N-xing and non N-xing
trees and and crops on NO and N2O emissions from Senegalese soils. Journal
of Biogeography 33, 416423.
Dong-Gill, K., 2012. Estimation of net gain of soil carbon in a nitrogen-xing tree
and crop intercropping system in sub-Saharan Africa: results from re-examining
a study. Agroforestry Systems 86, 175184.
Dong-Gill, K., Hernandez-Ramirez, G., Giltrap, D., 2012. Linear and nonlinear
dependency of direct nitrous oxide emissions on fertilizer nitrogen input: A metaanalysis. Agriculture, Ecosystems and Environment 168, 5365.
Fagerstrm, M.H.H., Nilsson, S.I., van Noordwijk, M., et al., 2002. Does Tephrosia
candida as fallow species, hedgerow or mulch improve nutrient cycling and
prevent nutrient losses by erosion on slopes in northern Viet Nam? Agriculture
Ecosystems and Environment 90, 291304.
Franche, C., Lindstrm, K., Elmerich, C., 2009. Nitrogen-xing bacteria
associated with leguminous and nonleguminous plants. Plant and Soil 321,
3559.
Gacheru, E., Rao, M.R., 2001. Managing Striga infestation on maize using organic
and inorganic nutrient sources in western Kenya. International Journal Pest
Management 47, 233239.
Hall, N.M., Kaya, B., Dick, J., et al., 2006. Effect of improved fallow on crop
productivity, soil fertility and climate-forcing gas emissions in semi-arid
conditions. Biology and Fertility of Soils 42, 224230.
Herridge, D., Peoples, M.B., Boddey, R.M., 2008. Global inputs of biological
nitrogen xation in agricultural systems. Plant and Soil 311, 118.
Isaac, M.E., Timmer, V.R., Quashie-Sam, S.J., 2007. Shade tree effects in an
8-year-old cocoa agroforestry system: biomass and nutrient diagnosis of
Theobroma cacao by vector analysis. Nutrient Cycling in Agroecosystems 78,
155165.
Jama, B., Getahun, A., 1991. Fuelwood production from Leucaena leucocephala
established in fodder crops at Mtwapa, Coast Province, Kenya. Agroforesto
Systems 16, 119128.
Jayasundara, H.P.S., Dennett, M.D., Sangakkara, U.R., 1997. Biological nitrogen
xation in Gliricidia sepium and Leucaena leucocephala and transfer of xed
nitrogen to an associated grass. Tropical Grasslands 31, 529537.
Jones, R.M., 1994. The role of Leucaena in improving the productivity of grazing
cattle. In: Gutteridge, R.C., Shelton, H.M. (Eds.), Forage Tree Legumes in
Tropical Agriculture. Wallinford, UK: CAB Intemational.
Kalinganire, A., Weber, J.C., Uwamariya, A., Kone, B., 2008. Improving rural
livelihoods through domestication of indigenous fruit trees in the parklands of
the Sahel. In: Akinnefesi, F.K., Leakey, R.B., Ajayi, O.C., et al. (Eds.), Indigenous
Fruit Trees in the Tropics: Domestication, Use and Commercialization.
Wallingford, UK: CABI, pp. 370392.
Kamara, C.S., Haque, I., 1992. Faidherbia albida and its effects on Ethiopian
highland Vertisols. Agroforestry Systems 18, 1729.
Kang, B.T., Caveness, F.E., Tian, G., Kolawole, G.O., 1999. Longterm alley cropping
with four hedgerow species on an Alsol in southwestern Nigeria Effect on
crop performance, soil chemical properties and nematode population. Nutrient
Cycling in Agroecosystems 54, 145155.
Kaonga, M.L., Coleman, K., 2008. Modelling soil organic carbon turnover in
improved fallows in eastern Zambia using the Roth C-26.3 model. Forest
Ecology and Management 256, 11601166.
Kass, D.C.L., Sylvester-Bradley, R., Nygren, P., 1997. The role of nitrogen xation
and nutrient supply in some agroforestry systems of the Americas. Soil Biology
and Biochemistry 29, 775785.
Kho, R.M., Yacouba, B., Yay, M., et al., 2001. Separating the effects of trees on
crops: the case of Faidherbia albida and millet in Niger. Agroforestry Systems
52, 219238.
Kimaro, A.A., Isaac, M.E., Chamshama, S.A.O., 2011. Carbon pools in tree biomass
and soils under rotational woodlot systems in Eastern Tanzania. In: Kumar, B.M.,
Nair, P.K.R. (Eds.), Carbon Sequestration Potential of Agroforestry Systems:
Opportunities and Challenges. Dordrecht, The Netherlands: Springer Science,
pp. 129143.
Kimaro, A.A., Timmer, V.R., Mugasha, A.G., Chamshama, S.A.O., Kimaro, D.A.,
2007. Nutrient use efciency and biomass production of tree species for
rotational woodlot systems in semi-arid Morogoro, Tanzania. Agroforestry
Systems 71, 175184.
Kuntashula, E., Mafongoya, P.L., Sileshi, G., Lungu, S., 2004. Potential of biomass
transfer technologies in sustaining vegetable production in the wetlands
(dambos) of eastern Zambia. Experimental Agriculture 40, 3751.
Kuntashula, E., Sileshi, G., Mafongoya, P.L., Banda, J., 2006. Farmer participatory
evaluation of the potential for organic vegetable production in the wetlands of
Zambia. Outlook on Agriculture 35, 299305.
Kwesiga, F., Coe, R., 1994. Potential of short rotation sesbania fallows in eastern
Zambia. Forest Ecology and Management 64, 161170.
Lal, R., 2007. Anthropogenic inuences on world soils and implications to global
food security. Advances in Agronomy 93, 6993.
LeBauer, D.S., Treseder, K.K., 2008. Nitrogen limitation of net primary productivity
in terrestrial ecosystems is globally distributed. Ecology 89, 371379.
Lefroy, E.C., Dann, P.R., Wildin, J.H., Wesley-Smith, R.N., McGowan, A.A., 1992.
Trees and shrubs as sources of fodder in Australia. Agroforestry Systems 20,
117139.
Liu, J., You, L., Amini, M., et al., 2010. A high-resolution assessment on global
nitrogen ows in cropland. PNAS 107, 80358040.
Lojka, B., Preininger, D., Van Damme, P., et al., 2012. Use of the Amazonian tree
species Inga edulis for soil regeneration and weed control. Journal of Tropical
Forest Science 24 (1), 89101.
Lose, S.J., Hilger, T.H., Leihner, D.E., Kroschel, J., 2003. Cassava, maize and
tree root development as affected by various agroforestry and cropping
systems in Bnin, West Africa. Agriculture, Ecosystems and Environment 100,
137151.
Mafongoya, P.L., Kuntashula, E., Sileshi, G., 2006. Managing soil fertility and
nutrient cycles through fertilizer trees in southern Africa. In: Uphoff, N., Ball, A.
S., Fernandes, E., et al. (Eds.), Biological Approaches to Sustainable Soil
Systems. Boca Raton, FL: Taylor & Francis, pp. 273289.
Mafongoya, P.L., Mpepereki, S., Dzowela, B.H., et al., 1997. Effect of pruning quality
and method of pruning placement on soil microbial composition. African Crop
Science Proceedings 3, 393398.
Makumba, W., Akinnifesi, F.K., Janssen, B., Oonema, O., 2007. Long-term impact of
gliricidia-maize simultaneous intercropping systems on carbon sequestration and
soil properties. Agriculture, Ecosystems and Environment 118, 237243.
Mapiye, C., Chimonyo, M., Marufu, M.C., Dzama, K., 2011. Utility of Acacia karroo
for beef production in Southern African smallholder farming systems: A review.
Animal Feed Science and Technology 164, 135146.
MacDonald, G.K., Bennett, E.M., Potter, P.A., Ramankutty, N., 2011. Agronomic
phosphorus imbalances across the worlds croplands. PNAS 108, 30863091.
Muchecheti, F., Madakadze, I.C., Soundy, P., 2012. Production of rape (Brassica
napus L.) on soils amended with leguminous tree prunings: Yield responses in
relation to the chemical composition of the tree prunings. African Journal of
Agricultural Research 7, 35413549.
Muoz, C., Zagal, E., Ovalle, C., 2007. Inuence of trees on soil organic matter in
Mediterranean agroforestry systems: an example from the Espinal of central
Chile. European Journal of Soil Science 58, 728735.
Mweta, D.E., Akinnifesi, F.K., Saka, J.D.K., et al., 2007. Green manure from
prunings and mineral fertilizer affect phosphorus adsorption and uptake by maize
crop in a gliricidia-maize intercropping. Scientic Research and Essay 2,
446453.
Mwihomeke, S.T., Chamshama, S.A.O., 2004. Fuelwood production by tree species
planted along contour strips on the slopes of west Usambara Mountains,
Tanzania. In: Rao, M.R., Kwesiga, F.R. (Eds.), Proceedings of the Regional
Agroforestry Conference on Agroforestry Impacts on livelihoods in Southern
Africa: Putting Research into Practice. Nairobi, Kenya: World Agroforestry Centre
(ICRAF), pp. 165171.
Ndayambaje, J.D., Mohren, G.M.J., 2011. Fuelwood demand and supply in Rwanda
and the role of agroforestry. Agroforestry Systems 87, 797814.
Ngugi D.N., 2002. Agroforestry in Malawi and Zambia. Summary Report of a CTA/
MAFFE study visit. The Netherlands: CTA, Wageningen, pp. 32.
Nyadzi, G.I., Otsyina, R.M., Banzi, F.M., et al., 2003. Rotational woodlot technology
in northwestern Tanzania: tree species and crop performance. Agrofory Systems
59, 253263.
Nyamadzawo, G., Nyamugafata, P., Chikowo, R., et al., 2006. Soil and carbon losses
under rainfall simulation from two contrasting soils under maize-improved
fallows rotation in Eastern Zambia. In: Roose, E.J., Lal, R., Feller, C., Barthes, B.,
Stewarts, B.A. (Eds.), Soil Erosion and Carbon Dynamics. Boca Raton, FL: Taylor
and Francis, pp. 197206.
Nyamadzawo, G., Nyamugafata, P., Chikowo, R., Giller, K., 2007. Residual effects of
fallows on selected soil hydraulic properties in a kaolinitic soil subjected to
conventional tillage (CT) and no tillage (NT). Agroforestry Systems 72, 161168.
Nyamadzawo, G., Nyamugafata, P., Chikowo, P., Giller, K.E., 2008a. Residual effects
of fallows on inltration rates and hydraulic conductivities in a kaolinitic soil
233
234
8-year-results. In: Scott, D.E., Mohtar, R.H., Steinhardt, G.C. (Eds.), Sustaining
the Global Farm. West Lafayette: USDA-ARS, pp. 333337.
Treydte, A.C., Heitknig, I.M.A., Prins, H.H.T., Ludwig, F., 2007. Trees enhance
grass layer quality in African savannas of distinct rainfall and soil fertility.
Perspectives in Plant Ecology, Evolution and Systematics 8, 197205.
Tudsri, S., Ishii, Y., Numaguchi, H., Prasanpanich, S., 2002. The effect of cutting
interval on the growth of Leucaena leucocephala and three associated grasses in
Thailand. Tropical Grasslands 36, 9096.
Weltzin, J.F., Coughenour, M.B., 1990. Savanna tree inuence on understory
vegetation and soil nutrients in northwestern Kenya. Journal of Vegetation
Science 1, 325334.
Wick, B., Khne, R.F., Vlek, P.L.G., 1998. Soil microbiological parameters as
indicators of soil quality under improved fallow management systems in southwestern Nigeria. Plant and Soil 202, 97107.
Wong, M.T.F., Hairiah, K., Utami, R., Alegre, J., 2002. Managing acidity and
aluminium toxicity in organic based agroecosystems. In: Ong, C., van Noordwijk,
M., Cadisch, G. (Eds.), Belowground interactions in tropical agroecosystems with
multiple plant components. Wallingford: CABI publication, pp. 143156.
Zahran, H.H., 1999. Rhizobium-legume symbiosis and nitrogen xation under severe
conditions and in an arid climate. Microbiology and Molecular Biology Reviews
63, 968989.
Glossary
Agroforestry The cultivation of trees and crops in
interacting combinations.
Alley farming A method of planting, in which rows of a
crop are sown between rows or hedges of nitrogen-xing
plants, the roots of which enrich the soil.
Climate change mitigation Actions to limit the
magnitude and rate of long-term climate change. Climate
change mitigation generally involves reductions in human
emissions of greenhouse gases.
Introduction
Livestock are key components of farming systems throughout
the world. Although livestock are often associated with wealth
in many countries, approximately 1 billion head of livestock
are held by more than 600 million poor smallholders, comprising approximately 70% of the world's rural poor (IFAD,
2004).
Low quality and quantity of feeds are major constraints
limiting animal productivity. Feeding livestock has become
particularly problematic in the developing world because of
rising population growth increasing the demand for livestock
products. In both developing and developed countries, the
supply of livestock feed has become more scarce because of
diminishing land availability due to the reduction in the
quantity and quality of rangeland and natural grasslands.
Changing cropping patterns, such as the recent increase in the
area under crops for biofuels, further exacerbates feed availability (FAO, 2001; Ayantunde et al., 2005; IFPRI, 2008).
Fodder trees and shrubs (the terms trees and shrubs are
used interchangeably) are both old and new solutions to feed
problems. They can be characterized as old solutions because
farmers have fed tree foliage to their livestock for centuries,
using wild browse or trees that grow naturally on their farms
(Le Hourou, 1980). They can be considered as new solutions
in that in recent years, there have been signicant movements
of germplasm and increased cultivation of fodder shrubs in
many areas of the world. Moreover, nearly all fodder trees can
be considered to be multipurpose, in that they provide many
benets to the farmer, the farming system, and the environment (Table 1; Shelton, 2005).
This article reviews the role of fodder trees in agroforestry
systems in which trees and crops are deliberately grown in
interacting combinations (Nair et al., 2004). Thus, the many
rangeland or forest systems in which pastoralists rely on wild
fodder trees, or systems in which fodder trees are grown in
monocropped plantations is not reviewed. As in many other
agroforestry systems, fodder trees can interact with adjacent
crops or enterprises; for example, competing for moisture,
doi:10.1016/B978-0-444-52512-3.00023-1
235
236
Table 1
For livestock
Valuable source of high quality, protein-rich forage for subsistence, and commercial production of livestock, including cattle, sheep, goats, rabbits,
poultry, sh, and bees
Able to supply foliage during dry periods when herbaceous species are not productive
Being deep rooted, they are drought tolerant and thus are important components of adaptation strategies to climate change
Living fences, around homesteads and elds
Some species have important medicinal attributes for treating livestock health issues
For farming systems
Source of nitrogen-rich mulch for cropping systems
Enhance the sustainability of farming systems due to fertility enhancement, longevity, soil cover, and control of soil erosion
Timber for trellises and stakes for climbing crops
Source of fruit, vegetables, and medicines
For people and the environment
Opportunity to intensify sustainable agricultural production
Means to stabilize sloping lands against soil erosion, due to their deep-rooting habit and permanent soil cover
Often an important source of timber, rewood, and charcoal, particularly for domestic consumption
Habitat for wildlife
As woody perennials, a sink for CO2 and contributor to climate change mitigation and adaptation
Source of cash income when sold as forage or when seed are marketed
A means to lower water table and to limit rise in salinity
Source: Adapted from Shelton, H.M., 2005. Forage tree legume perspectives. In: Reynolds, S.G., Frame, J. (Eds.), Grasslands: Development Opportunities Perspectives. Boca Raton,
FL: Science Publishers, pp. 81108.
Table 2
Species
Countries planteda
Altitude
range (m)
Mean annual
rainfall
(mm)
Frost
toleranceb
Tolerance to
poor
drainageb
Tolerance to
acidityb
Feed
qualityc
Acacia angustissima
Calliandra
calothyrsus
02600
02200
9002800
4800
M
NT
NT
NT
T
M
M
M
15003000
6001600
NT
NT
180930
01600
10004000
6003500
NT
NT
NT
NT
T
M
H
H
o2000
15003500
NT
NT
NT
01900
6501500
NT
NT
NT
10002000
7002000
04000
5002000
10001800
2502500
M
NT
T
NT
M
M
NT
M
M
M
H
H
0800
1002500
8004000
4500
NT
M
T
T
NT
T
H
H
Chamaecytisus
palmensis
Cratylia agentea
Gliricidia sepium
Leucaena
diversifolia
Leucaena
leucocephala
Leucaena pallida
Leucaena trichandra
Morus alba
Sesbania grandiora
Sesbania sesban
a
intake of digestible dry matter, presence of antinutritive compounds, and crude protein (Shelton, 2005). Shelton (2005)
reports that only approximately 20 fodder tree legumes are in
signicant use (that is used on large numbers of farms) out of
the several hundred fodder tree legume species regarded as
having potential as a feed source.
There is much debate over whether to use exotic or indigenous species. Indigenous species are widely used in
many farming systems; for example, there are reports of
29 indigenous fodder tree species used by farmers in Dendi
and Jeldu districts, West Shewa Zone, in central Ethiopia
(Kindu et al., 2006), whereas in Burkina Faso, farmers were
found to use 70 tree species for fodder across three land use
systems (Sibiri et al., 2000). Farmers in the Solma area of
Nepal use more than 90 species, subspecies, and land races of
trees for fodder (Thapa et al., 1997). Moreover, they have
considerable knowledge about their qualities. Thorne et al.
(1999) have conrmed that Nepalese farmers' knowledge of
tree fodder quality is quite consistent with the information
that nutritional researchers generate from laboratory analyses.
But scientists and development practitioners make relatively
little use of local species; they tend to draw on the exotics, for
which seed and information is readily available. Certainly,
more research is needed on indigenous species in many
countries to increase the knowledge base for scientists, development practitioners, and farmers. However, it seems to be
common for exotic species to out-yield indigenous ones. For
example, Atta-Krah et al. (1986) reported that a 2-year study of
22 native fodder species in Nigeria was abandoned because
none were nearly as productive as G. sepium or Leucaena
leucocephala.
There is considerable discussion in the literature on ideotypes, that is, characteristics of model trees for maximizing
economic yield in a particular environment for producing
well-dened end products (Smith, 1992; Dickman et al., 1994;
Leakey and Page, 2006). The discussion involves yield/quality
differences between species as well as within species (between
individual trees, progenies, and provenances). Characteristics
of model trees vary by location and environment but some of
the most frequently cited characteristics include:
Easy establishment.
High productivity under repeated cutting, grazing, or
browsing.
Resistance to pests and diseases.
High seed production ability or reliable vegetative
propagation.
High production of good quality forage in terms of protein,
minerals, palatability, and digestibility.
Suitability to different environments (e.g., temperature,
rainfall, soil acidity, drainage, or salinity).
237
238
Fodder Yields
Yields of fodder trees depend on several factors including
variety, soil and light characteristics, tree density, moisture
availability, and harvesting management (e.g., cutting intensity
and frequency) (Chen et al., 1992; Smith, 1992). Little information is available on the yield of fodder trees and most
available data are from experimental rather than farm conditions. Calliandra yields 1.5 kg dry matter per tree per year on
farms in central Kenya, grown in hedges pruned at 0.61 m
height, ve times per year (Patterson et al., 1998; Wambugu
et al., 2011). In Zimbabwe, where many farmers plant in pure
stands, Calliandra yields range from 2.5 to 5.6 t ha1 year1
and A. angustissima, L. leucocephala, and G. sepium produce
more than 3 t ha1 year1 when cut a single time at the end of
the wet season (Hove et al., 2003). In the semiarid areas
around Segou, Mali, G. sepium yields 2 t ha1 year1 and
Pterocarpus spp. yields 0.5 t ha1 year1. Mulberry yields up to
20 t ha1 year1 (dry leaves) in Tanzania and 45 t ha1 year1
(total yield) in Costa Rica (Sanchez, 2000).
In Indonesia, Devandra and Sevilla (2002) reported dry
matter yields of S. grandiora at 215412 g per tree or 9
11 t ha1 and those of G. sepium at 11476 g per tree or 13
27 t ha1. Calliandra yields range from 0.8 to 3.3 kg per tree,
and L. leucocephala, at 15.4 t ha1. Chen et al. (1992) reported
dry weight leaf yields of L. leucocephala in Asia and the Pacic
ranging from 4 to 15 t ha1 year1.
Animal Productivity
The feed value of a forage is a function of its nutrient content
and digestibility, its palatability and the associative effects of
other feeds (Smith, 1992). These factors interact among
themselves and with the health and breed of the animal to
determine the effective feed value of the material.
On average, fodder trees are richer in protein than tropical
grasses, such as Panicum maximum or Pe. purpureum. This is
239
240
Improved livelihoods
By-products:
firewood,
stakes, bee
fodder, and seed
Improved
growth,
health, and
reproduction
Using as
supplement
Enhanced resilience
Reduced
vulnerability
to drought
Planted on
contour to curb
soil erosion
Using as substitute
for concentrate
Food security, income, and livelihoods are grouped together in this diagram but contributing to one does not necessarily
contribute to the other, as when an increase of cash income is taken by the male head of household for his own use.
Figure 1 Principal ways that fodder trees contribute to improved food security, incomes, and livelihoods. Reproduced from Franzel, S., Carsan,
S., Lukuyu, B., Sinja, J., Wambugu, C., 2014. Fodder trees for improving livestock productivity and smallholder livelihoods in Africa. Current
Opinion in Environmental Sustainability 6, 98103.
Table 3
241
Benets of fodder shrubs, other than inceased milk production, according to dairy farmers in two African farming systems
Type of benet
Firewood
Soil fertility improvement
Improvement in animal health
Soil erosion control
Improved creaminess of milk (increase in butter fat)
Fencing
Revenue from sale of seedlings
Stakes
50
48
38
18
18
18
13
9
72
72
5
20
6
76
9
70
Note: Percentages sum to greater than 100 because many farmers mentioned more than one benet.
Source: Reproduced from Franzel, S., Carsan, S., Lukuyu, B., Sinja, J., Wambugu, C., 2014. Fodder trees for improving livestock productivity and smallholder livelihoods in Africa.
Current Opinion in Environmental Sustainability 6, 98103.
erosion control, and improvement in animal health and reproduction) (Franzel and Wambugu, 2007). Few estimates of
the quantities and values of these products and services were
found. In Kenya, hedges combining Napier grass and Calliandra or L. trichandra reduced runoff and soil erosion while not
reducing adjacent maize yields (Angima et al., 2002; Mutegi
et al., 2008). Fodder trees can also help farmers adapt to and
mitigate climate change (Badege et al., 2013). For adaptation,
they are deep rooted, resistant to drought, and maintain high
protein levels during the dry season, when high-quality feed is
scarce (Wambugu et al., 2011). For mitigation, fodder trees
improve livestock productivity, which helps reduce methane
emissions per unit of output and helps reduce carbon emissions by substituting for commercially manufactured concentrates. But no studies were found that explicitly quantify the
contributions of fodder trees to climate change adaptation or
mitigation.
Gender Considerations
There is widespread recognition that women are disadvantaged in the agricultural sector of many developing countries
(World Bank, 2012; Kiptot and Franzel, 2012). This has led to
research and development initiatives to try to redress the imbalance. Some of these initiatives have deliberately targeted
women groups to impart knowledge and technology to them,
to ensure that extension activities address different interest
groups, holding separate meetings for men and women and
training more women extension ofcers, particularly to serve
communities that have strong traditions that prohibit male
extension ofcers from interacting with women farmers. Research on gender and fodder trees has shown that women in
Africa can benet considerably from planting fodder shrubs,
for several reasons (Kiptot and Franzel, 2011). First, women in
many countries are responsible for collecting fodder off the
farm. Growing fodder on farms can thus reduce their time
spent searching for fodder, freeing up labor for attending to
their families or engaging in other productive enterprises.
Second, because women are often cash-constrained, they are
unable to purchase concentrates for feeding their livestock.
Fodder shrubs can provide protein at a much lower cost than
242
Acknowledgment
The authors are grateful for the support of the Consultative
Group on International Agriculture Research (CGIAR) programs, Forests, Trees and Agroforestry and Climate Change,
Agriculture and Food Security.
References
Abadi, A., Lefroy, T., Cooper, D., Hean, R., Davies, C., 2003. Protability of medium
to low rainfall agroforestry in the cropping zone. Publication No. 02. Barton,
Australia: Rural Industries Research and Development Corporation.
Acharya, K., Booth, E., Wambugu, C., et al., 2010. How can systems thinking, social
capital and social network analysis help programmes achieve impact at scale?
Results of a demonstration project in the Kenyan dairy sector. Working Paper
No. 116. Nairobi: World Agroforestry Centre.
Angima, S.D., Stott, D.E., O'Neill, M., Ong, C., Weesies, G.A., 2002. Use of
CalliandraNapier grass contour hedges to control erosion in central Kenya.
Agriculture Ecosystems and Environment 91, 523.
Atta-Krah, A.N., Sumberg, J.E., Reynolds, L., 1986. Leguminous fodder trees in
farming systems. In: Haque, I., Jutzi, S., Weate, P.J. (Eds.), An Overview of
Research at the Humid Zone Programme of ILCA in Southwestern Nigeria. Addis
Ababa: International Livestock Centre for Africa, pp. 307329.
Ayantunde, A.A., Fernndez-Rivera, S., McCrabb, G. (Eds.), 2005. Coping with feed
scarcity in smallholder livestock systems in developing countries. Nairobi:
International Livestock Research Institute.
Aye, P.A., Adegun, M.K., 2010. Digestibility and growth in West African dwarf sheep
fed gliciridia based multinutrient block supplements. Agricultural and Biology
Journal of North America 1 (6), 11331139.
Badege, B., Neufeldt, H., Mowo, J., et al., 2013. Farmers' strategies for adapting to
and mitigating climate variability and change through agroforestry in Ethiopia and
Kenya. Corvallis: Oregon State University.
Boffa, J., 1999. Agroforestry parklands in sub-Saharan Africa. FAO Conservation
Guide No. 34. Rome: FAO.
Bosma, R.H., Roothaert, R.L., Asis, P., et al., 2003. Financial and social benets of
new forage technologies in Mindanao, Philippines and Tuyen Quang, Vietnam.
CIAT Working Document No. 191. Los Banos, Philippines: CIAT.
Chen, C.P., Halim, R.A., Chin, F.Y., 1992. Fodder trees and fodder shrubs in
range and farming systems of the Asian and Pacic region. In: Speedy, A.,
Pugliese, J. (Eds.), Legume Trees and Other Fodder Trees as Protein
Sources for Livestock. Animal Production and Health Paper 102. Rome: FAO,
pp. 1125.
Chriyaa, A., 2005. The use of shrubs in livestock feeding in low rainfall areas. In:
UNESCO (Ed.), Land Use, Land Cover and Soil Sciences, Volume 5.
Encyclopedia of Life Support Systems. Oxford, UK: UNESCO and Eolss
Publishers.
Devandra, C., Sevilla, C.C., 2002. Availability and use of feed resources in cropanimal systems in Asia. Agroforestry Systems 71, 5973.
Dickman, D.I., Gold, M.A., Flore, J.A., 1994. Ideotype and genetic improvement of
tree crops. Plant Breeding Reviews 9, 163189.
FAO, 2001. Livestock Geography: An Introductory Atlas of Animal Resources. Rome:
FAO.
Franzel, S., Wambugu, C., 2007. The uptake of fodder shrubs among smallholders
in East Africa: Key elements that facilitate widespread adoption. In: Hare, M.D.,
Wongpichet, K. (Eds.), Forages: A Pathway to Prosperity for Smallholder
Farmers. Proceedings of an International Symposium, pp. 203222. Ubon
Ratchathani, Thailand: Ubon Ratchathani University.
Franzel, S., Wambugu, C., Nanok, T., et al., 2007. The production and marketing of
leaf meal from fodder shrubs in Tanga, Tanzania. A Pro-Poor Enterprise for
Muinga, R.W., Thorpe, W., Topps, J.H., 1992. Voluntary food intake, live-weight
change and lactation performance of crossbred cows given ad libitum
Pennisetum purpureum (Napier grass var. Bana) supplemented with
leucaena forage in the lowland and semi-humid tropics. Animal Production 55,
331337.
Murgueitio, E., Calle, Z., Uribe, F., Calle, A., Solorio, B., 2011. Native trees and
shrubs for the productive rehabilitation of tropical cattle ranching lands. Forest
Ecology and Management 261, 16541663.
Mutegi, J.K., Mugendi, D.N., Verchot, L., Kung'u, J.B., 2008. Combining napier
grass with leguminous shrubs in contour hedgerows controls soil erosion
without competing with crops. Agroforestry Systems 74, 3749.
Nair, P.K.R., Rao, M.R., Buck, L.E., 2004. New Vistas in Agroforestry. A
Compendium for the 1st World Congress of Agroforestry, 2004. Dordrecht,
Netherlands: Kluwer.
Niang, A.I., Ugeziwe, J., Cooper, P., et al., 1996. Forage potential of 8 woody
species: Intake and growth rates for local young goats in the highland region of
Rwanda. Agroforestry Systems 34 (2), 171178.
Njuki, J., Kaaria, S., Chamunorwa, A., Chiuri, W., 2011. Linking smallholder farmers
to markets, gender and intra-household dynamics: Does the choice of commodity
matter? European Journal of Development Research 23, 426443.
Nyaata, O.Z., O'Neil, M.K., Roothaert, R.L., 1998. Comparison of Leucaena
leucocephala with Calliandra calothyrsus in napier (Pennisetumpurpureum) fodder
banks. Shelton, H.M., Gutteridge, R.C., Mullen, B.F., Bray, R. (Eds.), Leucaenaadaptation Quality and Farming Systems. Proceedings of a Workshop held in
Hanoi, Vietnam, 914 February. ACIAR Proceedings 86, 257260. Canberra:
Australian Centre for International Agricultural Research.
Paterson, R.T., Karanja, G.M., Roothaert, R., Nyaata, Z., Kariuki, I.W., 1998. A review
of tree fodder production and utilization within smallholder agroforestry systems
in Kenya. Agroforestry Systems 41, 8199.
Paterson, R.T., Kiruiro, E., Arimi, H., 1999. Calliandra calothyrsus as a supplement
for milk production in the Kenya highlands. Tropical Animal Health and
Production 31, 115126.
Piggin, C., 2007. The role of Leucaena in swidden cropping and livestock
production in Nusa Tenggara Timur, Indonesia. In: Cairns, M. (Ed.), Voices From
the Forest: Integrating Indigenous Knowledge into Sustainable Upland Farming.
Washington, DC: Resources for the Future.
Place, F., Roothaert, R., Maina, L., et al., 2009. The Impact of Fodder Shrubs on
Milk Production and Income among Smallholder Dairy Farmers in East Africa
and the Role of Research Undertaken by the World Agroforestry Centre.
Occasional Paper 12. Nairobi: World Agroforestry Centre.
Roothaert, R., Franzel, S., 2001. Farmers' preferences and use of local fodder trees
and shrubs in Kenya. Agroforestry Systems 52 (3), 239252.
Roothaert, R., Franzel, S., Muriuki, K., 2003. On-farm evaluation of fodder trees and
shrubs preferred by farmers in central Kenya. Experimental Agriculture 39 (4),
423440.
Sanchez, M.D., 2000. World distribution and utilization of Mulberry. In: Potential for
Animal Feeding 2000 FAO Electronic Conference on Mulberry for Animal
Production. FAO: Rome. Available at: http://www.fao.org/AG/AGa/AGAP/FRG/
Mulberry/home.htm (accessed 02.07.13).
243
Shelton, H.M., 2005. Forage tree legume perspectives. In: Reynolds, S.G., Frame, J.
(Eds.), Grasslands: Development Opportunities Perspectives. Boca Raton, FL:
Science Publishers, pp. 81108.
Sibiri, J.O., KyDembele, C., Nianogo, A.J., 2000. Les espces fourragres forestires
dans les systmes de production au Burkina Faso: Prfreces et critres de choix
des paysans. In: Gintzburger, G., Bounejmate, M., Agola, C., Mossi, K. (Eds.),
Production and Utilization of Multi-purpose fodder shrubs and trees in West
Asia, North Africa and the Sahel. Aleppo, Syria: ICARDA and ILRI, pp. 2336.
Smith, O.B., 1992. Fodder trees and shrubs in range and farming systems in
tropical humid Africa. In: Speedy, A., Pugliese, J. (Eds.), Legume Trees and
Other Fodder Trees as Protein Sources for Livestock. Rome: FAO. Animal
Production and Health Paper 102.
Sonaiya, E.B., Swan, S.E.J., 2004. Poultry Production: Technical Guide. Rome: FAO.
Stewart, J.L., Allison, G.E., Simons, A.J. (Eds.), 1996. Gliricidia sepium: Gene
resources for farmers. Tropical Forestry Paper No. 33. Oxford: Oxford Forestry
Institute.
Swinkels, R., 1994. Cost comparison of two establishment methods of Calliandra on
farms in western Kenya. In: Atta-Krah, K. (Ed.), Agroforestry in the Highlands of
Eastern Africa. Summary Proceedings of AFRENA Workshop. Nairobi: ICRAF,
pp. 8794.
Thapa, B., Walker, D.H., Sinclair, F., 1997. Indigenous knowledge of the feeding
value of tree fodder. Animal Feed Science Technology 67, 97114.
Thorne, P.J., Subba, D.B., Walker, D.H., et al., 1999. The basis of indigenous
knowledge of tree fodder quality and its implications for improving the use of
tree fodder in developing countries. Animal Feed Science and Technology 81,
119131.
Tuwei, P.K., Kang'ara, J.N.N., Mueller-Harvey, I., et al., 2003. Factors affecting
biomass production and nutritive value of Calliandra calothyrsus leaf as fodder
for ruminants. Journal of Agricultural Science 141 (1), 113127.
Wambugu, C., Franzel, S., Cordero, J., Stewart, J., 2006. Fodder Shrubs for Dairy
Farmers in East Africa: Making Extension Decisions and Putting them into
Practice. Nairobi: World Agroforestry Centre and Oxford Forestry Institute.
Wambugu, C., Place, F., Franzel, S., 2011. Research, development and scaling up
the adoption of fodder shrub innovations in East Africa. International Journal of
Agricultural Sustainability 9 (1), 100109.
World Bank, 2012. World Development Report: Gender Equality and Development.
Washington, DC: The World Bank.
Relevant Websites
www.feedipedia.org
Feedipedia: Animal Feed Resources Information System.
http://192.156.137.110/ssafeed/
Sub-Saharan Africa Feed Composition Database.
www.tropicalforages.info
Tropical Forages: An Interactive Selection Tool.
Glossary
Competition Occurs when trees exploit the same
resources as crops.
Complementarity Occurs when trees acquire resources
that crops cannot acquire.
Hydraulic lift Upward transfer of water through roots
from wetter soil at depth to surface horizons.
Leang phenology Seasonal trend in leaf ushing and leaf
drop.
Introduction
In addition to their social and economic value, forests and
agroforestry (AF) have been widely promoted as a viable solution to overcome the loss of ecosystem functions associated
with the conversion of natural landscapes for human use (Jose,
2009). AF systems vary in the density and conguration of
trees in farming landscapes from a few scattered trees or line
plantings to dense and complex agroforests. However, the relationship between tree cover and water supply is not
straightforward and forest/agriculture policies are often at
odds with scientic understanding. In the tropics, forest/
farming and water policies were often based on the assumption that tree-covered landscapes are the most appropriate way
to maximize water yield, regulate seasonal ows, and ensure
high water quality under all hydrological and ecological situations (Calder et al., 2007). According to this assumption,
conserving or extending tree cover in upstream watersheds is
the most effective way to enhance water availability for agricultural, industrial, and domestic use and prevent oods in
downstream areas. Various national agencies, often with
international cofunding, are spending vast sums of money on
tree planting and soil conservation efforts based on the belief
that more trees mean more water.
However, forest hydrology research in the 1980s and
1990s suggests a different picture and has implications for AF.
Although the important role of upstream forest cover in ensuring the delivery of high-quality water has been conrmed,
earlier assumptions regarding its benets in terms of providing more temporally dispersed downstream seasonal and
annual ows were generally overestimated (Bruijnzeel, 2004).
Furthermore, in arid and semiarid ecosystems, forests and
savannah woodlands do not provide the best land cover to
increase downstream water yield. It is now recognized that
the protective role of forest cover in regulating extreme ow
in tropical ecosystems has been overestimated, particularly in
244
doi:10.1016/B978-0-444-52512-3.00028-0
245
246
247
248
Leaf cover
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
Ju
Au l
g
Se
p
O
c
N t
ov
D
ec
Ja
n
Fe
b
M
ar
Ap
M r
ay
Ju
n
Ju
l
2002
2001
(a)
3
Figure 2 Inuence of root pruning on one side of the Grevillea
robusta tree row 2 years previously (far side of the tree row) on the
growth of maize in Western Kenya. Note that growth was greatly
reduced by competition for below-ground resources on the unpruned
side of the tree row (foreground).
Leaf flush
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
Ju
Au l
g
Se
p
O
ct
N
ov
D
ec
Ja
n
Fe
b
M
ar
Ap
M r
ay
Ju
n
Ju
l
0
2001
(b)
2002
Leaf fall
-1
(c)
2001
G. robusta
2002
A. acuminata
P. fortunei
Figure 1 Time courses for (a) leaf cover, (b) leaf ush, and (c) leaf
fall in Grevillea robusta, A. acuminata, and Paulownia fortunei trees at
Thika, Kenya, between January 2001 and July 2001. Adapted from
Muthuri, C.W., Ong, C.K., Mati, B.M., van Noordwijk, M., 2005.
Modeling the effects of leang phenology on growth and water use by
selected agroforestry tree species in semi-arid Kenya. Land and Water
Resources Research 4, 111. Vertical bars show double standard
errors of the mean. Scores were ascribed using a four-point scale
ranging from 0 (absent), 1 (low), 2 (intermediate) to 3 (high).
249
1.2
Unpruned
Root pruned
1.0
0.8
0.6
0.4
0.2
0.0
10
12
14
16
18
20
22
Time (h)
(a)
Unpruned
10
Root pruned
Shoot pruned
7
6
5
4
3
2
1
0
(b)
Alnus
Calliandra
Sesbania
Figure 3 (a) Diurnal time courses of sap ow in unpruned and root-pruned Grevillea robusta trees shortly after root pruning was completed;
vertical bar shows standard error of the difference (SED) (Anyango, 2005) and (b) inuence of tree species and pruning treatment on mean daily
sap ow rates for A. acuminata, C. calothyrsus, and S. sesban; vertical bars 1, 2, and 3 show SED values for species, pruning treatment, and treepruning treatment interaction. Denotes signicance at po.001 (Siriri, 2013).
250
1200
250
First season LR 1999
Casuarina equisetifolia
1000
200
800
150
600
400
Sap flow g h1
100
50
0
250
0
1200
Grevillea robusta
1000
Second season SR 1999
800
200
% of crop only plot
200
600
400
150
200
100
0
0
50
10 12 14 16 18 20 22 24
Time of day
Root pruned
Control (unpruned)
0
250
Shoot
Crown pruned
Crown + root pruned
Root
Casuarina equisetifolia
Grevillea robusta
Eucalyptus camaldulensis
Markhamia lutea
Conclusions
This article shows that trees may have both benecial and
detrimental hydrological impacts at farm and watershed levels.
Temporal complementarity in the use of rainfall occurs if
residual water is available after the crop is harvested or rainfall
occurs when there is no scope for cropping. The most
remarkable example of temporal complementarity in water
use is the unusual phenology of the Sahelian tree, F. albida,
which is leafy during the dry season and sheds its leaves during
the rainy season. Improved soil water and nutrient status has
been reported under mature tree canopies in the savanna areas
of Africa, Central America, and North America. In theory, trees
can enhance soil water content beneath their canopies if the
water saved through decreases in soil evaporation caused by
shade and reduced runoff exceeds the quantity of water removed by their root systems. Hydraulic lift by tree roots may
also redistribute water from moist zones deep in the soil
prole to the surface horizons. However, spatial complementarity in water use is rare as tree and crop roots often
exploit the same surface soil horizons and rainfall seldom
recharges horizons below the crop rooting zone, although
there is clear evidence of spatial complementarity when
groundwater is accessible to tree roots.
Containing competition for water, nutrients, and light between trees and crops in AF systems remains a major challenge
in the semiarid tropics, especially in the search for an
acceptable substitute for eucalyptus. In Southern Australia, the
greatest challenge is to nd tree species that provide valuable
products and improve the poor drainage, which is responsible
for inducing salinity in millions of hectares of protable farm
land, with minimal loss of crop yield.
Finally, there is an urgent need to consider the impact of
climate change on water use by trees, which has received surprisingly little attention. Previous studies of watershed functions of forests and AF systems have focused on reward schemes
to upstream communities for providing environmental services
to downstream users, whereas Clean Development Mechanism
schemes in Africa have focused chiey on global benet. Rewards may well be an efcient and fair way of investing international funds in climate-change adaptation, which will have
profound hydrological impacts on AF at both local and global
scales (van Noordwijk et al., 2011).
References
Anyango, S.O., 2005. Sustainability of dryland agroforestry systems in Eastern
Kenya: Farmers perceptions, physiological factors and landscape patterns. PhD
Thesis, Kenyatta University, Nairobi, Kenya.
251
Asaah, E.K., Tchoundjeu, Z., Wanduku, T.N., Van Damme, P., 2010. Understanding
root systems of 5 year old African plum of seed and vegetative origins
(Dacryodes edulis (G.Don) H.J. Lam). Trees; Structure and Function 24,
789796.
Asaah, E.K., Wanduku, T.N., Tchoundjeu, Z., 2012. Does propagation affect the ne
root architecture of African plum (Dacryodes edulis)? Trees; Structure and
Function 26, 14611469.
Bayala, J., Heng, L.K., van Noordwijk, M., Ouedraogo, S.J., 2008. Hydraulic lift
study in two native tree species of agroforestry parklands of West African dry
savanna. Acta Oecologia 34, 370378.
Black, C.R., Ong, C.K., 2000. Utilisation of light and water in tropical agriculture.
Agricultural and Forest Meteorology 104, 2547.
Broadhead, J.S., Ong, C.K., Black, C.R., 2003a. Tree phenology and soil water
in semi-arid agroforestry systems. Forest Ecology and Management 180,
6173.
Broadhead, J.S., Black, C.R., Ong, C.K., 2003b. Tree leang phenology and
crop growth in semi-arid agroforestry systems. Agroforestry Systems 58,
137148.
Brooksbank, K., White, D.A., Veneklaas, E.J., Carter, J.L., 2011a. Hydraulic
redistribution in Eucalyptus kochii subsp. borealis with variable access to fresh
groundwater. Trees 25, 735744.
Brooksbank, K., Veneklaas, E.J., White, D.A., Carter, J.L., 2011b. The fate of
hydraulically redistributed water in a semi-arid zone eucalyptus species. Tree
Physiology 31, 649658.
Brooksbank, K., Veneklaas, E.J., White, D.A., Carter, J.L., 2011c. Water availability
determines hydrological impact of tree belts in dryland cropping systems.
Agricultural Water Management 100, 7683.
Bruijnzeel, L.A., 2004. Hydrological functions of tropical forests: Not seeing the soil
for the trees? Agriculture, Ecosystems and Environment 104, 185228.
Calder, I., Hofer, T., Vermont, S., Warren, P., 2007. Towards a new understanding of
forests and water. Unasylva 229, 310.
Caldwell, M.M., Dawson, T.E., Richards, J.H., 1998. Hydraulic lift: Consequences of
water efux for roots of plants. Oecologia 113, 151161.
Cannell, M.G.R., van Noordwijk, M., Ong, C.K., 1996. The central hypothesis: The
tree must acquire resources that the crop would not otherwise acquire.
Agroforestry Systems 33, 2731.
Chirwa, P.W., Black, C.R., Ong, C.K., Maghembe, J.L., 2003. Tree and crop
productivity in Gliricidia/maize/pigeonpea-based cropping systems in southern
Malawi. Agroforestry Systems 59, 265277.
Chirwa, P.W., Black, C.R., Ong, C.K., Maghembe, J.L., 2006. Nitrogen dynamics in
a Gliricidia sepium/pigeonpea/maize mixed cropping system in southern Malawi.
Agroforestry Systems 67, 93106.
FAO and CIFOR, 2005. Forests and Floods: Drowning in Fiction or Thriving on
Facts? RAP Publication 2005/03. Bangkok, Thailand: FAO Regional Ofce for
Asia and the Pacic.
Garrity, D.P., Akinnifesi, F.K., Ajayi, C., et al., 2010. Evergreen agriculture:
A robust approach to sustainable food security in Africa. Food Security 2,
197214.
Ikerra, S.T., Maghembe, J.A., Smithson, P.C., Buresh, R.J., 1999. Soil nitrogen
dynamics and relationships with maize yields in a Gliricidiamaize intercrop in
Malawi. Plant and Soil 211, 155164.
Itimu, O.A., 1997. Nitrogen dynamics and root distribution of Gliricidia sepium and
Senna spectabilis in maize (Zea mays)-based alley cropping systems in Malawi.
PhD Thesis, Wye College, University of London, Kent, UK.
Jackson, N.A., Wallace, J.S., Ong, C.K., 2000. Tree pruning as a means of
controlling water use in an agroforestry system in Kenya. Forest Ecology and
Management 126, 133148.
Jose, S., 2009. Agroforestry for ecosystem services and environmental benets.
Agroforestry Systems 76, 110.
Kho, R., Yacouba, B., Yaye, M., et al., 2001. Separating the effects of trees on
crops: The case of Faidherbia albida and millet in Niger. Agroforestry Systems
52, 219238.
Kizito, F., Dragila, M.I., Sen, M., et al., 2012. Hydraulic redistribution by two semiarid shrub species: Implications for Sahelian agro-ecosystems. Journal of Arid
Environments 83, 6977.
Lefroy, E.C., Stirzaker, R.J., 1999. Agroforestry for water management in the
cropping zone of southern Australia. Agroforestry Systems 45, 277302.
Lott, J.E., Howard, S.B., Black, C.R., Ong, C.K., 2000a. Long term productivity of a
Grevillea robusta-based agroforestry system in Kenya. I. Tree growth. Forest
Ecology and Management 139, 175186.
Lott, J.E., Howard, S.B., Black, C.R., Ong, C.K., 2000b. Long term productivity of a
Grevillea robusta-based agroforestry system in Kenya II. Crop growth and system
productivity. Forest Ecology and Management 139, 187201.
252
Lott, J.E., Ong, C.K., Black, C.R., 2009. Understorey microclimate and crop
performance in a Grevillea robusta-based agroforestry system in semi-arid Kenya.
Agricultural and Forest Meteorology 149, 11401151.
Ludwig, F., Dawson, T.E., Kroon, H., Brendse, F., Prins, H.H.T., 2003. Hydraulic lift
in Acacia tortilis trees on an east African savanna. Oecologia 134, 293300.
Ludwig, F., Dawson, T.E., Prins, H.H.T., Berendse, F., De Kroon, H., 2004. Belowground competition between trees and grasses may overwhelm the facilitative
effects of hydraulic lift. Ecology Letters 7, 623631.
Mulatya, J.M., Wilson, J., Ong, C.K., Deans, J.D., Sprent, J.I., 2002. Root
architecture of provenances, seedlings and cuttings of Melia volkensii:
Implications for crop yield in dryland agroforestry. Agroforestry Systems 56,
6572.
Muthuri, C.W., Ong, C.K., Mati, B.M., van Noordwijk, M., 2005. Modelling the
effects of leang phenology on growth and water use by selected agroforestry
tree species in semi-arid Kenya. Land and Water Resources Research 4, 111.
Namirembe, S., Brook, R.M., Ong, C.K., 2009. Manipulating phenology and water
relations in Senna spectabilis in a water limited environment in Kenya.
Agroforestry Systems 75, 197210.
van Noordwijk, M., Farida, Saipothong, P., et al., 2006. Watershed functions in
productive agricultural landscapes with trees. In: Garrity, D., Okono, A., Grayson,
M., Parrot, S. (Eds.), World Agroforestry into the Future. Nairobi: World
Agroforestry Centre, pp. 103112.
van Noordwijk, M., Haong, M.H., Neufeldt, H., Oborn, I., Yatich, T., 2011. How
Trees and People Can Co-adapt to Climate Change: Reducing Vulnerability in
Multifunctional Landscapes. Nairobi, Kenya: World Agroforestry Centre.
van Noordwijk, M., Luisana, B., 2000. WaNulCAS Version 2.0. Background on a
Model of Water, Nutrient and Light Capture in Agroforestry Systems. Bogor,
Indonesia: World Agroforestry Centre (ICRAF).
Okogun, J.K., Sanginga, N., Mulongoy, K., 2000. Nitrogen contribution of ve
leguminous trees and shrubs to alley cropped maize in Ibadan, Nigeria.
Agroforestry Systems 50, 123136.
Ong, C.K., 2003. The Eucalyptus dilemma: Friend or foe? Presented at RELMA-Sida
workshop: Eucalyptus Dilemma Forum, Nairobi, Kenya, 5 June 2003.
Ong, C.K., Black, C.R., Muthuri, C.W., 2006. Modifying forests and agroforestry for
improved water productivity in the semi-arid tropics. CAB Reviews: Perspectives
in Agriculture, Veterinary Science, Nutrition and Natural Resources 65, 119.
Ong, C.K., Leakey, R.R.B., 1999. Why treecrop interactions in agroforestry appear
at odds with treegrass interactions in tropical savannahs. Agroforestry Systems
45, 109129.
Ong, C.K., Wilson, J., Deans, J.D., et al., 2002. Treecrop interactions:
Manipulation of water use and root function. Agricultural and Water Management
53, 171186.
Phombeya, H.K., 1999. Farmers perceptions of the value of Faidherbia albida trees
in the farming system (Survey). In: Nutrient Sourcing and Recycling by
Faidherbia albida Trees in Malawi. PhD Thesis, Wye College, University of
London, UK.
Poschen, P., 1986. An evaluation of Acacia albida-based agroforestry practices in
the Haraghe highlands of Ethiopia. Agroforestry Systems 4, 3156.
Rao, M.R., Schroth, G., Williams, S.E., et al., 2004. Managing below-ground
interactions in agroecosystems. In: van Noordwijk, M., Cadisch, G., Ong, C.K.
(Eds.), Below-Ground Interactions in Tropical Agroecosystems: Concepts and
Models with Multiple Plant Components. Wallingford, UK: CABI Publishing,
pp. 309328.
Reij, C., Tappan, C., Smale, M., 2009. Agroenvironmental transformation in the
Sahel: Another kind of green revolution. IFPRI Discussion Paper 00914,
Washington DC.
Rhoades, C., 1995. Seasonal pattern of nitrogen mineralization and soil moisture
beneath Faidherbia albida (syn Acacia albida) in central Malawi. Agroforestry
Systems 29, 133145.
Richards, J.H., Caldwell, M.M., 1987. Hydraulic lift: Substantial nocturnal water
transport between layers by Artemisia tridentata roots. Oecologia 73, 486489.
Rockstrom, J., Lannerstad, M., Falkenmark, M., 2007. Assessing the water challenge
for a new green revolution in developing countries. Proceedings of the National
Academy of Sciences of the United States of America 104, 62536260.
Roupsard, O., Ferhi, A., Granier, A., et al., 1999. Reverse phenology and dry-season
water uptake by Faidherbia albida (Del.) A. Chev. in an agroforestry parkland of
Sudanese west Africa. Functional Ecology 13, 460472.
Rowe, E.C., Hairiah, K., Giller, K.E., van Noordwijk, M., Cadisch, G., 1999. Testing
the safety net role of hedgerow tree roots by 15N placement at different soil
depths. Agroforestry Systems 43, 8193.
Schroth, G., 1998. A review of below-ground interactions in agroforestry, focussing
on mechanisms and management options. Agroforestry Systems 43, 534.
Siriri, D., Ong, C.K., Wilson, J., Boffa, J.M., Black, C.R., 2010. Tree species and
pruning regime affect crop yield on bench terraces in SW Uganda. Agroforestry
Systems 78, 6577.
Siriri, D., Tenywa, M.M., Ong, C.K., Black, C.R., Bekunda, M., 2006. Water
inltration, conductivity and runoff under fallow agroforestry on sloping terraces.
African Crop Science Journal 14, 5971.
Siriri, D., Wilson, J., Coe, R., et al., 2012. Water storage and soil evaporation under
agroforestry systems and sole crops on bench terraces in SW Uganda.
Agroforestry Systems 87, 4558.
Siriri, D., Wilson, J., Coe, R., et al., 2013. Trees improve water storage and reduce
soil evaporation in agroforestry systems on bench terraces in SW Uganda.
Agroforestry Systems 87, 4558.
Smith, D.M., Jarvis, P.G., Odongo, J.C.W., 1997. Sources of water used by trees
and millet in Sahelian windbreak systems. Journal of Hydrology 198, 140153.
Spracklen, D.V., Arnold, S.R., Taylor, C.M., 2012. Observations of increased tropical
rainfall preceded by air passage over forest. Nature 489, 282286.
Stone, E.L., Kalisz, P.J., 1991. On the maximum extent of tree roots. Forest Ecology
and Management 46, 59102.
Tefera, A.T., 2003. Crown and root pruning of four year old boundary trees at Siaya
and Nyabeda in Western Kenya: Socioeconomics, utilization of soil water, and
maize and wood yields. PhD Thesis, University of Sokoine, Tanzania.
Wajja-Musukwe, T.-N., Wilson, J., Sprent, J.I., et al., 2008. Tree growth and
management in Ugandan agroforestry systems: Effects of root pruning on tree
growth and crop yield. Tree Physiology 28, 233242.
Wallace, J.S., Jackson, N.A., Ong, C.K., 1999. Modelling soil evaporation in an
agroforestry system in Kenya. Agricultural and Forest Meteorology 94, 189202.
Young, A., 1997. Agroforestry for Soil Conservation, 2nd edn. Wallingford, UK: CAB
International 320 p.
Relevant Websites
http://siteresources.worldbank.org/INTCARBONFINANCE/Resources/57853A_BioCarbon_LOW-RES.pdf
BioCarbon Fund, World Bank.
www.worldagroforestrycentre.org
World Agroforestry Centre.
Glossary
Apical dominance The process which regulates branching
in plants.
Circa situ conservation It is conservation through wise
use.
Introduction
The domestication of agroforestry trees is a technique for the
intensication of agroforestry as a low-input farming system
delivering multifunctional agriculture for the relief of poverty,
malnutrition, hunger, and environmental degradation in tropical and subtropical countries (Leakey, 2010, 2012a).
In the past, tree products were gathered from natural forests
and woodlands to meet the everyday needs of people living a
subsistence lifestyle. With the advent of the Industrial Revolution and, more recently, the intensive modern farming systems of the Green Revolution, the resource of these trees has
declined. This has been due to increased population pressures
for agricultural land and the escalation of deforestation. To rebuild and improve this useful resource, the concept of tree
domestication for agroforestry was proposed in 1992 (Leakey
and Newton, 1994) and subsequently implemented by the
World Agroforestry Centre (International Centre for Research in
Agroforestry (ICRAF)) as a global initiative from 1994 (Simons,
1996). Great progress has been made in the rst two decades of
this initiative (Leakey et al., 2005, 2012; Tchoundjeu et al.,
2006, 2008), which have encouraged local entrepreneurship in
the processing and marketing of agroforestry tree products
(AFTPs). This has had benecial impacts on farmers' livelihoods
(Tchoundjeu et al., 2010).
Strategy
Domestication through cultivar development relies on three
processes: selection, testing, and breeding. Selection identies
certain genotypes for cultivar development, testing exposes the
new cultivars to appropriate environments, and breeding creates new genetic variability.
As in animals, plant domestication is a continuous process
that, in crops like wheat, rice, maize, oranges, and apples,
started thousands of years ago and continues today. In trees,
two basic approaches are used to effect genetic improvement:
the seed-based breeding approach typical of forestry and the
clonal approach typical of horticulture, but the domestication
strategies are not dissimilar. In agroforestry, Leakey and
Akinnifesi (2008) have suggested a strategy based on the establishment of three interlinked tree populations (Figure 1):
Gene resource population.
Selection population.
Production population.
The gene resource population is basically the wild population from which new selections can be derived. The selection
population is the collection of selected provenances, progenies, or individual trees which are being tested and used to
develop clonal cultivars or integrated within breeding programs to create the next generation of breeding stock. A wide
range of genotypes may be kept in this population as long as
each one has at least one characteristic of possible future
interest. The production population consists of the highly selected clones, progenies, or provenances which are currently
being planted by farmers.
In their strategy paper, Leakey and Akinnifesi (2008) specically highlighted the development of a clonal approach to
the domestication of high value trees, particularly the traditionally important indigenous fruits and nuts. However, the
key element of the tree population strategy is equally applicable to less valuable tree species grown for their environmental
services and propagated by seed. It is important to remember
that the practice of domesticating a species is cyclical and thus
continuous. For this reason, commercial plantings have to be
made with whatever material is best at a given time, knowing
that they will be superseded later.
The strategy being implemented by ICRAF and others to
domesticate high-value indigenous trees for agroforestry, such
as those producing marketable fruits and nuts, is based on
participatory processes involving local communities. A participatory tree domestication strategy involves the consultation
with and participation of farmers to (1) determine their priority species for domestication (Franzel et al., 1996, 2008) (2)
make an inventory of the natural resource, (3) implement a
program of genetic selection and mass propagation aimed at
the sustainable production of AFTPs for food, tree fodder,
medicinals and nutriceuticals, timber, wood and bers, etc.,
and (4) sell and trade the products in local traditional and new
emerging markets further aeld. Such strategies also recognize
the importance of the wise use and conservation of genetic
resources; the reduction of deforestation and restoration of
degraded land. Participatory approaches have numerous advantages (Leakey et al., 2003) such as building on tradition
and culture and promoting rapid adoption by growers to enhance livelihoods and environmental benets (Simons and
Leakey, 2004). This participatory approach to domestication,
therefore, differs from the more common scientic approach
that has typically been implemented to develop most food
crops. Therefore these approaches can be thought of as the
farm and the research station pathways to domestication. In
doi:10.1016/B978-0-444-52512-3.00025-5
253
254
Agroforestry
context
Nonclonal
techniques
Domestication
strategy
Clonal
techniques
Strategy for
vegetative
propagation
Juvenile vs mature
Choice of techniques
Low tech vs high tech
Stockplant
management
Gene resource
population
Genetic diversity
Indigenous knowledge
Ideotypes
Predictive test
Selection population
(field trials)
Wild trees
Initial screening
Candidacy testing
Unproven trees
----------------
Clonal performance
Compatability trials
Proven trees
Gene banks
Breeding
In situ conservation
Ex situ conservation
Circa situ
conservation
Production
population
Agroforestry
practices
Figure 1 The agroforestry tree Domestication Strategy and the relationships between a Genetic Resources Strategy and the Strategies for
Vegetative Propagation and Clonal Selection. Reproduced from Leakey, R.R.B., Akinnifesi, F.K., 2008. Towards a domestication strategy for
indigenous fruit trees in the tropics. In: Akinnifesi, F.K., Leakey, R.R.B., Ajayi, O.C., et al. (Eds.), Indigenous Fruit Trees in the Tropics:
Domestication, Utilization and Commercialization. Wallingford, UK: CAB International, pp. 2849.
255
1. Improvement
through management
on farms
2. Major genetic
improvements
through science
Phase 1
Selection by farmers
For domestic use
For fulfilment of welfare needs
For low input farming (low investment)
For specific agroforestry systems
For local markets
Selection and
breeding research to improve
Phase 2
Participatory
domestication with
farmers
Domestication for
commercial markets
Agroforests
Figure 2 Tree domestication pathways. Reproduced from Leakey, R.R.B., Akinnifesi, F.K., 2008. Towards a domestication strategy for indigenous
fruit trees in the tropics. In: Akinnifesi, F.K., Leakey, R.R.B., Ajayi, O.C., et al. (Eds.), Indigenous Fruit Trees in the Tropics: Domestication,
Utilization and Commercialization. Wallingford, UK: CAB International, pp. 2849.
256
Years to
first
fruiting
15
15
Step 1
257
Higher crop
yields and
some food
security
Step 2
Diversified
agroecosystem
Income
Improved tree
products
Improved
nutrition
and health
Food security
and domestic
self sufficiency
Step 3
Product
processing
Employment
Income
Entrepreneurism
Value-adding
Trade
Empowerment
Market chain
development
Gender equity
Improved
infrastructure
Education
Figure 4 The delivery of multifunctional agriculture by three agroforestry steps. Step 1. Land rehabilitation with leguminous trees and shrubs,
Step 2. Domestication with indigenous trees producing marketable products, and Step 3. Marketing, processing, and value-adding indigenous tree
products (see Table 1). Modied from Asaah, E.K., Tchoundjeu, Z., Leakey, R.R.B., et al., 2011. Trees, agroforestry and multifunctional agriculture
in Cameroon. International Journal of Agricultural Sustainability 9, 110119.
different species will probably ll different spatial and temporal niches in the landscape and be planted in different
congurations and densities within farming systems. This is all
part of the diversication of the agroecosystem which is an
important component of enhancing agroecosystem functions
for the rehabilitation of degraded farmland (Leakey, 1999a,
2012b).
The domestication of indigenous trees producing highvalue products, such as traditional foods and medicines, is one
component of a novel strategy for the intensication (Leakey,
2012a) and diversication (Leakey, 2010) of smallholder
farming systems in the tropics and subtropics through agroforestry. In environmental terms, the diversication with longlived perennial plants is important because it is the way to
rebuild the ecological functions of agroecosystems and landscapes. Soil and land rehabilitation is crucial if agriculture is to
use land already cleared of forest rather than abandoning it
and cutting down more forest (Leakey, 2012b).
258
experience of the past 1015 years indicates that the rst income stream from agroforestry projects is derived from the
sales of plants from village nurseries to neighboring communities, especially the sale of seedlings of nitrogen-xing or
the so-called fertilizer trees (Asaah et al., 2011; Leakey and
Asaah, 2013). This is because the loss of soil fertility due to
frequent cropping without access to articial fertilizers is recognized as one of the main constraints to agricultural production. In addition, the benet ow from these trees is
obtained relatively quickly (13 years). However, it generally
takes longer to obtain returns from the production of AFTPs.
The strategy for increased income generation from AFTPs is,
in the rst instance, to build local markets and trade. This is
particularly important in the case of traditional foods and
medicines as local people are familiar with the use of these
products and the demand typically exceeds supply. In the
longer term, however, some of these products may have regional and even international markets, rstly with expatriates
from tropical countries living in Europe and America, and then
as products become more widely known or better processed
with global customers.
A secondary reason for focusing on local and regional rather than international markets is that if the demand expands
too fast there is a risk that large-scale entrepreneurs may enter
the marketplace and outcompete local business people (Leakey and Izac, 1996) thus, undermining the use of tree domestication as a development strategy. Having said that there
are a few interesting and potentially very important initiatives
in which multinational companies are becoming engaged with
local communities in tropical countries in PublicPrivate
Partnerships (Leakey, 2012b). These are generally operating in
a way that is contrary to the trend of globalization in which all
the economic benets ow to industrial countries rather than
at least some remaining in the tropical country.
Some tree products, notably fruits, are produced seasonally
and have a very short shelf life. To overcome this constraint to
year-round marketing, it is necessary to investigate opportunities for processing and value adding. This can take many
forms such as drying and airtight packaging; preservation in
oil, brine, or syrup; and freezing, etc. Generally, this involves
the need for a level of scale outside the capacity of a smallholder farmer, although cottage industries can be a possibility. If this approach to extending the marketing season has
to involve industrial companies, then new issues arise. One of
these is to involve the companies in the domestication process
so that traits which are important in the processed product are
included in the genetic selection program (Leakey, 1999b).
Later, issues of trading agreements that also result from the
involvement of processing companies in marketing will be
considered.
An alternative approach to processing can be to seek the
generally rare plants that ower and fruit outside the normal
seasonal pattern and then to develop these as cultivars. Although this can be quite simple to achieve, these out-of-season
plants may not have quality or yield traits that are as good as
those fruiting within the normal season. In this case, developing cultivars which expand the productive season may
need to also involve a breeding program.
As the commercialization process involves more players
and becomes more complex, the risks that the producers will
Product development.
Market development.
Supply chain development.
Institutional development.
259
wild products are highly variable in quality, often with unreliable levels of production. However, the focus on naturally
occurring wild resources is now changing with the recent
emergence of highly compatible propoor participatory domestication technologies for indigenous fruit and nut trees.
This offers great opportunities to improve product quality
through tree selection and cultivar development. Creating
these new crops should also greatly increase the supply of very
marketable produce. Thus, by realizing the importance of
commercialization for domestication and domestication for
commercialization, there is considerable opportunity for
agroforestry to alleviate poverty, malnutrition, and hunger in
marginalized agricultural communities of developing countries. Thus, the symbiotic relationship between domestication
and commercialization is a very important aspect of the
strategy needed to ensure real impact on the big socioeconomic issues affecting the world. The overall outcome of
such developments arising from improved agricultural
production and enhanced livelihoods should, therefore, be
improved access to clean water, better diets, healthcare, education, etc. Just as it is seen above regarding adaptability to
different environmental situations, this model case has great
adaptability to different socioeconomic situations (Leakey,
2012b).
Thus, in conclusion, when the social and commercial
components of the strategy that have been developed for
participatory domestication strategy are added to the agroecosystem benets from the adoption of agroforestry for land
rehabilitation, the emergence of a three-step generic model for
the delivery of a socially and economically desirable multifunctional agriculture by agroforestry can be seen (Figure 4,
Table 1).
Before moving on, however, it is important to recognize that
the trade in some new products will require regulatory approval
for European Union (EU) and American markets. It is, however,
possible to tie the approval of these products to the target
producers, as has been achieved by PhytoTrade Africa's successful application to have Baobab fruit approved as a novel
food ingredient in the EU under Regulation (EC) 258/97 and by
Unilever Deutschland GmbH for Allanblackia seed oil (European Food Security Authority No EFSA-Q-2007-059.
Techniques
Biological Components of the Techniques
Genetic selection
The domestication process is basically about the cultivation of
plants with superior genetic traits. In trees, two techniques can
be used to assist in the identication of superior mature trees
(sometimes called elite or plus trees) producing timber and
wood, indigenous fruits and nuts, or otherwise useful everyday
domestic products. In forestry for timber and wood production, genetic improvement is typically done by selection of
a population with inherent genetic quality (a provenance) and
by making seed collections from that population. Alternatively, when more is known about the genetic quality of
individuals within a population, seeds (a progeny) are typically collected from the best mother tree(s). The same
260
Table 1
Step 1: Adopt agroforestry technologies such as two year Improved fallows or Relay cropping with nitrogen-xing shrubs that improve maize yields
from approximately 1 ton ha1 per hectare up to approximately 45 tons ha1. This allows the farmers to both improve food security and reduce the
area of their holdings planted with maize and thus make space for other crops, perhaps cash crops which would generate income. An additional benet
arising from improved fallows with leguminous shrubs is the reduction of parasitic weeds like Striga hermontica and the reduced incidence of insects
pests like the stem borers of maize.
Step 2: Diversify the farming system by the inclusion of species producing marketable products or fodder for livestock. The adoption of participatory
approaches to the domestication of traditionally important indigenous food plants is a good way to rapidly create new cash crops that generate
income, improve nutritional security through diversied diets, enhance gender equity, provide diversied diets rich in micronutrients, empower
communities toward self-sufciency in products of day-to-day domestic importance, and maintain culture and traditions. The sale of these products
would allow the purchase of fertilizers and thus, potentially, the increase of maize yields up to 10 tons ha1. Consequently, the area under maize could
be reduced further to allow more cash cropping. The integration of fodder trees and livestock into a farm is one of the elements of diversication that
could be part of this step.
Step 3: Promote entrepreneurship and develop value-adding and processing technologies for the new tree crop products, thus increasing availability of
the products throughout the year, expanding trade, and creating employment opportunities. All of these are outputs which should help to reduce the
incidence of poverty and enhance gender equity.
Source: Modied from Leakey, R.R.B., 2010. Agroforestry: A delivery mechanism for multifunctional agriculture. In: Kellimore, L.R. (Ed.), Handbook on Agroforestry: Management
Practices and Environmental Impact. Environmental Science, Engineering and Technology Series. New York, USA: Nova Science Publishers, pp. 461471 and Leakey, R.R.B., 2013.
Addressing the causes of land degradation, food/nutritional insecurity and poverty: A new approach to agricultural intensication in the tropics and sub-tropics. In: Hoffman, U. (Ed.),
UNCTAD Trade and Environment Review 2012. Geneva, Switzerland: UNCTAD. Available at: www.unctad.org/Templates/Page.asp?intItemID=3723&lang=1 (accessed 16.09.12).
Flesh
Kernel
Fruit ideotype:
Nut ideotype:
Big fruit
Small / Av fruit
Flesh = 70%
Kernel = 40%
Small nut
Thin shell
Juicy
Tasty
Nutritious flesh
Nutritious kernel
Nursery management
Good nursery management involves many skills and attention to
detail. The process starts with acquisition of high-quality germplasm of known origin (accession records) and recorded genetic
quality, supported by documents recognizing the rights of the
supplier (Access and Benet Sharing agreements) for example,
see the Agroforestry Tree Genetic Resources Strategy of the World
Agroforestry Centre (ICRAF, 2012). Furthermore this germplasm
must have been appropriately stored and handled to avoid loss
of viability. Germplasm can be of two types: seeds and vegetative
propagules. Seeds also are of two main types: those that can be
stored by drying or freezing (orthodox) and those which cannot
be (recalcitrant). Both the latter and the vegetative propagules are
short lived (from a few days to at most a few weeks). They have
to be very carefully and rapidly handled to avoid water or temperature stress and any physical damage.
Accession records must be stored safely and the origin of
every plant in the nursery must be labeled or in some other
way traceable back to these records. Plants of unknown origin
are of zero importance in a domestication program.
Successful plant production is dependent on rapid germination of seeds and propagation of vegetative propagules
and their subsequent growth in good, free-draining potting
261
262
263
Regional
consumers
International
consumers
Local market
Local markets
Regional
markets
International
markets
Local
traders /
wholesaler
National
processors
Local traders
Exporters
Transport
Bulk collectors
Local
processors
Transport
Local
consumers
Transport
Producer
Local
consumers
Transport
Domestic user
Figure 8 The increasing importance of domestication in the value chain of an agroforestry tree product.
International
processors /
manufacturers
264
Outcomes
To date, studies on the environmental and socioeconomic
impacts of tree domestication have not been based on randomized controlled trials. Nevertheless, comparisons based
on household surveys have indicated that integrated rural
development based on agroforestry, tree domestication, and
local market initiatives with small-scale enterprises have
= Mfoundi (wholesale)
= Mfoundi (retail)
90
60
30
0
30
40
50
60
70
80
90
100
265
Figure 11 Value-added products developed from agroforestry tree species. Reproduced from Leakey, R.R.B., 2012b. Living with the Trees of
Life Towards the Transformation of tropical Agriculture. Wallingford, UK: CABI, 200 pp.
30 000
25 000
5 years
5 000
US$28 350
10 000
US$16 000
15 000
US$145
Income (US$)
10 years
20 000
0
Figure 12 Income generated from plant sales at Rural Resources
Centers in Cameroon after 2, 5, and 10 years. Reproduced from
Leakey, R.R.B., Asaah, E.K., 2013. Underutilised species as the
backbone of multifunctional agriculture The next wave of crop
domestication. Acta Horticulturae 979, 293310.
positive impacts on the lives of farming households in participating communities (Figure 12 and Table 2). Together these
impacts illustrate that agroforestry can deliver what the International Assessment of Agricultural Knowledge, Science and
Technology for Development (IAASTD) called Multifunctional
Agriculture (Table 3). Currently, the impacts are only on a local/
household/farm/village scale and there is much to be done to
upscale and outscale the agroforestry initiatives before the scales
are extended (Table 4).
The major outcome of participatory tree domestication, as expected, is new tree crop cultivars with improved product quality
and greater market demand. This is happening in many places
around the tropics in more than 50 species but is most
advanced in Cameroon, where these cultivars have been
developed by local farmers for cultivation in their own farms to
meet household needs. However, as the supply of product increases, it is expected that both these cultivars and their products
will be sold at rst locally and then more widely (Tchoundjeu
et al., 2010; Asaah et al., 2011; Leakey, 2012b). The cultivation
of these new cash crops is leading to the diversication of
farming systems and this is expected to result in healthier
agroecosystems. Another biological nding with likely impacts
on agroecosystems is that vegetatively propagated trees allocate
their dry matter differently, with less in ne root and more in
primary roots and shoots. Consequently, clonal cultivars are
more likely to be less competitive with annual crops (Asaah,
2012; Asaah et al., 2010, 2012).
266
Table 2
The social, marketing, and natural resource qualities that determine whether or not the impacts of commercializing indigenous fruits,
nuts, and other tree products are positive or negative
Winner qualities
Loser qualities
In product marketing
Commercial opportunities
Diversity of end markets
Diversity of end products
Positive marketing image
Unique characteristics of product
Raw product quality well matched to market
Many buyers of raw materials and products
Many sellers of raw materials and products
Buyers aware of product or brand
Rare resource
Slow replacement of harvested product
Destructive and damaging harvesting
Difcult to propagate
Genetically uniform or little potential for selection
Narrow use options
Low yielding and/or poor-quality product
Low-value product
Inconsistent and unpredictable production
Wild resource which is difcult to cultivate
Totally wild resource
Slow growing
Long time to production
Competitive with crops, labor intensive, etc.
Sensitive to adverse environmental conditions
Only locally distributed
Source: Reproduced from Leakey, R.R.B., Tchoundjeu, Z., Schreckenberg, K., Shackleton, S.E., Shackleton, C.M., 2005. Agroforestry tree products (AFTPs): Targeting poverty
reduction and enhanced livelihoods. International Journal in Agricultural Sustainability 3, 123.
Table 3
The impacts reported by farmers engaged in a
participatory domestication program for agroforestry trees in Cameroon
267
Table 4
The characteristics of the participatory domestication of
agroforestry trees important for the delivery of multifunctional
agriculture
Positive impacts
Increased number of farmers adopting agroforestry and the
domestication of indigenous trees
Increased production of tree products
Increased income from tree sales by nurseries
Increased income from sale of tree products
Increased income from better farming practices
Increased income from eligibility for micronance
Increased income used for schooling and school uniforms
Increased income used for medicines and healthcare
Increased income used for home improvements for example,
installation of water and electricity in the home, new buildings, etc.
Increased income used for farm improvement for example, livestock,
wells, agricultural inputs, etc.
New employment opportunities from nurseries
New employment opportunities from processing both agricultural crops
(such as cassava) and new markets for processed agroforestry
products (fruits, spices, herbs, and medicinals)
New employment opportunities in the emerging workshops producing
small tools and appropriate mechanized equipment to service the need
for food processing equipment
New employment opportunities from marketing as traders of processed
products and the food processing equipment
New employment opportunities in transport from producers to markets
and to the processors of agricultural produce
Retention of youths in the villages due to career opportunities by
domesticating trees in their village nurseries
Tree domestication has led to better diets and improved nutrition
Luxury food items consumed
Improved health from potable water
Piped water supplies for irrigation and use in nurseries
Increased livestock rearing due to tree fodder
Increased use of traditional medicines and better health
Increased honey production and processing
Reduced drudgery in women's lives from not having to collect water from
rivers and farm produce from remote farms, as well as from
mechanical processing of food crops
Reduced drudgery gives more time to look after their families and engage
in farming or other income-generating activities
Improved marketing for food and agroforestry products
Improved soil fertility from improved fallows has increased crop yields 2to 3-fold with better weed control
Improved tree fodder for goats and cattle
Having more time as a result of better farming methods, farmers had
more time for marketing and new farming activities
Community feeling empowered, stronger, and optimistic for the future in
ways that they could sustain
Knowledge has empowered the Rural Resource Centers as an agent of
change
Negative impacts
Increased jealousy and theft
New roads lead to deforestation and land degradation as a result of the
expansion of farming activities to more remote areas
Future Impact
Signicantly, one of the outcomes mentioned by young
people in the participating communities is that this now
means that they can see a future for themselves if they remain
in the village rather than feeling that they have to migrate to
towns and cities for a better life (Table 2).
268
References
Asaah, E.K., 2012. Beyond vegetative propagation of indigenous fruit trees:
Case of Dacryodes edulis (G.Don) H. J. Lam and Allanblackia oribunda Oliv.
PhD Thesis, Faculty of Bioscience Engineering, Ghent University, Belgium
231 pp.
Asaah, E.K., Tchoundjeu, Z., Leakey, R.R.B., et al., 2011. Trees, agroforestry and
multifunctional agriculture in Cameroon. International Journal of Agricultural
Sustainability 9, 110119.
Asaah, E.K., Tchoundjeu, Z., Wanduku, T.N., Van Damme, P., 2010. Understanding
structural roots system of 5-year-old African plum tree (D. edulis) of seed and
vegetative origins (G. Don) H. J. Lam). Trees 24, 789796.
Asaah, E.K., Wanduku, T.N., Tchoundjeu, Z., Kouodiekong, L., van Damme, P.,
2012. Do propagation methods affect the ne root architecture of African plum
(Dacryodes edulis)? Trees 26, 14611469.
Barrett, C.B., Ashley, J.G., Carter, M.R., 2010. The power and pitfalls of experiments
in development economics: Some non-random reections. Applied Economic
Perspectives and Policy 32, 515548.
Diamond, J., 1997. Guns, Germs and Steel: The Fates of Human Societies. London,
UK: W. W. Norton & Co.
Franzel, S., Akinnifesi, F.K., Ham, C., 2008. Setting priorities among indigenous fruit
tree species in Africa: Examples from southern, eastern and western Africa
regions. In: Akinnifesi, F.K., Leakey, R.R.B., Ajayi, O.C. et al. (Eds.), Indigenous
Fruit Trees in the Tropics: Domestication, Utilization and Commercialization.
Wallingford, UK: CABI, pp. 127.
Franzel, S., Jaenicke, H., Janssen, W., 1996. Choosing the right trees: Setting
priorities for multipurpose tree improvement. ISNAR Research Report 8, 87 pp.
The Hague, Netherlands: ISNAR.
ICRAF, 2012. Agroforestry Tree Genetic Resources Strategy 20132017, World
Agroforestry Centre PO Box 30677-00100 Nairobi, Kenya, 19 pp.
Jamnadass, R., Lowe, A., Dawson, I.K., 2009. Molecular markers and the
management of tropical trees: The case of indigenous fruits. Tropical Plant
Biology 2, 112.
Jamnadass, R.H., Dawson, I.K., Franzel, S., et al., 2011. Improving livelihoods and
nutrition in sub-Saharan Africa through the promotion of indigenous and exotic
fruit production in smallholders agroforestry systems: A review. International
Forest Review 13, 338354.
Kalinganire, A., Weber, J.C., Coulibaly, S., 2012. Improved Ziziphus mauritiana
germplasm for Sahelian smallholder farmers: First steps toward a domestication
programme. Forests, Trees and Livelihoods 21, 128137.
Kengni, E., Tchoundjeu, Z., Tchouangep, F.M., Mbofung, C.M.F., 2001. Sensory
evaluation of Dacryodes edulis fruit types. Forests, Trees and Livelihoods 11,
110.
Ladipo, D.O., Leakey, R.R.B., Grace, J., 1991. Clonal variation in a four year old
plantation of Triplochiton scleroxylon K. Schum. and its relation to the Predictive
Test for Branching Habit. Silvae Genetica 40, 130135.
Ladipo, D.O., Leakey, R.R.B., Grace, J., 1992. Variations in bud activity from
decapitated, nursery-grown plants of Triplochiton scleroxylon in Nigeria: Effects
of light, temperature and humidity. Forest Ecology and Management 50,
287298.
Leakey, R.R.B., 1999a. Agroforestry for biodiversity in farming systems. In: Collins,
W.W., Qualset, C.O. (Eds.), Biodiversity in Agroecosystems. New York: CRC
Press, pp. 127145.
Leakey, R.R.B., 1999b. Potential for novel food products from agroforestry trees.
Food Chemistry 64, 114.
Leakey, R.R.B., 2004. Physiology of vegetative reproduction. In: Burley, J., Evans, J.,
Youngquist, J.A. (Eds.), Encyclopaedia of Forest Sciences. London, UK:
Academic Press, pp. 16551668.
Leakey, R.R.B., 2010. Agroforestry: A delivery mechanism for multifunctional
agriculture. In: Kellimore, L.R. (Ed.), Handbook on Agroforestry: Management
Practices and Environmental Impact. Environmental Science, Engineering and
Technology Series. New York, USA: Nova Science Publishers, pp. 461471.
Leakey, R.R.B., 2012a. The intensication of agroforestry by tree domestication for
enhanced social and economic impact. CAB Reviews: Perspectives in Agriculture,
Veterinary Science, Nutrition and Natural Resources 7 (035), 13.
Leakey, R.R.B., 2012b. Living with the Trees of Life Towards the Transformation
of tropical Agriculture. Wallingford, UK: CABI, 200 pp.
Leakey, R.R.B., 2013. Addressing the causes of land degradation, food/nutritional
insecurity and poverty: A new approach to agricultural intensication in the
tropics and sub-tropics. In: Hoffman, U. (Ed.), UNCTAD Trade and Environment
Review 2012. Geneva, Switzerland: UNCTAD. Available at: www.unctad.org/
Templates/Page.asp?intItemID=3723&lang=1 (accessed 16.09.12).
Leakey, R.R.B., 2012d. Participatory domestication of indigenous fruit and nut trees:
New crops for sustainable agriculture in developing countries. In: Gepts, P.L.,
Famula, T.R., Bettinger, R.L. et al. (Eds.), Biodiversity in Agriculture:
Domestication, Evolution and Sustainability. Cambridge, UK: Cambridge
University Press, pp. 479501.
Leakey, R.R.B., Akinnifesi, F.K., 2008. Towards a domestication strategy for
indigenous fruit trees in the tropics. In: Akinnifesi, F.K., Leakey, R.R.B., Ajayi,
O.C. et al. (Eds.), Indigenous Fruit Trees in the Tropics: Domestication,
Utilization and Commercialization. Wallingford, UK: CAB International, pp. 2849.
Leakey, R.R.B., Asaah, E.K., 2013. Underutilised species as the backbone of
multifunctional agriculture The next wave of crop domestication. Acta
Horticulturae 979, 293310.
Leakey, R.R.B., Izac, A.-M., 1996. Linkages between domestication and
commercialization of non-timber forest products: Implications for agroforestry. In:
Leakey, R.R.B., Temu, A.B., Melnyk, M. (Eds.), Domestication and
Commercialization of Non-timber Forest Products. Rome, Italy: FAO, pp. 17.
Non-Wood Forest Products No. 9.
Leakey, R.R.B., Ladipo, D.O., 1987. Selection for improvement in vegetativelypropagated tropical hardwoods. In: Atkin, R., Abbott, J. (Eds.), Improvement of
Vegetatively Propagated Plants. London: Academic Press, pp. 324336.
Leakey, R.R.B., Mesn, J.F., Tchoundjeu, Z., et al., 1990. Low-technology techniques
for the vegetative propagation of tropical tress. Commonwealth Forestry Review
69, 247257.
Leakey, R.R.B., Newton, A.C. (Eds.), 1994. Tropical Trees: Potential for
Domestication, Rebuilding Forest Resources. London: HMSO, 284 pp.
Leakey, R.R.B., Page, T., 2006. The ideotype concept and its application to the
selection of AFTP cultivars. Forests, Trees and Livelihoods 16, 516.
Leakey, R.R.B., Schreckenberg, K., Tchoundjeu, Z., 2003. The participatory
domestication of West African indigenous fruits. International Forestry Review 5,
338347.
Leakey, R.R.B., Simons, A.J., 2000. When does vegetative propagation provide a
viable alternative to propagation by seed in forestry and agroforestry in the
tropics and subtropics? In: Wolf, H., Arbrecht, J. (Eds.), Problem of Forestry in
Tropical and Sub-tropical Countries The Procurement of Forestry Seed The
Example of Kenya. Germany: Ulmer Verlag, pp. 6781.
Leakey, R.R.B., Tchoundjeu, Z., Schreckenberg, K., Shackleton, S.E., Shackleton,
C.M., 2005. Agroforestry tree products (AFTPs): Targeting poverty reduction and
enhanced livelihoods. International Journal in Agricultural Sustainability 3, 123.
Leakey, R.R.B., Weber, J.C., Page, T., et al., 2012. Tree domestication in
agroforestry: Progress in the second decade. In: Nair, P.K., Garrity, D. (Eds.),
Agroforestry The Future of Global Land Use. USA: Springer, pp. 145173.
Lombard, C., Leakey, R.R.B., 2010. Protecting the rights of farmers and communities
while securing long term market access for producers of non-timber forest
products: Experience in southern Africa. Forests, Trees and Livelihoods 19,
235249.
269
Relevant Websites
www.internationaltreefoundation.org
International Tree Foundation.
www.worldagroforestrycentre.org
World Agroforestry Centre.
Glossary
Agroforestry Purposeful growing of trees, crops,
sometimes with animals, in interacting combinations for a
variety of objectives. Agrisilviculture trees crops;
Silvopasture trees pasture/animals;
Agrosilvopasture trees crops animals/pasture.
Alley cropping Growing crops in the interspaces between
rows of planted trees or shrubs. In the tropics, crops are
grown in the alleys between trees or regularly pruned
hedgerows of planted, usually nitrogen-xing, shrubs or
trees. In temperate zones, crops are grown in the alleys of
widely spaced timber trees.
Community forestry A form of social forestry, where treeplanting activities are undertaken by a community of people
on common or communally owned land.
270
doi:10.1016/B978-0-444-52512-3.00021-8
271
272
Other classication schemes of AFS have also been proposed (e.g., Sinclair, 1999); but essentially they are all based on
the above criteria and concepts. Various characterizations and
descriptions of AFS such as agrisilvicultural systems for fuelwood production in semiarid lands, silvopastoral systems for
animal production in sloping lands, multistrata homegardens
in humid tropics, etc., are common in agroforestry literature.
Moreover, descriptions of existing systems as well as recommendations of potential agroforestry technologies for specic
agroecological zones include a mixture of various forms of
agroforestry in terms of the nature and arrangement of components, and several AFS can be found within the same ecological regions. Thus, in general, any specic agroforestry
practice cannot be identied exclusively to a specic ecological
region, and vice versa.
The nature, complexity, and objectives of agroforestry vary
considerably between the tropics and the temperate region.
Table 1 presents a list of the major tropical practices. Local
adaptations and manifestations of these (and other) practices
exist as innumerable AFS with site-specic characteristics in
different parts of the tropics and subtropics (Nair, 1989;
1993).
Compared with the tropics, agroforestry practices and systems in the temperate zone are less diverse and complex. The
Association for Temperate Agroforestry (AFTA) has recognized
ve major agroforestry practices in North America: alley
cropping, forest farming, riparian buffer strips, silvopasture,
and windbreaks (Figure 1). Other temperate-zone AFS include
the ancient tree-based agriculture involving a large number of
multipurpose trees such as chestnuts (Castanea spp.), oaks
(Quercus spp.), carob (Ceratonia siliqua L.), olive (Olea europa
L.), and gs (Ficus spp.) in the Mediterranean region (Nair
et al., 2008; Rigueiro-Rodriguez et al., 2008). The dehesa system, grazing under oak trees with strong linkages to recurrent
cereal cropping in rangelands, is also a very old European
practice (Rigueiro-Rodriguez et al., 2008; Howlett et al., 2011;
Mosquera-Losada et al., 2012).
AFS Subgroups
To further streamline AFS nomenclature and reduce the
number of major groups, Nair (2012a) arranged the systems
into ve major subgroups with major types of AFS identied
under each, as listed below. These are followed in this article:
1. Multistrata systems
Homegardens (including mixed fruit and spice tree
gardens): Intimate multistory combinations of several
trees especially fruit- and nut-producing species and
crops in homesteads; livestock may or may not be present; the size of the garden is small (o1 ha) and the
garden is managed intensively usually by family labor.
Shaded perennials: Growing shade-tolerant species such
as cacao (Theobroma cacao L.) and coffee (Coffea sp.)
under or in between overstory shade-, timber-, or other
commercial tree crops.
Other multistrata agroforests: Various other forms of
complex multistrata agroforests and multilayer tree
gardens exist in different tropical humid lowland regions of Southeast Asia and parts of Africa and Latin
Table 1
273
Agroforestry practice
Brief description
Tropical agroforestry
Alley cropping (hedgerow
intercropping)
Fast-growing, preferably leguminous, woody species grown in crop elds; the woody species pruned
periodically to a low height (o1.0 m) to reduce shading of crops; the prunings applied as mulch into
the alleys as a source of organic matter and nutrients, or used as animal fodder.
Intimate multistory combinations of a diverse and large number of trees and crops in homesteads;
livestock may or may not be present.
Fast-growing, preferably leguminous, woody species planted and left to grow for short periods
(23 years) of fallow between cropping periods for soil fertility enhancement; woody species
may yield economic products.
Fruit trees and other MPTs scattered haphazardly or planted in some systematic arrangements in crop
or animal production elds; trees provide products such as fruits, fuelwood, fodder, and timber.
Integration of trees in animal production systems:
Homegardens
Improved fallow
Grazing systems
Cut-and-carry system
J
J
(Protein banks)
Shaded perennial-crop systems
Growing shade-tolerant species such as cacao and coffee under or in between overstory shade-,
timber-, or other commercial tree crops.
Use of trees to protect elds from wind damage, sea encroachment, oods, etc.
Growing agricultural crops during the early stages of establishment of forestry (timber) plantations.
Alley cropping
Forest farming
Riparian buffer
strips
Silvopasture
Windbreaks
Figure 1 Agroforestry practices in North America.
between-row spacing; the woody species pruned periodically at low height (o1.0 m) to reduce shading of crops;
the prunings applied as mulch into the alleys as a source
of organic matter and nutrients, or used as animal fodder.
Multipurpose trees on farmlands: Fruit-, fodder-, fuelwood-, and timber trees scattered or planted in some
systematic arrangements in crop- or animal-production
elds.
274
Table 2
AFS subgroup
Major AF practices
Multistrata
systems
Homegardens
Shaded perennials
Tree intercropping
Alley cropping
Trees on farmlands
Cut-and-carry and
browsing
Grazing under trees
Silvopasture
Protective systems
Agroforestry
woodlots
275
Windbreaks,
shelterbelts
Soil conservation
hedges
Boundary planting
Firewood and fodder
Land reclamation
Tropical
Tropical
Total
Temperate
Temperate
100
Forest farming
n/a
n/a
50
550
300
50
50
150
200
100
50
1250
350
Figure 2 Tropical alley cropping. Fast-growing, coppicing, nitrogenxing shrubs and trees are grown in rows 48 m apart in crop elds
and pruned periodically (46 week intervals); the succulent and easily
decomposable tree biomass so obtained is returned to the cropped
alleys as a source of nutrient for crops. The photo shows Gliricidia
sepium grown with maize (Zea mays), a practice followed by
thousands of farmers in eastern and southern Africa. Photo credit:
ICRAF, Nairobi, Kenya.
276
animals are let loose for grazing over crop residues and grasses.
The practice is therefore considered as extensive intercropping
or silvopasture.
Multistrata Systems
Intensive, multispecies, tree-based farming systems such as
homegardens, shaded perennial stands, and other complex
agroforests are common agroforestry practices in the humid
and subhumid parts of the tropics, especially in the lowlands
(Figure 5). The structural and functional diversity and various
other characteristics of these systems have been well described
and reviewed (Nair, 1989; Kumar and Nair, 2006). Homegardens have a long tradition of providing food and nutritional security as well as environmental sustainability in
smallholder production systems, often in heavily populated
regions of lowland humid tropics in south- and southeast Asia,
and to a small extent in other tropical and subtropical regions.
Although a few systems that have some similarities to tropical
homegardens can be found in parts of the temperate regions as
well (e.g., the satoyama system in Japan: Ichikawa and Toth,
2012), intensive multispecies homegardens are a unique
agroecosystem of the tropics.
Shaded-perennial systems that involve growing tree crops
such as coffee (Coffea sp.) and cacao (T. cacao) under the shade
of overstory tree species (Figure 6) represent another traditional example of high-intensity crop combination that has
some unique ecological features and commercial value. In
addition to coffee and cacao, several of the tropical fruit- and
nut-producing tree species that are harvested annually or at
shorter intervals are often grown in association with understory- or overstory species (Elevitch, 2006, 2011; Gama-Rodrigues et al., 2010). In some situations, the species combinations
and management features of these systems are very similar
to those of homegardens such that, at the landscape- and
village level, there is a continuum of plant associations from
277
Protective AFS
278
Figure 7 Riparian buffer. Bear Creek National Restoration Watershed (designated under the Clean Water Action Plan, 1999) and the USDA
designated Bear Creek National Research and Demonstration Site. The pictures are of various kinds of riparian buffers along Bear Creek. Photo
credit: The Iowa State University NREM Riparian Buffer Team, ISU, USA.
Silvopasture
Silvopasture that combines trees, forages, and shrubs with
livestock operations is another type of agroforestry practice
that is popular in both the tropics and the temperate regions.
Broadly, there are two major forms of silvopasture: grazingand tree-fodder systems. In grazing systems, cattle are allowed
to graze on pasture under widely spaced or scattered trees
(Figure 8), whereas in the tree-fodder systems, the animals are
stall-fed with fodder from trees or shrubs grown in blocks
(fodder banks) on farms (Nair et al., 2008; Kiptot and Franzel,
2012). Most silvopastoral systems in Africa and other developing regions of the world involve extensive open grazing
by free-roaming animals under scattered natural stands of trees
and shrubs mostly in semiarid to arid areas, as in the parklands of sub-Saharan Africa. More intensive grazing systems of
silvopasture are practiced in Latin America where animals are
penned in parcels of land with barbed-wired living-fence, and
grazing is regulated (Somarriba et al., 2012). Such organized
silvopastoral systems are also becoming popular in the extensive Cerrado region of Brazil (Nair et al., 2011). The most
Food Security
In sub-Saharan Africa, which is home to three-quarters of
the worlds ultra-poor (less than US$0.50 per day), approxi-
279
280
Table 3
Estimates of carbon sequestration in agroforestry systems in different ecological regions of Africa and Asia
Agroforestry
system
subgroup
Major AF practices
Multistrata
systems
Tree
Intercropping
Homegardens
Shaded perennials
Alley cropping
Multipurpose trees on
farmlands
Tree fodder (browsing, cutand-carry)
Grazing under trees
Windbreaks, shelterbelts,
soil conservation hedges,
boundary planting
Woodlots for rewood,
fodder, land reclamation
Silvopasture
Protective
systems
Agroforestry
Tree woodlots
Above ground
Below ground
(especially soils)
Above ground
2 to 18
5 to 15
Up to 15
Up to 12
Up to 200
Up to 300
Very low to 150
Very low to 150
0.53
14
0.54
0.22.5
1.53.5
1.05
1.53.5
1.53.5
1.83
Very low to 80
0.34
1.02.5
1.58
1.57
Very low to 60
Very low to 60
0.32
0.72
0.41.0
0.41.0
1.57
Very low to 60
15
1.06.0
Source: Reproduced from Nair, P.K.R., 2012b. Carbon stocks in agroforestry systems: A global appraisal. Presented at the ASA/CSSA/SSSA International Annual Meetings, 2124
October 2012, Cincinnati, OH, USA. Available at: www.agronomy.org/annualmeetings2012 (accessed 10.05.13).
Ecosystem Services
Exploiting nitrogen xation by tropical legumes, enhancing
the efciency of nutrient cycling, and benetting from the
deep-capture of nutrients are recognized as the primary bases
Conclusions
Modern agricultural systems have resulted in signicant gains
in agricultural production worldwide and averted large-scale
hunger over the past half century. Yet, many developing regions of the world, notably sub-Saharan Africa, lag behind the
rest of the world in food production and other aspects of development. This is because the input-intensive agricultural
technologies of the Green Revolution have turned out to be
unsuitable for Africas infertile soils, unforgiving climate, weak
infrastructure, and sociocultural traditions. During the past
35 years, research and development efforts have widely demonstrated the positive role of AFS in addressing some of the
major problems of Africa and other parts of the world such as
food- and nutritional insecurity, soil degradation, desertication, and climate change; yet agricultural development
efforts have vastly ignored the values of such time-tested integrated systems and their social values.
Conventionally, one has treated agriculture and forestry
separately although these sectors are often interwoven on the
References
Albrecht, A., Kandji, S.T., 2003. Carbon sequestration in tropical agroforestry
systems. Agriculture Ecosystems and Environment 99, 1527.
Boffa, J.-M., 1999. Agroforestry Parklands in Sub-Saharan Africa. FAO Conservation
Guide 34. Rome, Italy: Food and Agriculture Organization of the United Nations.
Brandle, J.R., Hodges, L., Tyndall, J., Sudmeyer, R.A., 2009. Windbreak practices.
In: Garrett, H.E. (Ed.), North American Agroforestry: An Integrated Science
and Practice, second ed. Madison, WI: American Society of Agronomy,
pp. 75104.
Brown, L.R., 2004. Outgrowing the Earth: The Food Security Challenge in an Age of
Falling Water Tables and Rising Temperatures. New York: W.W. Norton.
Buresh, R.J., Cooper, P.J.M. (Eds.), 1999. The science and practice of improved
fallows. Agroforestry Systems 47, 3358.
Elevitch, C.R. (Ed.), 2006. Traditional Trees of Pacic Islands. Holualoa, HI, USA:
Permanent Agriculture Resources.
Elevitch, C.R. (Ed.), 2011. Specialty Crops for Pacic Islands. Holualoa, HI, USA:
Permanent Agriculture Resources.
Gama-Rodrigues, E.F., Nair, P.K.R., Nair, V.D., et al., 2010. Carbon storage in soil
size fractions under two cacao agroforestry systems in Bahia, Brazil.
Environmental Management 45, 274283.
Garrett, H.E. (Ed.), 2009. North American Agroforestry: An Integrated Science and
Practice, second ed. Madison, WI: American Society of Agronomy.
Garrity, D.P., 2004. Agroforesty and the achievement of the Millennium Development
Goals. Agroforestry Systems 61, 517.
Garrity, D.P., 2012. Agroforestry and the future of global land use. In: Nair, P.K.R.,
Garrity, D.P. (Eds.), Agroforestry: The future of Global Land Use. Dordrecht, The
Netherlands: Springer, pp. 2127.
Garrity, D.P., Akinnifesi, F., Ajayi, O., et al., 2010. Evergreen agriculture:
A robust approach to sustainable food security in Africa. Food Security 2,
197214.
Gold, M.A., Garrett, H.E., 2009. Agroforestry nomenclature, concepts, and practices.
In: Garrett, H.E. (Ed.), North American agroforestry: An integrated science
and practice, second ed. Madison, WI: American Society of Agronomy,
pp. 4556.
Herrero, M., Thornton, P.K., Notenbaert, A.M., et al., 2010. Smart investments in
sustainable food production: Revisiting mixed crop-livestock systems. Science
327 (5967), 822825.
Howlett, D.S., Mosquera-Losada, M.R., Nair, P.K.R., Nair, V.D., Rigueiro-Rodrguez,
A., 2011. Soil carbon storage in silvopastoral systems and a treeless pasture in
northwestern Spain. Journal of Environmental Quality 40, 825832.
Ichikawa, K., Toth, G.G., 2012. The satoyama landscape of Japan: The future of
indigenous agricultural system in an industrialized society. In: Nair, P.K.R,
Garrity, D.P. (Eds.), Agroforestry: The Future of Global Land Use. Dordrecht. The
Netherlands: Springer, pp. 341358.
Jose, S., Gold, M., Garrett, H.E., 2012. The future of temperate agroforestry in the
United States. In: Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry: The Future of
Global Land Use. Dordrecht, The Netherlands: Springer, pp. 217245.
281
Kiptot, E., Franzel, S., 2012. Gender and agroforestry in Africa: Who benets?
The African perspective. In: Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry:
The Future of Global Land Use. Dordrecht, The Netherlands: Springer,
pp. 463496.
Kort, J., Turnock, R., 1999. Carbon reservoir and biomass in Canadian prairie
shelterbelts. Agroforestry Systems 44, 175186.
Kumar, B.M., Nair, P.K.R., 2004. The enigma of tropical homegardens. Agroforestry
Systems 61, 135152.
Kumar, B.M., Nair, P.K.R. (Eds.), 2006. Tropical Homegardens: A Time-tested
Example of Sustainable Agroforestry. Dordrecht, the Netherlands: Springer.
Lal, R., 2010. Beyond Copenhagen: Mitigating climate change & achieving food
security through soil carbon sequestration. Food Security 2, 169177.
Leakey, R.R.B., 2012a. Living with the trees of life: Towards the transformation of
tropical agriculture. Wallingford, UK: CABI.
Leakey, R.R.B., 2012b. The intensication of agroforestry by tree domestication for
enhanced social and economic impact. CAB Reviews: Perspectives in Agriculture,
Veterinary Science, Nutrition and Natural Resources 7 (35), 13.
Leakey, R.R.B., Weber, J.C., Page, T., et al., 2012. Tree domestication in
agroforestry: Progress in the second decade (20032012). In: Nair, P.K.R.,
Garrity, D.P. (Eds.), Agroforestry: The Future of Global Land Use. Dordrecht, The
Netherlands: Springer, pp. 145173.
Matocha, J., Schroth, G., Hills, T., Hole, D., 2012. Integrating climate change
adaptation and mitigation through agroforestry and ecosystem conservation. In:
Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry: The Future of Global Land Use.
Dordrecht, The Netherlands: Springer, pp. 105126.
Michel, G.A, Nair, V.D, Nair, P.K.R., 2007. Silvopasture for reducing phosphorus
loss from subtropical sandy soils. Plant and Soil 297, 267276.
Mosquera-Losada, M.R., Moreno, G., Pardini, A., et al., 2012. Past, present, and
future of agroforestry in Europe. In: Nair, P.K.R., Garrity, D.P. (Eds.),
Agroforestry: The Future of Global Land Use. Dordrecht, The Netherlands:
Springer, pp. 285312.
Mutuo, P.C., 2005. Potential of agroforestry for carbon sequestration and mitigation
of greenhouse gas emissions from soils in the tropics. Nutrient Cycling in
Agroecosystems 71, 4354.
Nair, P.K.R., 1985. Classication of agroforestry systems. Agroforestry Systems 3,
97128.
Nair, P.K.R. (Ed.), 1989. Agroforestry Systems in the Tropics. Dordrecht, The
Netherlands: Kluwer.
Nair, P.K.R., 1993. An Introduction to Agroforestry. Dordrecht, The Netherlands:
Kluwer.
Nair, P.K.R., 2012a. Climate change mitigation and adaptation: A low hanging fruit
of agroforestry. In: Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry: The Future of
Global Land Use. Dordrecht, The Netherlands: Springer, pp. 3167.
Nair, P.K.R., 2012b. Carbon stocks in agroforestry systems: A global appraisal.
Presented at the ASA/CSSA/SSSA International Annual Meetings, 2124
October 2012, Cincinnati, OH, USA. Available at: www.agronomy.org/
annualmeetings2012 (accessed 10.05.13).
Nair, P.K.R., Garrity, D.P., 2012. Agroforestry research and development The way
forward. In: Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry: The future of global
land use. Dordrecht, The Netherlands: Springer, pp. 515531.
Nair, P.K.R, Gordon, A.M, Mosquera-Losada, M.R., 2008. Agroforestry. In:
Jorgensen, S.E, Faith, B.D. (Eds.), Encyclopedia of Ecology, vol. 1. Oxford, UK:
Elsevier, pp. 101110.
Nair, P.K.R., Kumar, B.M., 2006. Introduction Tropical Homegardens: A Time-tested
Example of Sustainable Agroforestry. Dordrecht, The Netherlands: Springer
110.
Nair, P.K.R., Kumar, B.M., Nair, V.D., 2009. Agroforestry as a strategy for carbon
sequestration. Journal of Plant Nutrition and Soil Science 172, 1023.
Nair, P.K.R., Nair, V.D., Kumar, B.M., Showalter, J.M., 2010. Carbon sequestration
in agroforestry systems. Advances in Agronomy 108, 237307.
Nair, P.K.R., Tonucci, R.G., Garcia, R., Nair, V.D., 2011. Silvopasture and carbon
sequestration with special reference to the Brazilian Savanna (Cerrado). In:
Kumar, B.M., Nair, P.K.R. (Eds.), Carbon Sequestration in Agroforestry Systems.
Dordrecht, The Netherlands: Springer, pp. 145162.
Polglase, P., Paul, K., Hawkins, C., et al., 2008. Sustainable Ecosystems. Canberra,
Australia: CSIRO RIRDC Publication No. 08/176.
Quinkenstein, A., Freese, D., Bhm, C., Tsonkova, P., Httl, R., 2012. Agroforestry
for mine-land reclamation in Germany: Capitalizing on carbon sequestration
and bioenergy production. In: Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry:
The Future of Global Land Use. Dordrecht, The Netherlands: Springer,
pp. 313339.
Rao, M.R., Nair, P.K.R., Ong, C.K., 1998. Biophysical interactions in tropical
agroforestry systems. Agroforestry Systems 38, 350.
282
Reij, C., Tappan, G., Smale, M., 2009. Agroenvironmental Transformation in the
Sahel: Another Kind of Green Revolution. Washington, DC: International Food
Policy Research Institute IFPRI Discussion Paper 00914.
Rigueiro-Rodriguez, A., McAdam, J.H., Mosquera-Losada, M.R., 2008. Agroforestry
in Europe. Dordrecht, The Netherlands: Springer.
Saha, S.K., Nair, P.K.R., Nair, V.D., Kumar, B.M., 2010. Carbon storage in relation
to soil size-fractions under some tropical tree-based land-use systems. Plant and
Soil 328, 433446.
Sanchez, P.A., 1999. Improved fallows come of age in the tropics. Agroforestry
Systems 47, 312.
Schultz, R.C., Isenhart, T.M., Colletti, J.P., et al., 2009. Riparian and upland buffer
practices. In: Garrett, H.E. (Ed.), North American Agroforestry: An Integrated
Science and Practice, second ed. Madison, WI: American Society of Agronomy,
pp. 163218.
Sinclair, F.L., 1999. A general classication of agroforestry practice. Agroforestry
Systems 46, 161180.
Smith, J.R., 1950. Tree Crops A Permanent Agriculture. New York, NY: The
Devin-Adair Company.
Somarriba, S., Beer, J., Orihuela, J., et al., 2012. Mainstreaming agroforestry
in Latin America. In: Nair, P.K.R., Garrity, D.P. (Eds.), Agroforestry: The
Future of Global Land Use. Dordrecht, The Netherlands: Springer, pp. 429453.
Swaminathan, M.S., 2012. Agroforestry for an ever-green revolution. In: Nair, P.K.R.,
Garrity, D.P. (Eds.), Agroforestry: The Future of Global Land Use. Dordrecht, The
Netherlands: Springer, pp. 710.
Thevathasan, N.V., Gordon, A.M., Bradley, R., et al., 2012. Agroforestry research and
development in Canada: The way forward. In: Nair, P.K.R., Garrity, D.P. (Eds.),
Agroforestry: The Future of Global Land Use. Dordrecht, The Netherlands:
Springer, pp. 247283.
United Nations, 2010. Fact Sheet. Retrieved 26 Sept 2012 from UNFCCC Website:
http://unfccc.int/press/fact_sheets/items/4987.php
World Agroforestry Centre, 2008. Transforming Lives and Landscapes, Strategy
20082015. Nairobi, Kenya: World Agroforestry Centre 51 pp.
Zomer, R.J., Trabucco, A., Coe R., Place, F., 2009. Trees on farm: An analysis of
global extent and geographical patterns of agroforestry. ICRAF Working Paper no.
89. Nairobi, Kenya: World Agroforestry Centre.
Relevant Websites
www.aftaweb.org
Association for Temperate Agroforestry (AFTA).
Agroforestry.net.au
Australian Master Tree Grower Program.
www.earth-policy.org
Earth Policy Institute.
www.icraf.org
World Agroforestry Centre (ICRAF).
http://www.icraf.cgiar.org/
World Agroforestry Centre (ICRAF).
Glossary
Air Pollutant Foreign and/or natural substances occurring
in the atmosphere that may result in adverse effects to
humans, animals, and/or the surrounding environment.
Ammonia (NH3) A colorless gaseous compound of
nitrogen and hydrogen that is highly soluble in water and
has the ability to react with oxides of nitrogen to form
ammonium nitrate, a particulate matter that contributes to
air pollution and the resulting health implications.
Anaerobic digestion A biochemical process in which
bacteria break down biodegradable organic material, such
as manure, in an oxygen-free environment. The breakdown
of organic materials results in the production of biogas,
typically a mixture of methane and carbon dioxide.
Anthropogenic Originating from human activity.
Conned Animal Feeding Operation (CAFO) Agricultural
operations where animals are kept and raised in conned
areas, where animals feed, manure, and production
operations are on a small land area. Usually, feed is brought
to animals in CAFOs rather than the animals grazing. The US
Environmental Protection Agency (EPA) separates CAFOs
into three categories (large, medium, and small) based on the
number of animals in a facility.
Criteria pollutant Six emissions identied and regulated
by the EPA, including: sulfur dioxide, nitrogen dioxide,
particulate matter, carbon monoxide, ozone, and lead.
Introduction
The world population is expected to grow from today's 7 billion people to 9.3 billion people by 2050 (United Nations,
2009). Although the human population shows this dramatic
growth, the amount of arable agricultural land needed to grow
food to nourish these people is limited and can only increase
moderately. Furthermore, increasing disposable income in
developing and emerging countries leads to higher per capita
consumption of animal protein, leading to an expected increase in global dairy and meat consumption of 74% and
58%, respectively (UNFAO, 2012). Thus, food production
must become more efcient and intensication is one of the
most viable solutions. In general, concentrated animal feeding
operations (CAFOs) allow the production of relatively low
cost food; however, there are externalities associated with
CAFOs, such as air and water pollutants, and greenhouse gas
(GHG) emissions.
Over the past decades, there has been a shift from traditional, rather low input, and extensive farms to CAFOs in the
US and throughout much of the developed world. Owing to
the increase in the number of CAFOs and the air quality
issues surrounding them, the US Environmental Protection
Agency (EPA) has created nationwide specications for what
constitutes a CAFO as well as what emissions from these operations must be monitored and mitigated.
For an animal operation to be considered a CAFO, it must
rst meet the denition of an animal feeding operation (AFO).
An AFO is an operation where animals have been, are, or will
be stabled or conned and fed or maintained for a total of 45
days or more in any 12-month period and where vegetation is
not sustained in the connement area during the normal
growing season (USEPA, 2012b). Maintained in this case
means that the animals are conned in the same area where
waste is generated or concentrated and can include areas where
animals are fed, watered, cleaned, groomed, milked, or medicated (USEPA, 2012b). This denition also distinguishes AFOs
from pasture- or grazing-based systems; therefore, animals
raised on pasture are not considered to be produced in an AFO.
AFOs are dened as either medium- or large-sized CAFOs if
a series of EPA specications apply. Most signicantly, an AFO
is considered a CAFO if it is determined to be a signicant
contributor of pollutants to waters of the US (USEPA, 2012b).
Dairy and beef cattle, veal calves, swine, chickens, turkeys,
ducks, horses, and sheep can all fall within the CAFO designation if specic threshold numbers are met. This article presents three types of CAFOs, namely those for large ruminants
(beef and dairy cattle), swine, and poultry (broiler and layer).
doi:10.1016/B978-0-444-52512-3.00090-5
283
284
Air Pollutants
Air pollutants affect human and animal health as well as
ecosystem health and visibility (Pope et al., 2009; CambraLopez et al., 2010). Criteria pollutants that are regulated in the
US and that have the greatest effects on air quality include
carbon monoxide (CO), lead (Pb), nitrogen dioxide (NO2),
particulate matter (PM) of less than 10 m in diameter
(PM10), PM of less than 2.5 m in diameter (PM2.5), ground
level ozone (O3), and sulfur dioxide (USEPA, 2001). These
criteria pollutants and some of their precursor compounds are
regulated under the Clean Air Act and enforced by the USEPA,
to address direct public health concerns (USEPA, 2012a). The
National Research Council (NRC, 2003) provided a list of air
emissions, which contribute most signicantly to air quality
concerns (Tables 1 and 2). In CAFOs, the primary air pollutants of concern are PM, ammonia (NH3), hydrogen sulde
(H2S), volatile organic compounds (VOC), and odors. Although NH3, H2S, VOCs, and odors are not directly regulated
from most environmental agencies (with the exception of
central and southern California), it is important to minimize
these emissions because they can lead to the formation of
criteria pollutants and often constitute nuisances. For example,
ammonia can contribute to secondary PM formation (Pinder
et al., 2007), VOCs can contribute to O3 formation (Shaw
et al., 2007; Sun et al., 2008), and both NH3 and VOCs contribute to odor production, a growing concern for policymakers as well as the general public. Additionally, there is an
association between exposure to PM and adverse human and
animal health effects in livestock CAFOs (Aneja et al., 2009).
Table 1
Human exposures to PM2.5 have been associated with pulmonary disease (Pope et al., 2009) and those to PM10 with
decreased lung function, cardiac arrhythmia, heart attacks, and
premature death (Madden et al., 2008). PM also contributes to
impaired atmospheric visibility by scattering and absorbing
light (Boylan et al., 2006), issues which are discussed in other
article.
The following section discusses air quality issues emitted
across all CAFO types.
Ammonia
Livestock is estimated to be the single largest source of NH3
emissions in the US, producing 71.3% of annual emissions
(USEPA, 2000). Ammonia primarily results from manure
degradation and forms when urease, an enzyme present in
animal feces, catalyzes the hydrolysis of urea from urine (Sun
et al., 2008). The formation of ammonia occurs as follows:
(NH2)2CO+H2OCO2+2NH3
Ammonia emissions are dependent on the amount of urea
nitrogen (urea-N) and degree of mixing between urine and
feces (Bussink and Oenema, 1998) and as a result, there are
great variations in NH3 emissions between farms (James et al.,
1999; VandeHaar and St-Pierre, 2006), manure land-application methods (Amon et al., 2006), and time of year (Bussink
and Oenema, 1998). The production rate of urea-N, and
subsequently NH3, is directly related to the concentration of
nitrogen ingested by animals. Urea in ruminants is produced
in the liver (detoxication of ammonia from blood circulation) and excreted in the urine. Overfeeding protein in the
diet commonly leads to increased urea excretions, which affects NH3 formation (Burgos et al., 2010). The volatilization of
NH3 from any CAFO can be highly variable depending on the
total NH3 concentration in the solid or liquid phase, temperature, pH, and manure storage time. Emissions depend on
how much of the N in solution reacts to form NH3 versus
ionized ammonium (NH4+), which is nonvolatile (i.e., a
nongaseous compound) (USEPA, 2001).
In general, NH3 loss to the atmosphere can lead to PM
formation, soil acidication, and eutrophication of surface
waters (Fangmeier et al., 1994; Krupa, 2003; CAST, 2011) and
decreased livestock performance (Drummond et al., 1980).
Ranking of the importance of Animal Feed Operation (AFO) emissions at global and local scales
Emissions
Methane (CH4)
Nitrous oxide (N2O)
Ammonia (NH3)
Volatile organic compounds(VOCs)b
Particulate matter
Odor
Signicanta
Signicant
Major
Insignicant
Insignicant
Insignicant
Insignicant
Insignicant
Minor
Minor
Signicant
Major
Ranking of the importance of each emissions based on NRC recommendations for the potential impact of emissions, both locally and nationally. Rank order from high to low
is as follows: major, signicant, minor, and insignicant.
b
According to the NRC, 2003, compared with other sources, VOC emissions from AFOs are considered to be insignicant; however, recent research may warrant changes in
this classication.
Source: Adapted from National Research Council (NRC), 2003. Air Emissions from Animal Feeding Operations: Current Knowledge, Future Needs. Washington, DC: National
Academies Press.
Table 2
285
Emissions
Criteria pollutant
Greenhouse gas
CH4
N2O
NH3
Volatile organic compounds
Particulate matter
Odor
Precursor of ozone
X
X
X
X
X
Source: Adapted from National Research Council (NRC), 2003. Air Emissions from Animal Feeding Operations: Current Knowledge, Future Needs. Washington, DC: National
Academies Press.
Hydrogen Sulde
Hydrogen sulde (H2S) and other reduced sulfur compounds
are produced as manure decomposes anaerobically, resulting
in the breakdown of organic matter. Hydrogen sulde can
arise from storage, handling, and decomposition of animal
waste. There are two primary sources of sulfur in animal manures: (1) the sulfur amino acids present in animal feed and
(2) inorganic sulfur compounds, such as copper sulfate and
zinc sulfate, which are used as feed additives to supply animals
with trace minerals and serve as growth stimulants for animals
(USEPA, 2001; NRC, 2003). Although sulfates are used as trace
mineral carriers in all sectors of animal agriculture, their use is
more extensive in the poultry and swine industries. A possible
third source of sulfur in some locations is trace minerals in
drinking water (USEPA, 2001; NRC, 2003). Under anaerobic
conditions, any excreted sulfur that is not in the form of H2S
will be reduced microbially to H2S. Therefore, manure managed in liquid form or slurries are potential sources of H2S
emissions. The magnitude of H2S emissions is a function of
liquid phase concentration, temperature, and pH. Temperature
and pH affect the solubility of H2S in water. The solubility of
H2S in water increases at pH values above 7. Therefore, as pH
shifts from alkaline to acidic, the potential for H2S emissions
increases (Snoeyink and Jenkins, 1980; USEPA, 2001). Under
anaerobic conditions, livestock and poultry manures are
acidic, with pH values below 5.5 (USEPA, 2001). In addition,
H2S causes respiratory problems (Donham et al., 1986) and
may lead to adverse effects on workers health (Mitloehner and
Calvo, 2008). Hydrogen sulde is toxic and can be highly
dangerous especially when it is suddenly released in high
concentrations from stored manure in a conned area and has
caused human and animal mortalities (Ni et al., 2012).
Odors
Odors from CAFOs are a major nuisance and have the potential to negatively impact the quality of life for the nearby
residents (Fournel et al., 2012). Gaseous compounds associated with odor vary greatly in molecular weight and odorant
strength making it challenging to quantify and compare odors.
As a result, the concept of an odor unit (OU) was developed
as a way to normalize the specic odor-related effect of an
odor or mixture of odors. There are six major groups of
odorous compounds, as identied by Mackie et al. (1998),
which includes the previously discussed air pollutants, NH3
and VOCs, and several sulfur-containing compounds.
286
Ammonia
The main sources of NH3 emissions from dairies are fresh
manure, long-term manure storage, and land application of
manure (Bussink and Oenema, 1998). Similarly, primary
emissions from beef CAFOs are from corrals, manure storage,
and eld-applied manure (Stackhouse-Lawson et al., 2012).
Both dairy and beef cattle have the unique ability, being ruminants, to recycle N back to rumen bacteria that would
otherwise be excreted as urinary urea-N. Although this
physiological process reduces N losses, an excess of dietary
crude protein (CP) beyond the animal's nutritional needs
leads to an increase in urinary urea-N content (Marini and Van
Amburgh, 2005). As mentioned in the Section Air Pollutants,
NH3 emissions can be very variable depending on the climate,
time of year, etc. For example, NH3 emissions from dairies
were found to be two to three times greater during the summer
compared with winter (Todd et al., 2008; Bluteau et al., 2009).
Emissions of NH3N from feedlots has been estimated to be as
low as 9% and as high as 56% of N fed to animals (Faulkner
and Shaw, 2008; Todd et al., 2008; CAST, 2011). Total NH3
losses at dairy CAFOs can range from 17 to 40 kg N per year
per cow (Bussink and Oenema, 1998) or between 20 and 40 g
NH3per day per AU (animal unit) in freestall areas (Groot
Koerkamp et al., 1998; Snell et al., 2003). Diet can be altered to
reduce the amount of NH3 emissions from manure (James
et al., 1999; VandeHaar and St-Pierre, 2006). Through optimization of N content of a diet, N excretion per unit of
product, and the related NH3 emissions, can be reduced (de
Boer et al., 2011). The use of precision feeding that closely
matches the nutritional needs of an animal can help to minimize the emissions from manure (Tylutki et al., 2008).
Through precision feeding, producers can avoid the expenses
associated with overfeeding animals and minimize nutrient
excretion that can lead to emissions. This is especially benecial when monitoring CP content of the diet because it avoids
excess N being converted to urea-N, thus avoiding extra
emissions of NH3 to the environment, as mentioned above.
Manure management in dairy and beef CAFOs can also
result in variability of NH3 emissions. For example, ammonia
emissions from scraped or dirt-oored corrals have been
found to be three times greater than those from ushed systems (Kroodsma et al., 1993). Additionally, with short-term
manure storage, solid manure has been found to have signicantly higher NH3 emission rates than liquid manure;
however, long-term storage of manure has a reverse effect
(Dewes, 1999). In the case of lagoons, a cover provided by
either crust or tarp reduces NH3 compared with uncovered
manure storage structures (Sommer et al., 1993). One method
to control emissions from manure is through the use of
additives. Manure additives include commercially available
products that are intended to reduce ammonia volatilization
from manure. The additives are typically mixed with water and
poured evenly into the manure slurry but effectiveness is
variable (USEPA, 2001).
Hydrogen Sulde
The most signicant source of H2S in dairy and beef CAFOs is
from stored manure. When manure is stored in anaerobic
lagoons (as is the case in many dairies) and undergoes microbial degradation, both NH3 and H2S are produced (Xue
and Chen, 1999). Hydrogen sulde is the result of anaerobic
decomposition of sulfur-containing amino acids within these
lagoons. Hydrogen sulde emissions also contribute to the
formation of odorous pollutants, which is further discussed in
the Odor Section below.
Odor
According to the National Research Council (2003) the main
sources of odors emitted from dairy CAFOs result from silage
mounds, barns, waste storage facilities, or land-applied manure.
The greatest contributors of odors in livestock CAFOs are several
groups of VOCs, including sulfur-containing compounds
(hydrogen sulde), volatile fatty acids (VFAs), phenols, and
indoles (Shabtay et al., 2009). Odor emissions from beef cattle
fattening operations are affected by life stage and manure
management (Shabtay et al., 2009). In dairies, VOCs have the
greatest impact on odors. Additionally, land application of
manure, storage of manure, and dairy housing have been found
to produce odor emissions of 1.590, 5.132, and 1.3
3.0 OU s1 m2, respectively (Pain et al., 1991; ASABE, 2006).
Techniques to minimize odor from manure storage include
covering lagoons, either with a natural crust or an articial
Table 3
287
Swine Facilities
To optimize production efciency, the majority of swine facilities use enclosed and ventilated barns for housing. The hog
production cycle has three main phases consisting of farrowing, nursing, and growing/nishing. Swine CAFOs can
consist of one or two of these phases per barn but most
commonly encompass all three in a farrow-nish production
program (USEPA, 2001). In swine CAFOs, emissions are primarily generated from anaerobic microbial decomposition of
organic matter in manure and spoiled feedstuff occurring either in barns, manure storage structures, or during manure
land application (CAST, 2011). As with other livestock species,
swine diet composition has a signicant impact on the concentration and type of emissions coming from animal manure.
There are various management methods utilized in swine
production settings. In the US, swine are mainly intensively
managed indoors on bedded or slatted oors. Bedding, such as
straw, cornstalks, or sawdust, is used to collect solid manure
and this bedding along with the manure is applied to cropland
as fertilizer. There are four principal types of waste management systems used with connement housing in the swine
industry: deep-pit, pull-plug pit, pit recharge, and ush systems (Table 3). These differ depending on the state of manure
collection and frequency of cleaning and draining. All of these
systems use slatted oors (USEPA, 2001). The pit system
allows the animal waste to fall through the slats directly into a
pit and is collected in liquid form (Hamon et al., 2012). Manure storage is in either an anaerobic lagoon or an external
storage facility. In the pit systems, the space may be cleaned
from daily to annual intervals, depending on the type utilized.
In ush systems, manure is removed several times a day
(USEPA, 2001). The pull-plug system removes manure from
the pit after being stored for about a week and is then moved
to outside storage facilities. This keeps emissions lower within
the swine facilities but not necessarily with the later storage of
removed manure (Cole et al., 2000). These storage practices
result in the decomposition of manure and formation of
biogas. Ammonia, hydrogen sulde, and VOC emissions may
be higher in ush systems than from pit recharge and pull-plug
pit systems due to turbulence during ushing.
Ammonia
The major air quality concern from swine CAFOs is NH3
emissions from manure (Cole et al., 2000). Ammonia
Summary of emissions from Swine Model Farms (tons per year per 500 animal unit farm)
Type of manure
Ammonia (NH3)
Flush
Pit recharge
Pull-plug with lagoon
Pull-plug with storage tank
Deep pit
15
15
15
11
12
2.6
0.9
0.9
NA
0.3
0.6
0.6
0.6
NA
NA
Source: Adapted from US Environmental Protection Agency (USEPA), 2001. Emissions from Animal Feeding Operations. EPA 68-D6-0011. Research Triangle Park, NC: USEPA.
288
Hydrogen Sulde
Hydrogen sulde forms in deep-pit, pull-plug pit, and in external manure storage management systems (USEPA, 2001).
According to Zahn et al. (2001), on average, lagoons emitted
0.25 g H2S per square meter per day; deep-pit and pull-plug
systems emitted 0.32 g H2S per square meter per day; and the
eternal tanks emitted 0.95 g H2S per square meter per day.
Once again, the external tanks emitted a signicant amount
more than the lagoons, and deep-pit and pull-plug systems. In
addition to being a health hazard and air pollutant in swine
facilities, H2S contributes to odors, as outlined in the following Odors Section.
Odor
Odors from swine CAFOs are primarily comprised of NH3 and
H2S emissions (Cole et al., 2000; Hamon et al., 2012). Emissions of odors are dependent on seasonal and climatic parameters, as is the case with other CAFOs. Anaerobic processes
can also release VFAs that can be considerably more offensive
than ammonia or hydrogen sulde. In terms of manure
management, odors increase as the animal manure decomposes (Cole et al., 2000). H2S creates a very pungent and
noticeable sulfur odor. In addition to odor contributions from
NH3 and H2S emissions, feed composition also plays a direct
role in the quantity and intensity of the odors produced
(Gralapp et al., 2002). Although NH3 and H2S are abundant
odors in terms of concentrations in swine CAFOs, approximately 400 different odorous compounds have been identied
(Hamon et al., 2012).
Poultry Facilities
Poultry CAFOs include both broiler (chickens used for meat
production) and layer (chickens used for egg production) facilities. Broilers are typically produced in littered oor systems,
where birds are kept in a closed structure (termed a house)
with space to move and access to feed and water systems.
Bedding for broiler housing varies by geographical location,
but material can include rice hulls, wheat or rye hulls, sawdust
or wood shavings, peanut shells, sand, chopped straw, or corn
stalks. The bedding used in broiler houses is referred to as litter
when it is mixed with feces (USEPA, 2001). Most of the litter is
reused (also known as built-up litter) over multiple ocks of
production (CAST, 2011). Alternatively, caked litter (i.e., litter
that has a wet and hardened surface layer, usually found along
the feed and water lines where much of the manure is deposited) is removed between each ock (CAST, 2011; USEPA,
2001). Layer chickens are primarily raised in cage systems,
where the birds are housed in cages with a relatively limited
amount of space. These can either be in high-rise (HR) (65
70% of cage systems), or manure-belt (MB), (2530% of cage
systems) housing systems (CAST, 2011; Xin et al., 2010) but
alternative cage-free housing systems do exist and are increasingly popular. Manure in HR facilities is typically stored
in the lower level of the house for 1 year and removed as solid
manure in the fall for cropland application. Manure in MB
houses is removed daily to weekly, via the MB, and can be
stored either on-site, in separate storage, or a composting facility (Xin et al., 2010).
As with other livestock facilities, emissions vary depending
on housing and manure management systems. Although a
substantial amount of research has been performed to determine air quality emissions associated with on-site production
and storage of manure, there is limited data on emissions
associated with land-applied poultry manure (a common
practice for poultry facilities). Air quality in poultry CAFOs is
an area of concern; however, most research is on NH3, whereas
data on other air pollutants, such as PM and VOCs is limited.
Mitigation techniques in poultry facilities are utilized
mainly by manure management. Dietary manipulation (Roberts
et al., 2007), topical application of chemical or mineral
additives to poultry manure (Li et al., 2008), treatment of exhaust air via a biolter or wet scrubber (Melse and Ogink,
2005; Manuzon et al., 2007; Shah et al., 2008), and faster
application of land-applied manure have been investigated as
possible mitigation techniques to minimizing emissions associated with manure from poultry CAFOs. Through direct
incorporation, or injection, of manure into soil with immediate tillage there is the potential to minimize emissions from
land-applied manure (CAST, 2011). Injection of manure
during land application can minimize odors, NH3, and VOC
emissions. In layer facilities specically the use of MB systems
should be used for manure management because they signicantly reduce odors and NH3 emissions (Fournel et al.,
2012).
Ammonia
Among both layer and broiler CAFOs, NH3 is the major
noxious gas produced. The primary source of NH3 from
poultry is from manure, both in-house and off-site. Manure
excreted from poultry has a high MC and as the moisture
evaporates, NH3 is emitted (USEPA, 2001). The generation
and concentration of indoor NH3 is inuenced by housing and
manure management practices, as with other livestock CAFOs.
Broiler manure storage is in-house, so continuous airow from
ventilation systems is used to help minimize the amount of
NH3 exposure for animals, as NH3 is emitted year round
(USEPA, 2001). However, this does not minimize NH3 emissions; rather it likely leads to elevated emissions of NH3 to the
atmosphere (CAST, 2011). Manure management in layer
housing systems that utilize manure belts allows manure to
dry to between 30% and 60% MC, making it easier to transport and creating less NH3 emissions (Xin et al., 2010). Ammonia concentrations in MB housing are generally lower than
in other housing systems (Green et al., 2009) due to the higher
frequency of manure removal (Green et al., 2009). Long-term
broiler manure storage with high MC can further mineralize
organic nitrogen to NH3 (USEPA, 2001). Though only a small
amount of research has been performed in regard to landapplied poultry manure, NH3N losses from land-applied
poultry manure (expressed as a percentage of manure nitrogen
content) have been estimated at 7% for dry laying-hen manure
(Lockyer and Pain, 1989), 41.5% for wet laying-hen manure
(Lockyer and Pain, 1989), and 25.1% for broiler litter (Cabera
et al., 1994). Prolonged exposure to elevated NH3 concentrations adversely affects bird health, such as the respiratory
system and productivity (e.g., feed intake, bodyweight gain,
egg production, and feed conversion) (CAST, 2011). For
poultry housing, the recommended indoor NH3 concentration
is less than 25 ppm (MidWest Plan Service, 1990; United Egg
Producers, 2010).
Hydrogen Sulde
With dry manure collection from poultry and the associated
manure storage facilities, any sulfur excreted should be oxidized to nonvolatile sulfate, thus making H2S production
negligible (USEPA, 2001). Hydrogen sulde emissions are
varied because of MC, the time manure stays in the facility, the
289
Odor
Odor associated with poultry is often a result of manure and
the most noxious odor has been identied as ammonia (CAST,
2011). Although there is odor associated with poultry CAFOs,
its incidence is much less than that of swine facilities and is
produced at constant concentrations throughout the day (Zhu
et al., 2000). In layer facilities the use of MB systems, both
forced air drying and natural drying, reduces odor emissions,
respectively, by 37% and 42% compared with odor emissions
from a deep-pit technique (Fournel et al., 2012). MB systems
also produce less odor than deep-pit systems due to their
frequent manure removal (Fournel et al., 2012). Odor incidence in poultry increases as a result of higher temperatures
during summer months, and odor varies depending on the age
of birds and the season (Fournel et al., 2012; Hayes et al.,
2006). Odor from broiler facilities is associated with litter and
worsens when the litter is damp (Hayes et al., 2006). Broiler
house odors of the same concentration are perceived as more
intense than odors emitted from pig slurry and there is a
greater correlation between poultry manure odor intensity and
290
concentration than in swine (Misselbrook et al., 1993). Composting of litter also produces odor as organic compounds can
be volatilized during composting (Turan et al., 2007).
Conclusion
As the global human population rises and the degree of afuence in developing nations grows, people demand more food
and in particular more high quality animal protein. This demand for protein requires intensication of animal facilities in
order to maximize production on limited land. CAFOs have
become the main mode for efcient animal production in the
US. However, the high stocking density of CAFOs leads to
greater amounts of air pollutants and a rise in associated concerns. Additionally, manure and feed storage and management
have been a recurring contributor to air quality issues in all three
CAFOs. Dairy, beef, swine, and poultry CAFOs all emit NH3,
H2S, VOCs, and odors, and these air pollutants can impact
human and animal health. Numerous approaches to mitigate
emissions are currently being studied and include improvements of animal production efciency, herd health, nutrition,
and feed production, as well as manure management strategies.
References
Alanis, P., Ashkan, S., Krauter, C., Campbell, S., Hasson, A.S., 2010. Emissions of
volatile fatty acids from feed at dairy facilities. Atmospheric Environment 44,
50845092.
Alanis, P., Sorenson, M., Beene, M., et al., 2008. Measurement of non-enteric
emission uxes of volatile fatty acids from a California dairy by solid phase
micro-extraction with gas chromatography/mass spectrometry. Atmospheric
Environment 42, 64176424.
American Society of Agricultural and Biological Engineers (ASABE), 2006. Air quality
and emissions from livestock and poultry production/waste management systems.
In: Rice, J.M., Caldwell, D.F., Humenik, F.J. (Eds.), Animal Agriculture and the
Environment: National Center for Manure and Animal Waste Management White
Papers. St. Joseph, Michigan: ASABE, pp. 140.
Amon, B., Kryvoruchko, V., Amon, T., Zechmeister-Boltenstern, S., 2006. Methane,
nitrous oxide and ammonia emissions during storage and after application of
dairy cattle slurry and inuence of slurry treatment. Agriculture, Ecosystems, &
Environment 112, 153162.
Aneja, V.P., Schlesinger, W.H., Erisman, J.W., 2009. Effects of agriculture upon the
air quality and climate: Research, policy, and regulations. Environmental Science
& Technology 43, 42344240.
Arogo, J., Westerman, P.W., Heber, A.J., 2003. A review of ammonia emissions
from conned swine feeding operations. Transactions of the ASAE 46, 805817.
Bicudo, J.R., Schmidt, D.R., Powers, W., et al., 2002. Odor and VOC emissions
from swine manure storages. In: Proceedings of Odor and Toxic Air Emissions,
Water Environment Federation, 2002, pp. 123135. Albuquerque, New Mexico:
WEF.
Bluteau, C.V., Masse, D.I., Leduc, R., 2009. Ammonia emission rates from dairy
livestock buildings in eastern Canada. Biosystems Engineering 103, 480488.
de Boer, I.J.M., 2003. Environmental impact assessment of conventional and organic
milk production. Livestock Production Science 80, 6977.
de Boer, I.J.M., Cederberg, C., Eady, S., et al., 2011. Greenhouse gas mitigation in
animal production: Towards an integrated life cycle sustainability assessment.
Current Option in Environmental Sustainability 3, 423431.
Boylan, J.W., Odman, M.T., Wilkinson, J.G., Russell, A.G., 2006. Integrated
assessment modeling of atmospheric pollutants in the southern Appalachian
Mountains: Part II. Fine particulate matter and visibility. Journal of Air Waste
Management Association 56, 1222.
Burgos, S.A., Embertson, N.M., Zhao, Y., et al., 2010. Prediction of ammonia
emission from dairy cattle manure based on milk urea nitrogen: Relation of milk
urea nitrogen to ammonia emissions. Journal of Dairy Science 93, 23772386.
Bussink, D.W., Oenema, O., 1998. Ammonia volatilization from dairy farming
systems in temperate areas: A review. Nutrient Cycling in Agroecosystems 51,
1933.
Cabera, M.L., Chiang, S.C., Merka, O.C., Pancorbo, O.C., Thompson, S.C., 1994.
Pelletizing and soil water effects on gaseous emission from surface-applied
poultry litter. Soil Science Society of America Journal 58, 807811.
Cambra-Lopez, M., Aarnink, A.J.A., Zhao, Y., Calvet, S., Torres, A.G., 2010.
Airborne particulate matter from livestock production systems: A review of an air
pollution problem. Environmental Pollution 158, 117.
Carter, W.P.L., 1994. Development of ozone reactivity scales for volatile organic
compounds. Journal of Air & Waste Management 44, 881899.
Chung, M.Y., Beene, M., Ashkan, S., Krauter, C., Hasson, A.S., 2010. Evaluation of
non-enteric sources of non-methane volatile organic compound (NMVOC)
emissions from dairies. Atmospheric Environment 44, 786794.
Cole, D., Todd, L., Wing, S., 2000. Concentrated swine feeding operations and
public health: A review of occupational and community health effects.
Environmental Health Perspective 108, 685699.
Council for Agricultural Science and Technology (CAST), 2011. Air Issues
Associated with Animal Agriculture: A North American Perspective. Ames, Iowa:
CAST. Issue Paper 47.
Davis, J.G., Stanton, T.L., Haren, T., 2002. Management: Feedlot Manure
Management. Fort Collins, CO: Colorado State University Cooperative Extension.
Dewes, T., 1999. Ammonia emissions during the initial phase of microbial
degradation of solid and liquid cattle manure. Bioresource Technology 70,
245248.
Donham, K.J., Scallon, L.J., Popendorf, W., Treuhaft, M.W., Roberts, R.C., 1986.
Characterization of dusts collected from swine connement buildings. American
Industrial Hygiene Association Journal 47, 404410.
Drummond, J.G., Curtis, S.E., Simon, J.S., Norton, H.W., 1980. Effects of aerial
ammonia on growth and health of young pigs. Journal of Animal Science 50,
10851091.
Duchaine, C., Grimard, Y., Cormier, Y., 2000. Inuence of building maintenance,
environmental factors, and seasons on airborne contaminants of swine
connement buildings. American Industrial Hygiene Association Journal 61,
5663.
Fangmeier, A., Hadwiger-Fangmeier, A.L., Van der Eerden, L., Jger, H.J., 1994.
Effects of atmospheric ammonia on vegetation A review. Environmental
Pollution 86, 4382.
Faulkner, W.B., Shaw, B.W., 2008. Review of ammonia emission factors for United
States animal agriculture. Atmospheric Environment 42, 65676574.
Filipy, J., Rumburg, B., Mount, G., Westberg, H., Lamb, B., 2006. Identication and
quantication of volatile organic compounds from a dairy. Atmospheric
Environment 40, 14801494.
Fournel, S., Pelletier, F., Godbout, S., Lagac, R., Feddes, J.J.R., 2012. Odour
emissions, hedonic tones and ammonia emissions from three cage layer housing
systems. Biosystems Engineering 112, 181191.
Gralapp, A.K., Powers, W.J., Faust, M.A., Bundy, D.S., 2002. Effects of dietary
ingredients on manure characteristics and odorous emissions from swine.
Journal of Animal Science 80, 15121519.
Green, A.R., Wesley, I., Trampel, D.W., Xin, H., 2009. Air quality and hen health
status in three types of commercial laying hen houses. Journal of Applied
Poultry Research 18, 605621.
Groot Koerkamp, P.W.G., Metz, J.H.M., Uenk, G.H., et al., 1998. Concentrations and
emissions of ammonia in livestock buildings in Northern Europe. Journal of
Agricultural Engineering Research 70, 7995.
Hamon, L., Andres, Y., Eric, D., 2012. Aerial pollutants in swine buildings: A review
of their characterization and methods to reduce them. Environmental Science &
Technology 46, 1228712301.
Hayes, E.T., Curran, T.P., Dodd, V.A., 2006. Odour and ammonia emissions from
intensive poultry units in Ireland. Bioresource Technology 97, 933939.
Heber, A.J., Lim, T.T., Tao, P.C., Ni, J.Q., 2004. Control of air emissions from
swine nishing buildings ushed with recycled lagoon efuent. In the 2004
ASAE/CSAE Annual International Meeting. Ottawa, ON: ASAE.
Heber, A.J., Ni, J.Q., Lim, T.T., et al., 2000. Effect of a manure additive on ammonia
emission from swine nishing buildings. Transactions of the ASABE 43,
18951902.
Heber, A.J., Tao, P., Ni, J.Q., Lim, T.T., Schmidt, A.M., 2005. Air emissions
from two swine nishing buildings with ushing: Ammonia characteristics.
Livestock Environment VII Proceedings 7th International Symposium. Beijing,
China: ASAE.
Hobbs, P.J., Webb, J., Mottram, T.T., Grant, B., Misselbrook, T.M., 2004. Emissions
of volatile organic compounds originating from UK livestock agriculture. Journal
of the Science of Food and Agriculture 84, 14141420.
Howard, C., Kumar, A., Mitloehner, F.M., et al., 2010b. Direct measurements of the
ozone formation potential from livestock and poultry waste emissions.
Environmental Science and Technology 44, 22922298.
Howard, C.J., Kumar, A., Malkina, I.A., et al., 2010a. Reactive organic gas
emissions from livestock feed contribute signicantly to ozone production
in central California. Environmental Science and Technology 44, 2309
2314.
Jacobson, L.D., Heber, A.J., Hoff, S.J., et al., 2006. Aerial emissions from conrmed
animal buildings. In: Proceedings of the Workshop on Agricultural Air Quality:
State of the Science, pp. 775784. Washington, DC, USA: Agricultural Air
Quality.
James, T., Meyer, D., Esparza, E., DePeters, E.J., Perez-Monti, H., 1999. Effects of
dietary nitrogen manipulation on ammonia volatilization from manure from
Holstein heifers. Journal of Dairy Science 82, 24302439.
Kroodsma, W., Huis in't Veld, J.W.H., Scholtens, R., 1993. Ammonia emissions and
its reduction from cubicle house by ushing. Livestock Production Science 35,
293302.
Krupa, S.V., 2003. Effects of atmospheric ammonia (NH3) on terrestrial vegetation: A
review. Environmental Pollution 124, 179221.
Leneman, H., Oudendag, D.A., van der Hoek, K.W., Janssen, P.H.M., 1998. Focus
on emissions factors: A sensitivity analysis of ammonia emission modelling in
the Netherlands. Environmental Pollution 102, 205210.
Li, H., Xin, H., Burns, R.T., Liang, Y., 2008. Reduction of ammonia emission from
stored poultry manure using additives: Zeolite, Al+clear, Ferix-3 and PLT.
Journal of Applied Poultry Research 17, 421431.
Lim, T.T., Heber, A.J., Ni, J.Q., 2003. Air quality measurements at a laying hen
house: Odor and hydrogen sulde emissions. In: International Symposium on
Control of Gaseous and Odor Emissions from Animal Production Facilities,
Horsens, Denmark, pp. 273282. Foulum, Denmark: Danish Institute of
Agricultural Sciences.
Lockyer, D.R., Pain, B.F., 1989. Ammonia emission from cattle, pig, and poultry
wastes applied to pasture. Environmental Pollution 56, 1930.
Mackie, R.I., Stroot, P.G., Varel, V.H., 1998. Biochemical identication and
biological origin of key odor components in livestock waste. Journal of Animal
Science 76, 13311342.
Madden, N.M., Southard, R.J., Mitchell, J.P., 2008. Conservation tillage reduces
PM10 emissions in dairy forage rotations. Atmospheric Environment 42,
37953808.
Malkina, I.L., Kumar, A., Green, P.G., Mitloehner, F.M., 2011. Identication of
volatile organic compounds emitted from dairy silages and other feedstuffs.
Journal of Environmental Quality 40, 2836.
Manuzon, R.B., Zhao, L.Y., Keener, H.M., Darr, M.J., 2007. An acid spray wet
scrubber for absorbing ammonia emissions from exhaust fans of animal
buildings. Transactions of the ASABE 50, 13951407.
Marini, J.C., Van Amburgh, M.E., 2005. Partition of nitrogen excretion in urine and
the feces of Holstein replacement heifers. Journal of Dairy Science 88,
17781784.
Melse, R.W., Ogink, N.W.M., 2005. Air scrubbing techniques for ammonia and odor
reduction at livestock operations: Review of on-farm research in the Netherlands.
Transactions of the ASABE 48, 23032313.
Midwest Plan Service, 1990. Mechanical Ventilating Systems for Livestock Housing.
Ames, Iowa: Iowa State University.
Misselbrook, T.H., Clarkson, C.R., Pain, B.F., 1993. Relationship between
concentration and intensity of odours for pig slurry and broiler houses. Journal
of Agricultural Engineering Research 55, 163169.
Mitloehner, F.M., Calvo, M.S., 2008. Worker health and safety in concentrated
animal feeding operations. Journal of Agricultural Safety and Health 14,
163187.
National Research Council (NRC), 2003. Air Emissions from Animal Feeding
Operations: Current Knowledge, Future Needs. Washington, DC: National
Academies Press.
Ni, J., Chai, L., Chen, L., et al., 2012. Characteristics of ammonia, hydrogen sulde,
carbon dioxide, and particulate matter concentrations in high-rise and manurebelt layer hen houses. Atmospheric Environment 57, 165174.
Pain, B.F., Clarkson, C.R., Phillips, V.R., et al., 1991. Odour emission arising from
application of livestock slurries on land: Measurements following spreading
291
292
Zahn, J.A., Hateld, J.L., Liard, D.A., et al., 2001. Functional classication of swine
manure management systems based on efuent and gas emissions
characteristics. Journal of Environmental Quality 30, 635647.
Zhu, J., Jacobson, L., Schmidt, D., Nicolai, R., 2000. Daily variations in odor and
gas emissions from animal facilities. Applied Engineering in Agriculture 16,
153158.
Relevant Websites
http://cfpub.epa.gov/npdes/home.cfm?program_id=7
US Environmental Protection Agency.
http://www.epa.gov/airquality/particlepollution/
US Environmental Protection Agency.
doi:10.1016/B978-0-444-52512-3.00088-7
293
294
Methane
Nitrous oxide
F-gases
(a)
Africa
Americas
Asia
Europe
Oceania
(b)
Figure 1 (a) Total global greenhouse gas emissions in 2004 and (b) global emissions from agriculture between 2000 and 2010 (FAO, 2012).
F-gases, uorinated gases. Reproduced from Food and Agriculture Organisation's Statistical Database; FAOSTAT. Rome. Reproduced from data
reported by the IPCC (2007). Summary for policymakers. In: Solomon, S., Qin, D., Manning, M., et al. (Eds.), Climate Change 2007: The Physical
Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge,
UK and NY, USA: Cambridge University Press.
(FAO, 2012). This has grown by 13% over the two decades
between 1990 and 2010. However, the rate of growth has been
highly uneven, with strong growth in emissions from agriculture from non-Annex 1 countries (including Asia and South
America), occurring at the same time as Annex 1 countries
(that includes North America and Europe) showed a small
decline in emissions (Figure 2).
Reporting
The reporting of emissions of greenhouse gases from agriculture and other emission sources is guided by methodologies developed by the IPCC (2006). In accordance with
295
g CO2e 1015
3
Annex l countries
Non-Annex l countries
World
0
1990
1995
2000
2005
2010
Figure 2 The changes in emissions of total greenhouse gases from agriculture at a global scale between 1990 and 2010. Annex I, North America
and Europe; Non-annex I, Asia and South America. Reproduced from FAO, 2012. Food and Agriculture Organisation's Statistical Database,
FAOSTAT. Rome. Available at: http://faostat3.fao.org/ (accessed 24.01.14).
Nitrous Oxide
Measurement/modeling
Nature of Gas
296
5000
4500
4000
3500
kt N2O
3000
Soils
2500
Manure management
Waste burning
2000
1500
1000
500
0
1970
1975
1980
1985
1990
1995
2000
2005
Figure 3 Global emissions of nitrous oxide from agriculture between 1970 and 2008, partitioned by source. Reproduced from European
Commission, Joint Research Centre (JRC)/Netherlands Environmental Assessment Agency (PBL), 2011. Emission Database for Global Atmospheric
Research (EDGAR), release version 4.2. Available at: http://edgar.jrc.ec.europa.eu (accessed 24.01.14).
297
N2
N2O
Fixation
NH3
Decomposition
Organic N
Uptake
NH4+
Mineralisation
NO3
Denitrification
Leaching
Nitrification
Figure 4 A simplied schematic diagram of N cycling in agricultural systems. Nitrogen pools are represented by the purple boxes and processes
are indicated by the light blue boxes.
298
5.00
4.50
4.00
3.50
USA
China
UK
India
Japan
Kenya
3.00
2.50
2.00
1.50
1.00
0.50
0.00
1970
1975
1980
1985
1990
1995
2000
2005
Year (19702005)
Figure 5 Comparison of N2O emissions for different nations relative to 1970. levels. Reproduced from European Commission, Joint Research
Centre (JRC)/Netherlands Environmental Assessment Agency (PBL), 2011. Emission Database for Global Atmospheric Research (EDGAR), release
version 4.2. Available at: http://edgar.jrc.ec.europa.eu (accessed 24.01.14).
Mitigation
Mitigation options for N2O emissions generally aim to increase the efciency with which fertilizer N is used by crops
and thereby reduce the potential for losses. This can be
achieved by improving soil conditions, for example, by improved drainage and soil structure. Other approaches focus on
reducing the presence of available N in soils by altering the
timing of fertilizer applications to better match crop demand
or by reducing overall N inputs. The use of a winter crop cover
and species introductions can also help to reduce emissions by
making more efcient use of added N. Legumes offer an important opportunity to reduce greenhouse gas emissions, because they are able to x atmospheric nitrogen biologically
and release less N2O than fertilizer nitrogen. Another interesting approach has been to use inhibitors that slow down the
nitrication process and therefore have the potential to both
reduce N2O production and increase crop N uptake. Although
such additives are expensive, they have been widely used in
New Zealand to reduce N2O emissions and increase fertilizeruse efciency.
Demand side measures also have the potential to reduce
N2O emissions, because meat consumption is strongly linked
to N2O production. Improved efciency of the food system
and avoiding food loss and wastage are viable options which
could substantially reduce emissions. To assess both the potential magnitude of results as well as the cost of different
mitigation options, marginal abatement cost curves can be
utilized (MacLeod et al., 2010). Different mitigation
Methane
Nature of the Gas
Methane (CH4) is a principal component of natural gas. It is a
simple molecule that consists of four hydrogen and one carbon atom, and at 1.8 ppm, it is the most abundant non-CO2
greenhouse gas in todays atmosphere (Montzka et al., 2011).
Methane is a powerful greenhouse gas with a global warming
potential 25 times greater than that of CO2, and it plays a
central role in tropospheric chemistry. Like N2O, concentrations of CH4 have increased signicantly in recent decades
(Figure 6). However, unlike N2O, CH4 is produced by a much
wider variety of sources. Methane is relatively stable in the
atmosphere and remains there for approximately 915 years.
Sources
A major source of CH4 emissions from agriculture is the enteric fermentation of ruminant livestock (IPCC, 2007). In
domesticated ruminant livestock, CH4 is generated as a result
of the complex microbiological fermentation in the rumen
and the large intestine and is released via the mouth or nostrils. The process of enteric fermentation is a microbial
299
120
100
Mt methane
80
60
40
20
0
1970
1975
1980
1985
1990
1995
2000
Agricultural soils
Manure management
Enteric fermentation
Biomass burning
2005
Figure 6 Global methane emissions from agricultural sources apportioned by source between 1970 and 2008.
Sinks
Once methane is released, it is removed from the atmosphere
by atmospheric consumption processes or sinks. The amount
of CH4 released and removed ultimately determines atmospheric CH4 concentrations and thus how many years they will
remain in the atmosphere. Global CH4 sinks arise primarily
from the oxidation by chemical reaction with hydroxyl radicals
(OH) in the atmosphere (IPCC, 2007). In the tropospheric
layer of the atmosphere, CH4 reacts with OH to produce CH3
and water.
Methane is also removed from the atmosphere (though in
smaller amounts) through stratospheric oxidation. From both
processes, small amounts of CH4 are destroyed by reacting
with the OH in the atmosphere, and this accounts for approximately 90% of methane removal from the atmosphere
(IPCC, 2007). Other CH4 sinks include the microbial uptake
in soils as well as reaction with chlorine atoms in the atmosphere. These sinks contribute an estimated 7% and 2% of the
total methane removal, respectively.
300
Growth Rate
Records of ice sheets indicate that CH4 is more abundant in
the earths atmosphere now than at any time during the past
400 000 years (IPCC, 2007). Global average atmospheric
concentrations of CH4 have increased since 1750, from approximately 700 to 1745 parts per billion by volume (ppbv) in
1998, which equates to a 150% increase. Since 1998, CH4
emissions have increased, but the overall rate of CH4 growth
has reduced. A recent study by Bergamaschi et al. (2010),
highlights that atmospheric CH4 has been at a relatively steady
state of 1751 ppbv between 1999 and 2002. The IPCC (2007)
estimated that CH4 emissions increased by approximately
17% between 1990 and 2005, with an average annual increase
of 58 Mton CO2 equivalents per year.
Anthropogenic sources account for less than half global
CH4 emissions; however, they are the primary driver in
emission growth. Agriculture is the largest man-made source of
CH4, which contributes approximately 43% toward total anthropogenic emissions of CH4 (Cloy et al., 2012). This can be
accounted for by an increase in population pressure (also an
increase in demand for food, hence more meat and dairy
products), technological change, public policy, and economic
growth (increased gross domestic product particularly in some
developing countries) (IPCC, 2007). These emissions mainly
derive from large sources such as enteric fermentation by ruminant animals (25%) and rice cultivation (12%), with minor
contributions from animal waste (3%) and savannah (biomass) burning (3%) (Cloy et al., 2012).
Future projections highlight the potential for further increases in CH4 emissions. For example, the Food and Agriculture Organization has estimated that if emissions increase
in proportion to increases in livestock numbers, then global
livestock-related methane production is expected to increase
by up to approximately 60% (Steinfeld et al., 2006). This
prediction is feasible, particularly in developing countries such
as South America, as cattle population has increased from 176
to 379 M head between 1961 and 2004 (IPCC, 2007). Further,
all other livestock categories have increased in the order of 30
600% since 1961, which has been primarily due to food demand and is projected to increase further in the future years.
The USEPA (2006) predicts that combined CH4 emissions
from enteric fermentation and manure management will increase by 21% between 2005 and 2020.
Mitigation
Opportunities for mitigating CH4 emissions include effective
management of livestock, as more efcient use of feeds often
reduces amounts of CH4 produced (Clemens and Ahlgrimm,
2001). More intensive feeding regimes with a carefully tailored
feed (e.g., augmenting the volume of starches in the diet
greatly reduces CH4) and high-quality forage management
practices (e.g., livestock grazing on mixed alfalfa-grass pasture)
can reduce per capita emissions by up to 50% (Thorpe, 2009).
One strategy for reducing methane emissions is to inhibit the
production of methanogenesis within the animal husbandry
system. Such options include the application of ionophores,
methane oxidizers, and probiotics (Thorpe, 2009). However,
this method is unlikely on its own to achieve signicant
mitigation of emissions, may prove uneconomic in the long
term (Patra, 2012), and is currently outlawed in the EU. One
of the most straightforward CH4 emissions mitigation opportunities occurs as a consequence of herd reduction, although a less drastic option involves genetic selection and the
use of breeds with lower CH4 emissions (Thorpe, 2009; Bell
et al., 2011). The developed world has seen a general decline in
herd numbers over the past 20 years. This is a result of increasing concerns over meat consumption and health scares,
coupled with concerns over the nature of production (ibid,
2008). Strategies to mitigate emissions from rice cultivation
include draining the wetland twice during the growing season,
as this can effectively reduce CH4 release from 10% to 80%
(Smith et al., 2008). Kai et al. (2011) found that changes in
agricultural practices such as new high-yield rice species, coupled with greater application of fertilizers, often require shorter
inundation periods which, in turn, can reduce CH4 emissions.
Carbon Dioxide
Nature of Gas
301
Atmosphere
597 + 165
120
0.2
119.6
2.6
GPP
Weathering Respiration
Land
sink
1.6
Land
use
change
6.4
70.6 70
22.2 20
Vegetation,
soil and detritus
2300 + 101140
0.4
Fossil fuels
3700 244
0.8
Rivers
Surface ocean
900 + 18
Weathering
0.2
90.2
101
50
39
Marine biota
3
1.6
11
Intermediate
and deep ocean
37 100 + 100
0.2
Reservoir sizes in GtC
Fluxes and rates in GtC yr1
Surface sediment
150
Figure 7 The global carbon cycle (IPCC 2007). Figures in black represent natural processes and pools, whereas those in red represent the
contribution of anthropogenic inuences. GPP, gross primary production (http://www.ipcc.ch/graphics/ar4-wg1/jpg/g-7-3.jpg, with permission
from IPCC).
Cycling (Source/Sink)
Carbon moves naturally between land, oceans, and atmosphere
via the carbon cycle (Figure 7). The timescales for carbon
transformation vary greatly from seconds, such as during xation of CO2 via photosynthesis, to more than millions of
years, as in the case of fossil carbon formation. Not only are
humans responsible for emitting large amounts of greenhouse
gases into the atmosphere through the combustion of fossil
fuels, but soils also make a signicant contribution. The proportion of greenhouse gas emissions from different sectors illustrates that CO2 emissions directly attributable to agriculture
are relatively small, but agriculture, together with land-use
change, contributes to almost one-third of global emissions.
Despite this large loss of CO2, there is the ability to use land as
a means of reducing atmospheric CO2 levels by sequestering it
in soils. This brings the additional benet of improved soil
quality from organic matter, leading to enhanced agricultural
production. Agriculture and forestry are unique in that they can
provide both a source and a sink for CO2.
The two main sources of CO2 associated with agriculture are
the relatively small contribution made by the use of fossil fuels
and land-use change. Fossil fuels are needed in agriculture as
fuel for farming machinery, in the manufacture of agricultural
equipment, and during the production of agrochemicals. Fossil
fuel use in agriculture is low in relation to societies overall
302
380
360
March 2013
340
320
1960
1970
1980
1990
2000
2010
Year
Figure 8 The carbon dioxide data (red curve), measured as the mole fraction in dry air, on Mauna Loa. The black curve represents the seasonally
corrected data (www.esrl.noaa.gov/gmd/ccgg/trends/ (accessed 01.07.13)).
Growth Rate
Measurements of atmospheric CO2 concentrations are very reliable and have demonstrated a long period of annual increase
in atmospheric CO2 concentrations. However, there are uncertainties in the accuracy and quantication of terrestrial and
oceanic CO2 sinks. Growth rates in atmospheric CO2 concentrations have been recorded in Mauna Loa in the Pacic Ocean
since 1958 and were initiated by C. David Keeling of the Scripps
Institution of Oceanography in March of 1958 at a facility of the
National Oceanic and Atmospheric Administration (Keeling
et al., 1976). They show a continuous increase from less than
320 ppm in 1958 to nearly 400 ppm in 2013 (Figure 8). Since
1958, the average rate of increase in the atmospheric concentration of CO2 has been approximately 1 ppm per year (2 PgC
per year). In 2005, the atmospheric CO2 concentration was
approximately 380 ppm, which is an increase of approximately
35% since preindustrial times. Between 1959 and 2008, 43% of
each years CO2 emissions remained in the atmosphere (Le
Quere et al., 2009). However, in recent years, this amount has
been thought to have risen to up to 45% due to climate change
effects. Increasing CO2 concentrations correlate well with fossil
fuel combustion and land-use change patterns.
2011. Australia, Spain, Russia, and Canada experienced increases of 8%, 2%, 1%, and 7%, respectively. Economies
in Transition countries also experienced an increase in emissions such as in Ukraine, where emissions increased by 7%.
Total CO2 emissions for all industrialized countries that had
quantitative greenhouse gas mitigation targets under the Kyoto
Protocol decreased in 2011 by 0.7%. Figure 4 shows CO2
emissions per capita from combustion of fossil fuels and cement production of the top 5 emitting countries in 2011.
China and the European Union have similar per capita
emissions.
Mitigation
Reducing increases in atmospheric CO2 accumulation as a
result of agriculture and land-use change requires a commitment to avoiding land-use change that will release large
amounts of soil carbon. In particular, this must address deforestation, cultivation of pasture, and degradation of peaty
and organic soils. Such actions would help to avoid the increases in atmospheric CO2 that have been a characteristic of
the past century of human development; however, this also
requires recognition of the range of functions that land supports in addition to food production.
The management of agricultural soils also provides an opportunity to increase the quantities of carbon stored in soils that
are used on a continuous basis for agricultural production.
These include improved nutrient management, reduced tillage,
improved agronomy, the use of composts and manures,
improved rotations, and bioenergy crops. The efciency of different management options varies according to climate and
baseline agricultural practices; however, it has been estimated
that in Europe, there is a potential through improved agricultural management to sequester between 90 and 120 Mton
carbon per year, with benets in terms of greenhouse gas
mitigation and improved soil quality (Smith, 2004).
Conclusions
Agriculture, and the land use associated with agricultural
production systems, contributes signicantly to global greenhouse gas emissions. Most emissions are associated with N2O
emissions from N fertilizers and manures and from CH4
emissions from ruminant livestock and rice cultivation. A
smaller amount of emission is also associated with CO2 loss
from soils converted into croplands from forests and pastures.
There is an urgent need to improve the efciency of farming
systems in order to ensure that productivity is maintained or
increased at the same time as their environmental impact
(particularly greenhouse gas emissions) are reduced. Many
management options are available to reduce the emissions of
individual greenhouse gases in the crop and livestock
sectors. The implementation of such management practices
alongside protection of forests and permanent pasture from
conversion to croplands can be expected to signicantly
reduce emissions of greenhouse gases from the agriculture and
land-use sectors.
303
References
Andres, R.J., Boden, T.A., Breon, F.M., et al., 2012. A synthesis of carbon dioxide
emissions from fossil-fuel combustion. Biogeosciences 9, 18451871.
Bell, M., Wall, E., Simm, G., Russell, G., 2011. Effects of genetic line and feeding
system on methane emissions from dairy systems. Animal Feed Science and
Technology 16667, 699707.
Bergamaschi, P., Krol, M., Meirink, J., et al., 2010. Inverse modeling of European
CH(4) emissions 20012006. Journal of Geophysical Research Atmospheres
115.
Butterbach-Bahl, K., Gundersen, P., Ambus, P., et al., 2011. The European nitrogen
assessment: Sources, effects and policy perspectives. In: Sutton, M.A., Howard,
C.M., Erisman, J.W., et al. (Eds.), Nitrogen Processes in Terrestrial Ecosystems.
Cambridge, UK: Cambridge University Press, pp. 99125.
Clemens, J., Ahlgrimm, H.J., 2001. Greenhouse gases from animal
husbandry: Mitigation options. Nutrient Cycling in Agroecosystems 60,
287300.
Cloy, J.M., Rees, R.M., Smith, K.A., et al., 2012. Impacts of agriculture upon
greenhouse gas budgets. Environmental Impacts of Modern Agriculture 34,
5782.
Erisman, J.W., Sutton, M., Galloway, J.N., Klimont, Z., Winiwarter, W., 2008. How a
century of ammonia synthesis changed the world. Nature Geoscience 1,
636639.
FAO, 2012. Food and Agriculture Organisations Statistical Database; FAOSTAT.
Rome. Available at: http://faostat3.fao.org/ (accessed 24.01.14).
Global Carbon Project, 2012. Available at: http://www.globalcarbonproject.org/
(accessed 24.01.14).
Godfray, H.C.J., Beddington, J.R., Crute, I.R., et al., 2010. Food security: The
challenge of feeding 9 billion people. Science 327, 812818.
Houghton, R.A., 2003. Revised estimates of the annual net ux of carbon to the
atmosphere from changes in land use and land management 18502000. Tellus
Series B-Chemical and Physical Meteorology 55, 378390.
IPCC, 2006. IPCC Guidelines for National Greenhouse Gas Inventories; Prepared by
the National Greenhouse Gas Inventories Programme. Japan: IPCC.
IPCC, 2007. Summary for policymakers. In: Solomon, S., Qin, D., Manning, M.,
et al. (Eds.), Climate Change 2007: The Physical Science Basis. Contribution
of Working Group I to the Fourth Assessment Report of the Intergovernmental
Panel on Climate Change. Cambridge, UK and NY, USA: Cambridge University
Press.
Jones, S.K., Famulari, D., Di Marco, C.F., et al., 2011. Nitrous oxide emissions
from managed grassland: A comparison of eddy covariance and static chamber
measurements. Atmospheric Measurement Techniques 4, 21792194.
Kai, F.M., Tyler, S.C., Randerson, J.T., Blake, D.R., 2011. Reduced methane growth
rate explained by decreased Northern Hemisphere microbial sources. Nature 476,
194197.
Keeling, C.D., Bacastow, R.B., Bainbridge, A.E., et al., 1976. Atmospheric carbon
dioxide variations at Mauna Loa Observatory, Hawaii. Tellus 28, 538551.
Le Quere, C., Raupach, M.R., Canadell, J.G., Marland, G., 2009. Trends
in the sources and sinks of carbon dioxide. Nature Geoscience 2, 831836.
Li, C.S., Frolking, S., Xiao, X.M., et al., 2005. Modeling impacts of farming
management alternatives on CO2, CH4, and N2O emissions: A case study for
water management of rice agriculture of China. Global Biogeochemical Cycles
19, 1036.
MacLeod, M., Moran, D., Eory, V., et al., 2010. Developing greenhouse gas
marginal abatement cost curves for agricultural emissions from crops and soils
in the UK. Agricultural Systems 103, 198209.
Montzka, S., Dlugokencky, E., Butler, J., 2011. Non-CO2 greenhouse gases and
climate change. Nature 476, 4350.
Mosier, A.R., Duxbury, J.M., Freney, J.R., Heinemeyer, O., Minami, K., 1998.
Assessing and mitigating N2O emissions from agricultural soils. Climatic Change
40, 738.
304
Patra, A.K., 2012. Enteric methane mitigation technologies for ruminant livestock: A
synthesis of current research and future directions. Environmental Monitoring and
Assessment 184, 19291952.
Peters, G.P., Marland, G., Le Quere, C., et al., 2012. Correspondence: Rapid growth
in CO2 emissions after the 20082009 global nancial crisis. Nature Climate
Change 2, 24.
Ravishankara, A., Daniel, J.S., Portmann, R.W., 2009. Nitrous Oxide (N2O): The
dominant ozone-depleting substance emitted in the 21st century. Science 326,
123125.
Reay, D.S., Davidson, E.A., Smith, K.A., et al., 2012. Global agriculture and nitrous
oxide emissions. Nature Climate Change advance online publication.
Rees, R.M., 2011. Global nitrous oxide emissions: Sources and opportunities for
mitigation. In: Guo, L., Gunasekara, A.S., McConnell, L.L. (Eds.), Understanding
Greenhouse Gas Emissions from Agricultural Management. Washington DC,
USA: American Chemical Society, pp. 257273.
Rees, R.M., Augustin, J., Nyamangara, J., 2012. Nitrous oxide emissions from
European agriculture; an analysis of variability and drivers of emissions from
eld experiments. Biogeosciences Discuss 9, 92599288.
Rees, R.M., Baddeley, J.A., Bhogal, A., et al., 2013. Nitrous oxide mitigation in UK
agriculture. Soil Science and Plant Nutrition 59, 315.
Robertson, G.P., Vitousek, P.M., 2009. Nitrogen in agriculture: Balancing the cost of
an essential resource. Annual Review of Environment and Resources 34, 97125.
Sauerbeck, D.R., 2001. CO2 emissions and C sequestration by agriculture
perspectives and limitations. Nutrient Cycling in Agroecosystems 60, 253266.
Smith, P., 2004. Carbon sequestration in croplands: The potential in Europe and the
global context. European Journal of Agronomy 20, 229236.
Smith, P., Martino, D., Cai, Z., et al., 2007. Policy and technological constraints to
implementation of greenhouse gas mitigation options in agriculture. Agriculture
Ecosystems & Environment 118, 628.
Smith, P., Martino, D., Cai, Z., et al., 2008. Greenhouse gas mitigation in
agriculture. Philosophical Transactions of the Royal Society B-Biological
Sciences 363, 789813.
Steinfeld, H., Gerber, P., Wassenaar, T., et al., 2006. Livestocks Long Shadow;
Environmental Issues and Options. Rome: FAO
Sutton, M.A., Howard, C.M., Erisman, J.W., et al., 2011. The European Nitrogen
Assessment; Sources, Effects and Policy Perspectives. Cambridge, NY:
Cambridge University Press
Thorpe, A., 2009. Enteric fermentation and ruminant eructation: The role (and
control?) of methane in the climate change debate. Climatic Change 93,
407431.
Tilman, D., Fargione, J., Wolff, B., et al., 2001. Forecasting agriculturally driven
global environmental change. Science 292, 281284.
USEPA, 2006. Global Mitigation of Non-CO2 Greenhouse Gases. Washington, DC:
EPA.
Relevant Website
http://www.epa.gov/climatechange/science/
United States Environmental Protection Agency.
Abbreviations
ABAP
2,2-Azobis(2-samidinopropane)
dihydrocholoride
ABTS
2,2-Azinobis-(3-ethylbenzothiazoline-6
sulfonic acid)
CAA
Cellular antioxidant activity
CVD
Cardiovascular disease
DCF
Dichlorouorescein
DCFH
2,7-Dichlorouorescin
DCFH-DA Dichlorouorescindiacetate
DPPH
2,2-Diphenyl-1-picrylhydrazyl radical
scavenging capacity
FCR
FolinCiocalteu reagent
Introduction
Previous epidemiologic studies have consistently shown that
diet plays a crucial role in the prevention of chronic diseases
(Temple, 2000; Willett, 1994). Consumption of fruits and
vegetables, as well as grains, has been strongly associated
with reduced risk of cardiovascular disease, cancer, diabetes,
Alzheimer disease, cataracts, and age-related functional decline
(Temple, 2000; Willett, 1994; Willett, 1995). This convincing
evidence suggests that a change in dietary behavior such as
increasing consumption of fruits, vegetables, and whole grains
is a practical strategy for signicantly reducing the incidence of
chronic diseases (Liu, 2003).
Phytochemicals are the bioactive nonnutrient plant compounds such as the carotenoids, avonoids, isoavonoids, and
phenolic acids in fruits, vegetables, whole grains, and other
plant foods. Thousands of phytochemicals have been identied in foods, yet there are still many that have not been
identied. They have been linked to reductions in the risk of
major chronic diseases (Liu, 2003). For example, phytochemicals may inhibit cancer cell proliferation, regulate inammatory and immune response, and protect against lipid
oxidation (Hollman and Katan, 1997; Liu, 2003). A major role
of the phytochemicals is the protection against oxidation
(Boyer and Liu, 2004).
Cells in humans and other organisms are constantly exposed to a variety of oxidizing agents, some of which are necessary for life. These agents may be present in air, food, and
water, or they may be produced by metabolic activities within
cells. The key factor is to maintain a balance between oxidants
and antioxidants to sustain optimal physiologic conditions in
the body. Overproduction of oxidants can cause an imbalance,
leading to oxidative stress (Liu and Hotchkiss, 1995). Oxidative stress can cause oxidative damage to large biomolecules
such as proteins, DNA, and lipids, resulting in an increased
FRAP
GAE
HAT
KMBA
ORAC
PSC
RMCD
SBC
SET
TEAC
TOSC
TRAP
USDA
doi:10.1016/B978-0-444-52512-3.00058-9
305
306
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
FolinCiocalteu Assay
The FolinCiocalteu (FC) assay is one of the most popular
assays for phenolic analysis (Singleton and Rossi, 1965;
Singleton et al., 1999). The principle of the FC assay is the
reduction of the FolinCiocalteu reagent (FCR) in the presence
of phenolics resulting in the production of molybdenum
tungsten blue that is measured spectrophotometrically at
760 nm and the intensity increases linearly with the concentration of phenolics in the reaction medium as described by
Swain and Hillis (1959).
The FCR (Folin and Ciocalteu, 1927) provides an improvement over the FolinDenis reagent with the addition of
lithium sulfate to the reagent. The lithium salts reduce the
amount of precipitate that can form when high concentrations
of reagent are used to increase the assay's reactivity.
The FC assay is simple and widely used to determine total
phenolics in fruits and vegetables (Chu et al., 2002; Dewanto
et al., 2002a,b; Sun et al., 2002; Vinson et al., 2001; Wolfe et al.,
2003; Liu et al., 2005; Sun and Liu, 2006).
The common protocol is performed according to Singleton
et al. (1999) with some modications according to Dewanto
et al. (2002a,b). Volumes of 0.5 ml of deionized water and
0.125 ml of diluted fruit extracts were added to a test tube.
FCR (0.125 ml) was added to the solution and allowed to
react for 6 min. Then, 1.25 ml of 7% sodium carbonate solution was aliquoted into the test tubes, and the mixture was
diluted to 3 ml with deionized water. The color was developed
after 90 min, and the absorbance was read at 760 nm.
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
Methods Description
The total avonoids method can be used in fruits, vegetables,
whole grains, dietary supplements, and nutraceutical products.
First, the quantitative methods of avonoids were based on
307
308
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
The principle of the SBC method to quantify total avonoids content is: avonoids with a 4-carbonyl group (avones,
avonols, avonones, avononols, and isoavonoids) were
reduced to avan-4-ols (catechins) using sodium borohydride
(Sweeny and Iacobucci, 1977a). This reaction was catalyzed by
the addition of aluminum chloride to achieve a high yield of
avan-4-ols. The avanols (catechins) were oxidized to
anthocyanins by chloranil in acetic acid solution (Sweeny and
Iacobucci, 1977b; Sweeny and Iacobucci, 1981; Jurd, 1966).
The anthocyanins generated in the reaction were quantied
spectrophotometrically at 490 nm after the addition of vanillin and concentrated hydrochloric acid (Sarkar and Howarth,
1976; Broadhurst and Jones, 1978).
The protocol for total avonoids test is performed according to the method described by He et al. (2008). Briey,
4 ml extracts of tested samples were added into test tubes, then
dried to dryness under nitrogen gas, and reconstituted in 1 ml
of THF/EtOH (1:1, v/v). Catechin standards (0.18.0 mM)
were prepared fresh each day before use in 1 ml of THF/EtOH
(1:1, v/v). To each test tube with 1 ml of sample solution or
1 ml of catechin standard solution, 0.5 ml of 50 mM NaBH4
solution and 0.5 ml of 74.56 mM AlCl3 solution were added.
The mixture was shaken in an orbital shaker at room temperature for 30 min. Then an additional 0.5 ml of NaBH4 solution was added into each test tube with continuing shaking
for another 30 min at room temperature. Cold acetic acid
solution (2.0 ml of 0.8 M, 4 1C) was added into each test tube,
and the solutions were kept in the dark for 15 min after a
thorough mix. Then, chloranil (1.0 ml, 20 mM) was added
into each tube, which was heated at 100 1C with shaking for
60 min in a reciprocal shaking bath. The reaction solutions
were cooled using tap water, and the nal volume was brought
to 4 ml using methanol. Then, 1 ml of 1052 mM vanillin was
added into each tube, followed by mixing. Concentrated HCl
(2.0 ml, 12 M) was added into each tube, and the reaction
solutions were kept in the dark for 15 min after a thorough
mix. Aliquots of the nal reaction solutions (200 ml) were
added into each well of a 96-well plate, and absorbances were
measured at 490 nm.
wide use, including the ORAC (Cao et al., 1993), total radicaltrapping antioxidant parameter (TRAP) (Ghiselli et al., 1995;
Wayner et al., 1985), TEAC (Miller et al., 1993), total oxyradical scavenging capacity (TOSC) (Winston et al., 1998), and
the peroxyl radical scavenging capacity (PSC) assays, the latter
of which was developed by our laboratory (Adom and Liu,
2005). FRAP assay (Benzie and Strain, 1996) and the DPPH
free radical method (Brand-Williams et al., 1995) measure the
ability of antioxidants to reduce ferric iron and DPPH,
respectively.
For the methods based on similar principles of electron
transfer (ET), there are the TEAC, FRAP, and DPPH. For the
hydrogen atom transfer methods (HAT), there are the ORAC
method, TRAP, TOSC, and the PSC assays (Stratil et al., 2007;
Badarinath et al., 2010).
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
309
rubber septum-sealed vials in a nal volume of 1 ml. The reactions were initiated by injection of 100 ml of 200 mM ABAP
in water directly through the rubber septum. Ethylene production was measured by gas-chromatographic analysis of
1 ml aliquots taken directly from the head space of the reaction vials. By staggering the starting times for each vial, 810
serial samples can be monitored in sequence at 12-min
intervals. Analyses were performed with a gas chromatograph
equipped with a ame ionization detector.
310
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
311
antioxidant activity assays commonly used to screen antioxidant materials for potential biological activity (Wolfe and
Liu, 2007).
It has been suggested that the following should be considered in choosing appropriate methods to measure antioxidant activity: physiologically relevant substrates; conditions
that mimic biological systems; low levels of oxidants that
represent all stages of oxidation; measurement of different
compounds at comparable concentrations and use of plant
extracts where the phenolic composition is known; and
quantication based on induction period, percent inhibition,
rates of product formation/decomposition, or median effective
dose (Frankel and Meyer, 2000).
In CAA method, the probe, DCFH-DA, is taken up by
HepG2 human hepatocarcinoma cells and deacetylated to
DCFH. Peroxyl radicals generated from ABAP lead to the oxidation of DCFH to uorescent DCF, and the level of uorescence measured upon excitation is proportional to the level
of oxidation. Pure phytochemical compounds and food extracts quench peroxyl radicals and inhibit the generation of
DCF. Thus, the CAA assay uses the ability of peroxyl radicals,
reactive products of lipid oxidation, to induce the formation of
a uorescent oxidative stress indicator in the cell culture and
measures the prevention of oxidation by antioxidants (Wolfe
and Liu, 2007).
The protocol for CAA method is performed according to
the method described by Wolfe and Liu (2007). Briey,
human hepatocellular carcinoma HepG2 cells were seeded at a
density of 6 104 per well on a 96-well microplate in 100 ml
of growth medium/well. Twenty-four hours after seeding, the
growth medium was removed, and the wells were washed with
PBS. Wells were treated in triplicate for 1 h with 100 ml of
treatment medium containing tested fruit extracts plus 25 mM
DCFH-DA. Then 600 mM ABAP was applied to the cells in
100 ml of HBSS, and the 96- well microplate was placed into a
plate reader at 37 1C. Emission at 538 nm was measured after
excitation at 485 nm every 5 min for 1 h. Each plate included
triplicate control and blank wells. Control wells contained
cells treated with DCFH-DA and ABAP. Blank wells contained
cells treated with DCFH-DA and HBSS. Results were expressed
as mmol quercetin equivalents (QE) per 100 g of fresh fruit.
312
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
References
Adom, K., Liu, R.H., 2005. Rapid peroxyl radical scavenging capacity (PSC) assay
for assessing both hydrophilic and lipophilic antioxidants. Journal of Agricultural
and Food Chemistry 53, 65726580.
Aldini, G., Yeum, K.J., Russell, R.M., Krinsky, N.I., 2001. A method to measure the
oxidizability of both the aqueous and lipid compartments of plasma. Free Radical
Biology and Medicine 31, 10431050.
Ames, B., Shigenaga, M., Hagen, T., 1993. Oxidants, antioxidants, and the
degenerative diseases of aging. Proceedings of the National Academy of
Sciences 90, 79157922.
Ames, B.N., Gold, L.S., 1991. Endogenous mutagens and the causes of aging and
cancer. Mutation Research 250, 316.
Ames, B.N., Shigenaga, M.K., Gold, L.S., 1993. DNA lesions, inducible DNA repair,
and cell division: The three key factors in mutagenesis and carcinogenesis.
Environmental Health Perspectives 101 (Suppl 5), 3544.
Arnao, M.B., Cano, A., Acosta, M., 2001. The hydrophilic and lipophilic contribution
to total antioxidant activity. Food Chemistry 73, 239244.
Arts, M.J.T.J., Dallinga, J.S., Voss, H.-P., Haenen, G.R.M.M., Bast, A., 2004. A new
approach to assess the total antioxidant capacity using the TEAC assay. Food
Chemistry 88, 567570.
Badarinath, A., Rao Mallikarjune, K., Chetty, C., et al., 2010. Review on in-vitro
antioxidant methods: Comparisions, correlations and considerations. International
Journal of PharmTech Research 2 (2), 12761285.
Beatty, S., Koh, H., Phil, M., Henson, D., Boulton, M., 2000. The role of oxidative
stress in the pathogenesis of age-related macular degeneration. Survey of
Ophthalmology 45 (2), 115134.
Benzie, I.F.F., Strain, J.J., 1996. The ferric reducing ability of plasma (FRAP) as a
measure of antioxidant power: The FRAP assay. Analytical Biochemistry 239,
7076.
Benzie, I.F., Strain, J.J., 1999. Ferric reducing/antioxidant power assay: Direct
measure of total antioxidant activity of biological uids and modied version for
simultaneous measurement of total antioxidant power and ascorbic acid
concentration. Methods in Enzymology 299, 1527.
Bernstein, P.S., Khachik, F., Carvalho, L.S., et al., 2001. Identication and
quantitation of carotenoids and their metabolites in the tissues of the human eye.
Experimental Eye Research 72 (3), 215223.
Bloor, S.J., 2001. Overview of methods for analysis and identication of avonoids.
Methods in Enzymology 335, 314.
Boyer, J., Brown, D., Liu, R.H., 2004. Uptake of quercetin and quercetin-3-glucoside
from whole onions and apple peels by Caco-2 cell monolayers. Journal of
Agricultural and Food Chemistry 52, 71727179.
Boyer, J., Brown, D., Liu, R.H., 2005. In vitro digestion and lactase treatment
inuence uptake of quercetin and quercetin glucoside by the Caco-2 cell
monolayer. Nutrition Journal 4, 1.
Boyer, J., Liu, R.H., 2004. Apple phytochemicals and their health benets. Nutrition
Journal 3, 520.
Brand-Williams, W., Cuvelier, M.E., Berset, C., 1995. Use of a free radical method to
evaluate antioxidant activity. Lebensmittel-Wissenschaft & Technologie 28, 2530.
Broadhurst, R.B., Jones, W.T., 1978. Analysis of condensed tannins using acidied
vanillin. Journal of the Science of Food and Agriculture 29, 788794.
Burton, G.W., Ingold, K.U., 1986. Vitamin E: Application of the principles of physical
organic chemistry to the exploration of its structure and function. Accounts of
Chemical Research 19, 194201.
Caldwell, C.R., 2001. Oxygen radical absorbance capacity of the phenolic
compounds in plant extracts fractionated by HPLC. Analytical Biochemistry 293
(2), 232238.
Cao, G., Alessio, H.M., Cutler, R.G., 1993. Oxygen-radical absorbance capacity
assay for antioxidants. Free Radical Biology and Medicine 14 (3), 303311.
Cao, G., Prior, R.L., 1998. Comparison of different analytical methods for assessing
total antioxidant capacity of human serum. Clinical Chemistry 44, 13091315.
Cao, G., Verdon, C.P., Wu, A.H., Wang, H., Prior, R.L., 1995. Automated assay of
oxygen radical absorbance capacity with the COBAS FARA II. Clinical Chemistry
41, 17381744.
Chang, C.-C., Yang, M.-H., Wen, H.-M., Chern, J.-C., 2002. Estimation of total
avonoid content in propolis by two complementary colorimetric methods.
Journal of Food and Drug Analysis 10, 178182.
Christ, B., Muller, K., 1960. Zur serienmaessigen bestimmung des gehaltes an
avonol-derivaten in drogen. Archiv der Pharmazie 293 (65), 10331042.
Chu, Y.F., Sun, J., Wu, X., Liu, R.H., 2002. Antioxidant and antiproliferative
activities of vegetables. Journal of Agricultural and Food Chemistry 50,
69106916.
Deprez, S., Mila, I., Huneau, J., Tome, D., Scalbert, A., 2001. Transport of
proanthocyanidin dimer, trimer, and polymer across monolayers of human
intestinal epithelial Caco-2 cells. Antioxidants & Redox Signaling 3, 957967.
Dewanto, V., Wu, X., Adom, K.K., Liu, R.H., 2002a. Thermal processing enhances
the nutritional value of tomatoes by increasing total antioxidant activity. Journal
of Agricultural and Food Chemistry 50, 30103014.
Dewanto, V., Wu, X.Z., Liu, R.H., 2002b. Processed sweet corn has higher
antioxidant activity. Journal of Agricultural and Food Chemistry 50, 49594964.
Dobes, J., Zitka, O., Sochor, J., et al., 2013. Electrochemical tools for determination
of phenolic compounds in plants. A review. International Journal of
Electrochemical Science 8, 45204542.
Eberhardt, M.V., Lee, C.Y., Liu, R.H., 2000. Nutrition Antioxidant activity of fresh
apples. Nature 405, 903904.
Folin, O., Ciocalteu, V., 1927. On tyrosine and tryptophane determinations in
proteins. Journal of Biological Chemistry 73, 627650.
Frankel, E.N., Meyer, A.S., 2000. The problems of using onedimensional methods to
evaluate multifunctional food and biological antioxidants. Journal of the Science
of Food and Agriculture 80 (13), 19251941.
Garcia-Alonso, F.J., Guidarelli, A., Periago, M.J., 2007. Phenolic-rich juice prevents
DNA single-strand breakage and cytotoxicity caused by tert-butylhydroperoxide in
U937 cells: The role of iron chelation. Journal of Nutritional Biochemistry 18,
457466.
Gardner, E.J., Ruxton, C.H.S., Leeds, A.R., 2007. Black tea Helpful or harmful? A
review of the evidence. European Journal of Clinical Nutrition 61, 318.
Garrett, D.A., Filla, M.L., Sarama, R.J., Craft, N., 1999. Accumulation and retention
of micellar -carotene and lutein by Caco-2 human intestinal cells. Journal of
Nutritional Biochemistry 10, 573581.
Ghiselli, A., Serani, M., Maiani, G., Azzini, E., Ferro-Luzzi, A., 1995. A
uorescence-based method for measuring total plasma antioxidant capability.
Free Radical Biology and Medicine 18 (1), 2936.
Gil, M.I., Tomas-Barberan, F.A., Hess-Pierce, B., Holcroft, D.M., Kader, A.A., 2000.
Antioxidant activity of pomegranate juice and its relationship with phenolic
composition and processing. Journal of Agricultural and Food Chemistry 48
(10), 45814589.
Gutierrez, F., Arnaud, T., Garrido, A., 2001. Contribution of polyphenols to the
oxidative stability of virgin olive oil. Journal of the Science of Food and
Agriculture 81, 14631470.
Hanasaki, Y., Ogawa, S., Fukui, S., 1994. The correlation between active oxygens
scavenging and antioxidative effects of avonoids. Free Radical Biology and
Medicine 16, 845850.
Hatch, W., Tanner, C.E., Butler, N.M., O'Brien, E.P., 1993. A micro-Folio-Denis
method for the rapid quantication of phenolic compounds in marine plants and
animals. Platform Presentation at the 10th Annual Meeting of the International
Society of Chemical Ecology, Tampa, Florida.
He, X., Liu, D., Liu, R.H., 2008. Sodium borohydride/chloranil-based assay for
quantifying total avonoids. Journal of Agricultural and Food Chemistry 56,
93379344.
Hertog, M.G., Feskens, E.J., Hollman, P.C., Katan, M.B., Kromhout, D., 1993.
Dietary antioxidant avonoids and risk of coronary heart disease: The Zutphen
Elderly Study. Lancet 342, 10071011.
Hertog, M.G., Feskens, E.J., Hollman, P.C., Katan, M.B., Kromhout, D., 1994.
Dietary avonoids and cancer risk in the Zutphen Elderly Study. Nutrition and
Cancer 22, 175184.
Hertog, M.G., Hollman, P.C., 1996. Potential health effects of the dietary avonol
quercetin. European Journal of Clinical Nutrition 50, 6371.
Hollman, P.C.H., Arts, I.C.W., 2000. Flavonols, avones and avanols Nature,
occurrence and dietary burden. Journal of the Science of Food and Agriculture
80, 10811093.
Hollman, P., Katan, M., 1997. Absorption, metabolism and health effects of dietary
avonoids in man. Biomedicine & Pharmacotherapy 51, 305310.
Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J.A., Deemer, E.K., 2002.
Development and validation of oxygen radical absorbance capacity assay for
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
313
Ou, B., Hampsch-Woodill, M., Prior, R.L., 2001. Development and validation of an
improved oxygen radical absorbance capacity assay using uorescein as the
uorescent probe. Journal of Agricultural and Food Chemistry 49, 46194626.
Perron, N., Brumaghim, J., 2009. A review of the antioxidant mechanisms of
polyphenol compounds related to iron binding. Cell Biochemistry and Biophysics
53, 75100.
Prior, R.L., Cao, G., 2000. Analysis of botanicals and dietary supplements for
antioxidant capacity: A review. Journal of AOAC International 83 (4), 950955.
Prior, R.L., Hoang, H., Gu, L., et al., 2003. Assays for hydrophilic and lipophilic
antioxidant capacity (oxygen radical absorbance capacity (ORAC(FL))) of plasma
and other biological and food samples. Journal of Agricultural and Food
Chemistry 51, 32733279.
Prior, R.L., Wu, X., Schaich, K., 2005. Standardized methods for the determination
of antioxidant capacity of phenolics in foods and dietary supplements. Journal of
Agricultural and Food Chemistry 53, 42904302.
Pryor, W.A., Cornicelli, J.A., Devall, L.J., et al., 1993. A rapid screening test to
determine the antioxidant potencies of natural and synthetic antioxidants. Journal
of Organic Chemistry 58, 35213532.
Pulido, R., Bravo, L., Saura-Calixo, F., 2000. Antioxidant activity of dietary
polyphenols as determined by a modied ferric reducing/antioxidant power assay.
Journal of Agricultural and Food Chemistry 48, 33963402.
Regoli, F., Winston, G.W., 1999. Quantication of total oxidant scavenging capacity
of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals.
Toxicology and Applied Pharmacology 156, 96105.
Sarkar, S.K., Howarth, R.E., 1976. Specicity of vanillin test for avonols. Journal of
Agricultural and Food Chemistry 24, 317320.
Seeram, N.P., Aviram, M., Zhang, Y., et al., 2008. Comparison of antioxidant
potency of commonly consumed polyphenol-rich beverages in the United States.
Journal of Agricultural and Food Chemistry 56, 14151422.
Sharma, A., Bhardwaj, S., Mann, A.S., Jain, A., Kharya, M.D., 2007. Screening
methods of antioxidant activity: An overview. Pharmacognosy Reviews 1,
232238.
Singleton, V.L., Orthofer, R., Lamuela-Ravento, R.M., Lester, P., 1999. Analysis of
total phenols and other oxidation substrates and antioxidants by means of
FolinCiocalteu reagent. Methods in Enzymology. New York, NY: Academic
Press, pp. 152178.
Singleton, V.L., Rossi Jr., J.A., 1965. Colorimetry of total phenolics with
phosphomolybdicphosphotungstic acid reagents. American Journal of Enology
and Viticulture 16, 144158.
Snodderly, D.M., 1995. Evidence for protection against age-related macular
degeneration by carotenoids and antioxidant vitamins. American Journal of
Clinical Nutrition 62 (6), 1448S1461S.
Stratil, P., Klejdus, B., Kuban, V., 2007. Determination of phenolic compounds and
their antioxidant activity in fruits and cereals. Talanta 71, 17411751.
Sun, J., Chu, Y.F., Wu, X.Z., Liu, R.H., 2002. Antioxidant and antiproliferative
activities of common fruits. Journal of Agricultural and Food Chemistry 50,
74497454.
Sun, J., Liu, R.H., 2006. Cranberry phytochemical extracts induce cell cycle arrest
and apoptosis in human MCF-7 breast cancer cells. Cancer Letters 241,
124134.
Swain, T., Hillis, W.E., 1959. The phenolic constituents of Prunus domestica. The
quantitative analysis of phenolic constituents. Journal of the Science of Food and
Agriculture 10, 2738.
Sweeny, J.G., Iacobucci, G.A., 1977a. Synthesis of anthocyanins. II. The synthesis of
3-deoxyanthocyanidins from 5-hydroxy-avanones. Tetrahedron 33, 29272932.
Sweeny, J.G., Iacobucci, G.A., 1977b. Synthesis of anthocyanins. I. The oxidative
generation of avylium cations using benzoquinines. Tetrahedron 33, 29232926.
Sweeny, J.G., Iacobucci, G.A., 1981. Synthesis of anthocyanins-III: Total synthesis of
apigeninidin and luteolinidin chlorides. Tetrahedron 37, 14811483.
Temple, N.J., 2000. Antioxidants and disease: More questions than answers.
Nutrition Research 20, 449459.
Vaya, J., Mahmood, S., 2006. Flavonoid content in leaf extracts of the g Ficus
carica L.), carob (Ceratonia siliqua L.) and pistachio (Pistacia lentiscus L.).
BioFactors 28, 169175.
Vinson, J.A., Proch, J., Zubik, L., 1999. Phenol antioxidant quantity and quality in
foods: Cocoa, dark chocolate, and milk chocolate. Journal of Agricultural and
Food Chemistry 47, 48214824.
Vinson, J.A., Su, X., Zubik, L., Bose, P., 2001. Phenol antioxidant quantity and
quality in foods: Fruits. Journal of Agricultural and Food Chemistry 49,
53155321.
Visioli, F., Bellomo, G., Galli, C., 1998. Free radical-scavenging properties of olive
oil polyphenols. Biochemical and Biophysical Research Communications 247,
6064.
314
Analyses of Total Phenolics, Total Flavonoids, and Total Antioxidant Activities in Foods and Dietary Supplements
Wayner, D.D., Burton, G.W., Ingold, K.U., Locke, S., 1985. Quantitative measurement
of the total, peroxyl radical-trapping antioxidant capability of human blood
plasma by controlled peroxidation. The important contribution made by plasma
proteins. FEBS Letters 187 (1), 3337.
Willett, W.C., 1994. Diet and health: What should we eat? Science 254, 532537.
Willett, W.C., 1995. Diet, nutrition, and avoidable cancer. Environmental Health
Perspectives 103 (8), 165170.
Winston, G.W., Regoli, F., Duga Jr., A.J., Fong, J.H., Blanchard, K.A., 1998. A rapid
gas chromatographic assay for determining oxyradical scavenging capacity of
antioxidants and biological uids. Free Radical Biology and Medicine 24 (3),
480493.
Wolfe, K.L., Liu, R.H., 2007. Cellular antioxidant activity (CAA) assay for assessing
antioxidants, foods, and dietary supplements. Journal of Agricultural and Food
Chemistry 55, 88968907.
Wolfe, K., Wu, X., Liu, R.H., 2003. Antioxidant activity of apple peels. Journal of
Agricultural and Food Chemistry 51, 609614.
Wu, X., Beecher, G.R., Holden, J.M., et al., 2004. Lipophilic and hydrophilic
antioxidant capacities of common foods in the United States. Journal of
Agricultural and Food Chemistry 52, 40264037.
Yates, J.L., Peckol, P., 1993. Effects of nutrient availability and herbivory on
polyphenolics in the seaweed Fucus vesiculosus. Ecology 74, 17571766.
Glossary
Anorexia A symptom that reects the lack of appetite.
It could induce weight loss that is considered
unhealthy.
Ataxia A nonspecic neurological sign that consists of lack
of voluntary coordination of muscle movements. It could be
as a result of dysfunction of the cerebellum, the loss of
sensitivity to the positions of joint and body parts
(proprioception), or to dysfunction of the vestibular system
(disequilibrium).
Dyspnea A symptom of breathlessness commonly
associated to respiratory distress.
Enzootic Organism that is native to a place or a specic
fauna.
Fomite Any object or substance capable of carrying
infectious organisms and able to transfer them from one
individual to another.
Introduction
Ectoparasites and vectorborne diseases have a major impact on
the productivity and welfare of livestock and wildlife and
represent a constant risk for the survival and well-being of
major human groups throughout the world (McDermott et al.,
1999; Perry and Sones, 2007; Herrero et al., 2010; Thornton,
2010; Gachohi et al., 2011; Rich and Perry, 2011; FAOSTAT,
2012; Grace et al., 2012).
Recent surveys have estimated that the livestock population
worldwide has reached 24 billion in 2012 (FAOSTAT, 2012).
Analysis of the Food and Agriculture Organization of the
United Nations Statistical Program (FAOSTAT) indicates that
there are ve major groups of livestock with major economical
and welfare impact for humans worldwide: cattle/buffaloes,
sheep/goats, chickens, swine, and horses (Table 1). Cattle and
buffaloes with 1.6 billion heads worldwide are mostly concentrated in Asia (32% with more than 520 million animals),
followed by South America (20%), Africa (15%), North
America (14%), and Europe (10%). Similarly, sheep/goats
with more than 2000 million animals worldwide are mainly
distributed in Asia (4670 million), Africa (4250 million),
and Oceania (4100 million).
Ectoparasites, such as ticks, eas, biting ies, ked, mites,
midges, lice, and mosquitoes, could impose a heavy burden to
livestock affecting productivity. Blood loss, irritation, and
discomfort could induce damage to the animal skin (hides and
wool), reduce milk production, decrease immunity response,
and cause retarded growth rates. In addition, ectoparasites
represent a constant threat to livestock due to their competence (either as ampliers or mechanically) for the transmission of a large number of pathogens with high morbidity
and mortality implications. In addition to the worldwide
doi:10.1016/B978-0-444-52512-3.00192-3
315
316
Table 1
Region
Country
Livestocka total
Cattle/buffaloes
Sheep/goats
Horses
Swine
Chicken
Asia
India
China
Pakistan
Bangladesh
USA
Mexico
Brazil
Argentina
Colombia
Nigeria
Gabon
Ghana
Sudan
Ethiopia
New Zealand
Australia
Vietnam
Indonesia
Philippines
France
Germany
United Kingdom
559.1
875.8
153.4
76.2
177.4
71.5
281.9
75
36.5
115.7
0.5
10.6
138
103.7
42.9
101.9
37.6
51
23.6
43.8
42.2
46.2
321
108
65
24.4
94
32.6
210.7
49
28
16
NS
1.5
42
53.4
9.9
26.7
8.8
15.6
5.8
19.6
13
10.1
228
285
88
51.8
8.6
17
26.7
20
4.6
92
0.3
8.6
96
48.3
32.7
72.6
1.3
27.8
4.2
9.3
2.2
31.2
0.5
6.8
0.4
NA
9.8
6.4
5.5
3.7
2.1
0.2
NS
NS
NS
2
NS
0.3
0.1
0.4
0.2
0.4
0.5
0.4
9.6
476
NA
NA
65
15.5
39
2.3
1.8
7.5
0.2
0.5
NS
NS
0.3
2.3
27.4
7.2
13.4
14.5
26.5
4.5
774
4803
321
228
2100
506
1239
96
157
192
3.2
47.8
43
49
14
83
218
1623
159
124
114
164
North America
South America
West Africa
East Africa
Oceania
SE Asia
Europe
ness, exhaustion, and death. Similarly, psoroptic ear mite infestation could cause scaling, crusting, inammation, and hair
loss of the ear as well as accumulation of wax, ear scratching,
head shaking, and rubbing of the head and ears. Chronic infestations can lead to anemia and weight loss and in extreme
cases can be fatal.
Early reports on losses caused by lice in the United States,
for example, estimate that lice cause a 68 lb per head weight
loss in 12% of the cattle slaughtered, representing an estimated
cost of more than US$126 million (Drummond, 1985). The
losses in weight gain, hide values, and even those associated
with the type of housing, including damage of fences, hay
racks, and buildings, due to rubbing are very dependent on
variables, such as sex, age, and immunity (Michel et al., 1979;
Geden and Stoffolano, 1980; Lancaster et al., 1982; Meyer
et al., 1982; Gibney et al., 1985; Lancaster, 1986).
Anemia due to blood intake could result in animals with
high parasitism. Some examples include mosquitoes that
could cause painful bites, loss of weight, and reduction of milk
production; sucking lice infestation that could result in loss of
weight, poor performance, and reduction of milk production
due to blood loss; and the lethargy associated with the dullness, nervousness, and irritation induced by the lice-feeding
activity. Ticks that bite may induce inammation, itching, and
swelling and potentially induce secondary infections.
Ticks have a negative impact on cattle as they cause weight
loss in animals and decrease the milk production. Some estimates showed that infestation with large number of engorged
Boophilus female ticks could reduce the annual weight by up to
0.5 kg per animal and decrease the annual milk production by
up to 200 l per animal.
Table 2
317
Major parasite groups, species (scientic and common names) and their impact on the hosts
Parasite
Species
Common name
Host
Consequences
Biting
ies
Simulium spp.
Sheep
Melophagus
ovis
Tabanus spp.
Haematobia
irritans
Horne y
Oestrus ovis
Hypoderma spp.
Gasterophilus
spp.
Cochliomyia
hominivorax
Screw-worm y
Cuccoides spp.
and
Leptoconops
spp.
(Continued )
318
Table 2
Continued
Parasite
Species
Common name
Host
Consequences
Hippobosca spp.
Forest y,
Ornithodoros
spp. and
Otobius spp.
Hyalomma spp.,
Ixodes spp.,
Dermacentor
spp.,
Amblyomma
spp.,
Boophilus
spp., and
Rhipicephalus
spp.
Damalinia spp.
Soft tick
Ticks
Lice
Haematopinus
spp.,
Linognathus
spp., and
Solenopotes
spp.
Bovicola spp.
Mites
Sarcoptes spp.,
Psoroptes
spp., Psorobia
spp.,
Demodex
spp., and
Dermanyssus
spp.,
Hard tick
Heartwater (Cowdriosis)
Heartwater is a septicemic, infectious tick-transmitted disease
of cattle, sheep, goats, and other ruminants caused by Ehrlichia
ruminantium (Health, 2012). All domestic and wild subclinical-infected ruminants, including cattle, buffalo (Syncerus
caffer), black wildebeest or white-tailed gnu (Connochaetes
gnou), oryx (Taurotragus oryx oryx), giraffe (Giraffe camelopardalis), sable antelope (Hippotragus niger), Rusa deer (Rusa
Mosquitoes, biting
midges
Hard ticks
Otobius spp.
Otobius spp.
Soft ticks
Rhipicephalus spp., A.
variegatum, and
Haemaphysalis spp.
Boophilus spp., Dermacentor
spp., Rhipicephalus spp.,
Ixodes spp., Hyalomma spp.,
and Ornithodoros spp.
Aedes spp., Anopheles spp.,
Culex spp., Deinocerites spp.,
Mansonia spp., Psorophora
spp., Coquiletidia spp.,
Ochlerotatus spp., and
Simulium spp.
Ornithodoros porcinus
Species
Host
Easter Equine
Encephalitis (EEE),
Venzuelan Equine
encephalitis (VEE),
Western Equine
Encephalitis (WEE),
West Nile Virus
(WNV), Japanese
Ecephalitis (JE)
Equine babesiosis
(piroplasmosis)
Heartwater
Bovine babesiosis
(redwater)
Coxiella burnetii
Francisella tularensis
Etiological agent
Q-fever
Tularemia
Diseases
Yes
North, Central and
South America and
the Caribbean (VEE
and EEE) or USA
(WEE), worldwide
(WNV), and Japan
(JE)
(Continued )
Yes
Yes
Yes
Yes
Human
Worldwide, Africa,
Mediterranean basin
to China
Worldwide
Worldwide
Worldwide
Worldwide
Worldwide
Worldwide
Occurrence
Major parasites groups as vectors of diseases: Vector species names, host, diseases, etiological agent, and occurrence. Information about the potential zoonotic transmission to humans is
Vector
Table 3
indicated
Biting ies
Vector
Table 3
Continued
Culicoides spp.
Culex spp.
Melophagus ovinus
Aedes spp.
Host
Species
Bluetongue
Trypanosomiasis
(surra, nagana, Pesteboba, Tahaga)
Bluetongue, bovine
ephemeral fever
(Three Day Sickness),
african horse sickness
Nairobi sheep disease,
Crimean Congo
hemorrhagic fever
Rift Valley Fever
Diseases
Vesiculovirus spp.
Trypanosoma evansi, T.
equinum, T. brucei, T. vivax,
T. congolense
Vesiculovirus spp.
Capripoxvirus spp.
Etiological agent
Worldwide
Yes
Yes
Yes
Yes
Africa
Yes
Human
Worldwide, Europe
Occurrence
320
Animal Health: Ectoparasites
No commercial vaccines are available at present. Attenuated bacterial strains used as vaccines (such as Gardel,
Senegal, or Welgevonden strains) confer protection against
homologous lethal challenges, but they induce limited or
nonprotection against heterologous strain challenges. Inactivated vaccines using the Gardel or Mbizi strain or recombinant DNA vaccines do not prevent infection but
rather confer some protection and reduction of death on
animals exposed to a wide variety of live strains.
As for many tick-transmitted infectious diseases, the most
effective prophylaxis is the eradication or control (repellents and acaricides) of the tick vector.
321
Anaplasmosis
Anaplasmosis in ruminants (also known as bovine anaplasmosis and Gall sickness) is an infectious hemotropic disease
of ruminants caused by several species of bacteria of the
genus Anaplasma: Anaplasma marginale, Anaplasma centrale,
Anaplasma ovis, Anaplasma bovis, Anaplasma caudatum, and
Anaplasma phagocytophilum (Health, 2012). Cattle, sheep, or
goats that have recovered from the clinical disease or other
species of ruminants, such as water buffalo (Bubalus bubalis),
white-tailed deer, mule deer (Odocoileus hemionus hemionus),
black-tailed deer (Odocoileus hemionus columbianus), pronghorn (Antilocapra americana americana), Rocky Mountain Elk
(Cervus elaphus nelsoni), bighorn sheep (Ovis canadensis canadensis), black wildebeest (Connochaetes gnu), blesbuck
(Damaliscus albifrons), and duiker (Sylvicapra grimmi grimmi),
can serve as reservoir. These pathogens are transmitted by
several hard tick species of the genera Boophilus spp., Dermacentor spp., Rhipicephalus spp., Ixodes spp., Hyalomma spp.,
and Ornithodoros spp. In addition, athropods such as horse
ies (Tabanus spp.) and mosquitoes (Psorophora spp.) (Blouin
et al., 2000; Kocan et al., 2000, 2001, 2002, 2003, 2004a,b;
de la Fuente et al., 2002; Kocan and de la Fuente, 2003; De La
Fuente et al., 2004; de la Fuente et al., 2005) and fomites
(such as needles and surgical instruments that were in direct
contact with blood-infected materials) could also be responsible for the transmission. Anaplasmosis is present in
most tropical, subtropical, and in some temperate areas,
which account for its worldwide distribution.
Anaplasmosis in characterized in the acute form by fever,
anemia, weakness, anorexia, constipation, yellowing of the
mucous membranes, dehydration, dyspnea, reduced or poor
performance and milk production, and weight loss. Mortality
could be as high as 70% (OIE, World Organization for Animal
Health, 2012; Health, 2012).
322
Bluetongue
Bluetongue is a viral disease in sheep and cattle caused by
several species of the genus Orbivirus (Health, 2012). There are
24 recognized serotypes of the bluetongue virus (BTV). The
virus affects a wide range of ruminants, such as sheep, goats,
cattle, buffaloes, white-tailed deer, pronghorn (Antilocapra
americana), bighorn sheep (Ovis canadensis), African antelope,
and other Artiodactyla species such as camels. Ruminants seem
not to be the natural reservoir for the virus, because it does not
establish persistent infections. The survival of the agent in the
environment may be associated with insect or potentially with
an unknown reservoir. The virus is transmitted among sheep
and cattle by biting midges of the genus Culicoides and perhaps
the wingless biting y Melophagus ovinus (among sheep).
Transmission occurs when midges feed on viremic animals
and then on healthy individuals. Bluetongue is not a contagious disease; however, the virus can be spread mechanically
on surgical equipment and needles. The distribution and
prevalence of the disease is mostly associated with environmental factors (i.e., high rainfall, temperature, and humidity)
and has a seasonal occurrence. The BTV has been found in
many parts of the world, including Africa, Europe, the Middle
East, Australia, the South Pacic, North and South America,
and parts of Asia (Holbrook et al., 1985; Osburn et al., 1985;
Parsonson et al., 1985; OIE, World Organization for Animal
Health, 2012).
The pathological signs and the severity of the infection
varies widely, from asymptomatic to fatal, depending on
factors related to agent, host, and environment. Some common lesions associated with the disease may include fever,
congestion, edema, hemorrhages, and ulcerations of digestive
and respiratory mucosae. Mucopurulent nasal discharges,
excessive salivation, depression, dyspnea, and hyperemic of
the muzzle, tongue, lips, face, eyelids, and ears are also
common in susceptible animals. The tongue may become
edematous and cyanotic protruding from the mouth. This
symptomatology is what the disease is named after. In addition, hypertrophy of lymph nodes and splenomegaly have
also been commonly reported. Morbidity in sheep can reach
100% with mortality between 30% and 70% in more susceptible breeds. In wild ruminants, especially white-tailed
deer and pronghorn antelope, morbidity rate could reach
100%, with a mortality rate that can reach 90% (Health,
2012). It is estimated that the annual losses due to morbidity
and mortality of animals, trade embargoes, and vaccination
costs worldwide may be as high as US$3 billion (Anderson
Live attenuated and inactivated virus vaccines are available; however, they showed to be serotype specic.
Nevertheless, attenuated or live vaccines should be used
cautiously because the viruses in attenuated vaccines can
be transmitted to unvaccinated animals and could reassort
with eld strains, resulting in new viral strains. In addition, vaccines can cause fetal malformations in pregnant
ewes.
As for most arboviral infections, the most effective control
is to limit the spread or the occurrence of the disease by
quarantine or limit the movement (housing) of animals;
preventive vector control with insecticides such as synthetic
pyrethroids or organophosphates is recommended.
No treatment is available for infected animals.
Bovine Babesiosis
Babesiosis, or tick fever, is a febrile tick-transmitted disease of
domestic and wild animals caused by several species of the
genus Babesia (Babesia bovis, Babesia bigemina, Babesia divergens,
Babesia major, Babesia ovata, Babesia occultans, and Babesia jakimovi), a protozoan parasite distributed worldwide (Barnett,
1974; Health, 2012). The natural reservoirs of the protozoan
are subclinical infected ruminants, such as cattle, buffalo
(Bufalus bubalis and Syncerus caffer), reindeer (Rangifer tarandus), and white-tailed deer. The protozoan does not survive
outside of its hosts and is transmitted mainly by two genera of
hard tick: Rhipicephalus spp. (Rhipicephalus microplus, Rhipicephalus annulatus, Rhipicephalus decoloratus, Rhipicephalus geigyi,
and Rhipicephalus evertsi), which are vectors of B. bovis and B.
bigemina; and Ixodes ricinus, which is vector of B. divergens.
Bovine babesiosis is found in areas where its arthropod
vector is distributed, especially tropical and subtropical regions, including Africa, Asia, Australia, the Caribbean, and
Central and South America (Montenegro-James, 1992; OIE,
World Organization for Animal Health, 2012).
The pathologies associated with the disease depend on
the parasite species and the age and immune status of the host.
In general terms, clinical sings involve fever, anorexia,
hemolytic anemia, hemoglobinuria, hepatosplenomegaly
(enlarged spleen and liver), and production of dark red- or
brown-colored urine. Ataxia, incoordination, and signs of
general circulatory shock are common in B. Bovis-infected
animals, where parasitemia generally does not exceed 1%.
Hemoglobinuria and anemia are typical clinical signs of B.
Bigemina- and B. divergens-infected animals, with reports of
parasitemia levels of up to 30% (Health, 2012).
323
Trypanosomiasis
Trypanosomiasis, also known as surra, nagana, Peste-boba,
Tahaga, Kaodzera, Baleri, Gambian horse sickness, Cachexial
fevers, Dourine, mal de las caderas, etc., is a disease in cattle,
buffaloes, sheep, goats, deer, camelids, antelopes, lamas,
donkeys, horses, mules, deer, llamas, pigs, and elephants
caused by a several agellated protozoan species of the genus
Trypanosoma: Trypanosoma evansi, Trypanosoma equinum, Trypanosoma brucei, Trypanosoma vivax, and Trypanosoma congolense
(FAOWHO, 1969; Takken et al., 1988; Dargie et al., 1993;
Cecchi et al., 2009; Ilemobade, 2009; Health, 2012). It is
transmitted from animal to animal mechanically by
hematophagous ies, including Tabanus spp., Musca spp.,
Lyperosia spp., Stomoxys, and Atylotus genera. In addition,
hemophagous bats in South and Central America can serve as
hosts, reservoirs, and vectors of T. evansi by transmitting the
protozoan mechanically from animal to animal with their
saliva or through biting ies (Tabanus spp., Musca spp.,
Lyperosia spp., and Atylotus spp.). Species such as T. congolense,
T. vivax, T. brucei, Trypanosoma Uniforme, and Trypanosoma
simiae are known as tsetse-transmitted trypanosomiasis where
more than 23 species of Tsetse y (Glossina spp.) act as biological vector. The tsetse-transmitted trypanosomiasis is the
most economically important livestock disease in Africa, especially in cattle, affecting more than 37 countries with an
estimated annual overall loss of US$6 billion year1 (FAO
WHO, 1969; Dargie et al., 1993; Hendrickx et al., 1999; Cecchi
et al., 2008; Cecchi et al., 2009).
The disease in characterized by the presence of a nonregenerative anemia, intermittent fever, edema, lacrimation,
and enlarged lymph nodes, liver, and spleen. Infected animals
also show decreased fertility, loss of appetite, affected body
condition and productivity, emaciation, and early death (OIE,
World Organization for Animal Health, 2012; Health, 2012).
324
not amplied in equines and they are considered less pathogenic. The viruses of these subtypes have been isolated in
South, Central, and North America.
In addition to mosquitoes, other vectors such as Black ies
and mites can also mechanically transmit the epizootic viruses,
meanwhile ticks of the genera Amblyomma and Hyalomma can
be infected by both enzootic and epizootic VEEV strains.
Final Remarks
Ectoparasites and vectorborne pathogens will continue to
present signicant threats to human and animal health
worldwide. On a global basis and especially in poor or developing countries, where they are the major economical impediments to efcient parasite control and efcient livestock
production, the economic toll caused by ectoparasites and
vectorborne diseases is staggering. The outbreaks of endemic
disease, the threats of exotic disease introduction, and fears of
References
Anderson, G.A., Stott, J.L., et al., 1985. Subclinical and clinical bluetongue disease
in cattle: Clinical, pathological and pathogenic considerations. Progress in
Clinical and Biological Research 178, 103107.
Anishchenko, M., Alekseev, V.V., et al., 2006. Venezuelan equine encephalitis: Stateof-the-art. Voprosy Virusologii 51 (6), 1013.
Barnett, S.F., 1974. Babesia of horses in Britain. Veterinary Record 95 (15),
346347.
Barnett, S.F., Brocklesby, D.W., 1971. The isolation of a large Babesia species and
other blood parasites from British cattle. Veterinary Record 88 (10), 260.
de Bellard, M.E., Levine, S., et al., 1989. Venezuelan equine encephalitis. Review.
Investigacin clnica 30 (1), 3158.
Bigler, W.J., McLean, R.G., 1973. Wildlife as sentinels for Venezuelan equine
encephalomyelitis. Journal of the American Veterinary Medical Association 163
(6), 657661.
Blouin, E.F., Barbet, A.F., et al., 2000. Establishment and characterization of an
Oklahoma isolate of Anaplasma marginale in cultured Ixodes scapularis cells.
Veterinary Parasitology 87 (4), 301313.
Brocklesby, D.W., Barnett, S.F., 1972. The tick Haemaphysalis punctata, shown to be
a vector of Theileria mutans in Britain. Veterinary Record 90 (18), 512513.
Castillo-Olivares, J., Wood, J., 2004. West Nile virus infection of horses. Veterinary
Research 35 (4), 467483.
Cecchi, G., Mattioli, R.C., et al., 2008. Land cover and tsetse y distributions in
sub-Saharan Africa. Medical and Veterinary Entomology 22 (4), 364373.
Cecchi, G., Paone, M., et al., 2009. Towards the Atlas of human African
trypanosomiasis. International Journal of Health Geographics 8, 15.
Cunningham, M.P., Brown, C.G., et al., 1989. Theileria parva: The immune status of
calves born of dams immunised against East Coast fever. Research in Veterinary
Science 46 (1), 9094.
Dargie, J.D., Ooijen, C.J., et al., 1993. The FAO/IAEA DGIS Coordinated research
programmes on trypanosomiasis diagnosis and animal production in Africa.
Veterinary Quarterly 15 (2), 7578.
Davis, L.E., Beckham, J.D., et al., 2008. North American encephalitic arboviruses.
Neurologic Clinics 26 (3), 727757, ix.
De La Fuente, J., Vicente, J., et al., 2004. Anaplasma infection in free-ranging
Iberian red deer in the region of Castilla-La Mancha, Spain. Veterinary
Microbiology 100 (34), 163173.
Drummond, R.O., 1985. New methods of applying drugs for the control of
ectoparasites. Veterinary Parasitology 18 (2), 111119.
FAOSTAT, 2012. Available at: http://faostat3.fao.org/home/index.html. (accessed
15.04.14).
FAOWHO, 1969. African trypanosomiasis. Report of a Joint FAOWHO Expert
Committee. World Health Organization Technical Report Series 434, 179.
de la Fuente, J., Garcia-Garcia, J.C., et al., 2002. Infection of tick cells and bovine
erythrocytes with one genotype of the intracellular ehrlichia Anaplasma marginale
325
326
McDermott, J.J., Randolph, T.F., et al., 1999. The economics of optimal health and
productivity in smallholder livestock systems in developing countries. Revue
Scientique et Technique 18 (2), 399424.
McHardy, N., 1974. The effects of injecting anti-erythrocyte serum into calves
infected with Anaplasma marginale. Annals of Tropical Medicine and Parasitology
68 (1), 5157.
McHardy, N., Berger, J., et al., 1980. Comparison of gloxazone, an effective but
toxic anaplasmacide, with imidocarb dihydrochloride. Research in Veterinary
Science 29 (2), 198202.
McHardy, N., Simpson, R.M., 1973. Attempts at immunizing cattle against
anaplasmosis using a killed vaccine. Tropical Animal Health and Production 5
(3), 166173.
Meyer, J.A., Lancaster Jr., J.L., et al., 1982. Comparison of habitat modication,
animal control, and standard spraying for control of the lone star tick. Journal of
Economic Entomology 75 (3), 524529.
Michel, J.F., Lancaster, M.B., et al., 1979. The effect of age, acquired resistance,
pregnancy and lactation on some reactions of cattle to infection with Ostertagia
ostertagi. Parasitology 79 (1), 157168.
Minjauw, B., Otte, M.J., et al., 1998. Effect of different East Coast fever control
strategies on disease incidence in traditionally managed Sanga cattle
in Central Province of Zambia. Preventive Veterinary Medicine 35 (2),
101113.
Montenegro-James, S., 1992. Prevalence and control of babesiosis in the Americas.
Memrias do Instituto Oswaldo Cruz 87 (Suppl 3), 2736.
Morzaria, S.P., Barnett, S.F., et al., 1974. Isolation of Theileria mutans from cattle in
Essex. Veterinary Record 94 (12), 256.
OIE, World Organization for Animal Health, 2012. Manual of Diagnostic Tests and
Vaccines for Terrestrial Animals, World Organization for Animal Health.
Osburn, B.I., 1994. Bluetongue virus. Veterinary Clinics of North America: Food
Animal Practice 10 (3), 547560.
Osburn, B.I., Calisher, C.H., et al., 1985. WHO/FAO working team report:
Immunology. Progress in Clinical and Biological Research 178, 697698.
Osburn, B.I., de Mattos, C.A., et al., 1996. Bluetongue disease and the molecular
epidemiology of viruses from the western United States. Comparative
Immunology Microbiology and Infectious Diseases 19 (3), 181190.
Parsonson, I.M., Bowen, R.A., et al., 1985. WHO/FAO working team report:
Pathology. Progress in Clinical and Biological Research 178, 657660.
Perry, B., Sones, K., 2007. Science for development. Poverty reduction through
animal health. Science 315 (5810), 333334.
Rich, K.M., Perry, B.D., 2011. The economic and poverty impacts of animal diseases
in developing countries: New roles, new demands for economics and
epidemiology. Preventive Veterinary Medicine 101 (34), 133147.
Takken, W., Taylor-Lewis, E.G., et al., 1988. Field studies on animal
trypanosomiasis in Mozambique. I. Effectiveness of the prophylactic drugs
isometamidium chloride and pyrithidium bromide. Tropical Animal Health and
Production 20 (4), 243255.
Thornton, P.K., 2010. Livestock production: Recent trends, future prospects.
Philosophical Transactions of the Royal Society B: Biological Sciences 365
(1554), 28532867.
Tsai, T.F., 1991. Arboviral infections in the United States. Infectious Disease Clinics
of North America 5 (1), 73102.
UNEP, 2012. Africa Environment Outlook 2. Africa Environment Outlook 2 Our
Environment, Our Wealth (AEO-2).
Ward, M.P., Carpenter, T.E., et al., 1994. Host factors affecting seroprevalence of
bluetongue virus infections of cattle. American Journal of Veterinary Research 55
(7), 916920.
Glossary
Antivirals/biotherapeutics Class of medication to treat or
prevent viral infections.
Immunity (adaptive) The mechanism of defense against
pathogens found in vertebrates that is acquired after
exposure to pathogens creating immune memory. Adaptive
immunity is triggered by vaccines and foreign pathogens.
Immunity (innate) The mechanism of defense against
pathogens present in plant and animal cells that functions
in a nonspecic manner. This type of immunity is induced
very rapidly after exposure to pathogens and before the
adaptive immune response.
Interferons Proteins made and released by mammalian
cells in response to the presence of pathogens including
viruses, bacteria, parasites, or tumor cells. Interferons allow
for communication between cells triggering protective
defenses against pathogens or tumors.
Outbreak Occurrence of disease greater than expected in a
particular time and place.
Introduction
Foot-and-mouth disease (FMD) is one of the most contagious
diseases of animals (Grubman and Baxt, 2004). The causative
agent, FMD virus (FMDV), is the type species of the genus
Aphthovirus within the Picornaviridae family (Grubman and Baxt,
2004). The virus is antigenically variable and consists of seven
serotypes, A, O, C, Asia-1, South African Territories 13 (SAT13), and numerous subtypes and strains within each serotype.
More than 70 species of domestic and wild cloven-hoofed
animals including cattle, swine, sheep, and goats are affected
by FMD (Bachrach, 1968). The disease generally causes fever,
lameness, and vesicular lesions on the tongue, snout, feet, and
teats of susceptible animals often resulting in sloughing off of
the epithelium and rupture of vesicles releasing copious
amounts of virus (Figure 1). Disease signs can vary among
species. In particular, sheep do not show overt signs of FMD
(Alexandersen et al., 2002d) and as a result an unnoticed infection of this species can spread an outbreak as rapidly as wild
re as it occurred in the United Kingdom in 2001 (Mahy,
2004).
FMD does not result in high mortality, except when young
animals are infected. However, the disease can have signicant
debilitating effects including weight loss, reduced milk production, loss of draft power and mobility, resulting in a decline in productivity for a period of time. Infection of young
animals can cause myocarditis and death as it occurred in the
1997 FMD outbreak in Taiwan, which caused an approximately 100% fatality rate in suckling pigs (Yang et al., 1999).
Historically, FMD was probably rst recognized in 1546
when the Franciscan monk, Hieronymus Fracastorius,
doi:10.1016/B978-0-444-52512-3.00195-9
327
328
Legend:
Pool 1
Pool 2
Pool 3
Pool 4
Pool 5
Pool 6
Serotype O
Serotype A
Serotype Asia 1
Serotype SAT 1
Serotype SAT 2
Serotype SAT 3
Pool 7
Figure 1 Countries affected by foot-and-mouth disease virus (FMDV). World map showing the different countries that reported an outbreak of
FMDV between January 2010 and February 2013. Each color represents the different FMDV serotypes that affected the indicated region.
Reproduced from Food and Agriculture Organization of the United Nations (FAO). European Commission for the control of FMD. Foot-and-Mouth
Disease Situation. February 2013.
The Agent
Genome Organization
FMDV contains a positive-sense single-stranded ribonucleic
acid (RNA) genome of approximately 8500 nucleotides (nt)
covalently linked at the 5 end to a virus-encoded protein (3B,
also known as VPg) and packed into a nonenveloped icosahedral capsid. Figure 3 shows a schematic diagram of the
FMDV genome displaying the predominant protein products
(a)
(b)
(c)
(d)
329
Figure 2 Common lesions of FMDV in cattle and swine. Vesicular lesions in the tongue and coronary bands of cattle (a and b) and pigs (c and
d). (a) Ruptured vesicles on the tongue and along upper gum with sharp margins of lesions and red raw appearance of exposed dermis. (b) Foot
of a steer with an unruptured vesicle in the heel-bulb. (c) Mouth of pig showing single, 1-day-old, unruptured vesicle at edge of tongue. (d) Swine
feet with vesicles along the coronary bands of main and supernumerary digit with clear presence of sero-brinous in-lling.
330
IRES
PKs
3B
cre
poly(C)
Lpro
1A
1B
1C
1D
3UTR
3B123
2A
**
2B
2C
3Dpol
3Cpro
3A
poly(A)
5UTR
Partial
cleavage
products
P1/2A
P3
P2
1ABC
3B123CD
3AB123
Lpro
1AB
1C
1D
2B
3C
3A
2C
3CD
3D
3B1
3B2
3B3
Structural proteins
Nonstructural proteins
Cleavage sites
Lpro
3Cpro
2A
2 in-frame AUGs* *
Figure 3 Genome organization of FMDV. RNA elements are shown at the 5 and 3 untranslated regions (UTR) and are represented as thin lines.
The 5 UTR consists of S fragment, poly (C) tract, pseudoknots (PKs), cis-acting replicative element (cre) and internal ribosome entry site (IRES).
The ORF is depicted as outlined-open boxes. Filled triangles, squares, and diamonds indicate processing sites for 3Cpro, 2A, and Lpro, respectively.
Posttranslational proteolytic cleavages are shown as partial products as described in the text. Asterisks describe the two AUG initiation codons. The
3 UTR consists of a short stretch of RNA and a poly (A) sequence. 3B (VPg) protein is shown as covalently linked to the 5 end of the
genomic RNA.
Antigenic Variation
FMDV displays seven serotypes and multiple subtypes. New
variants continuously arise due to the number of animal
species that are susceptible to the virus, the different
environments the virus has adapted to, and the fact that viral
replication relies on RdRps. RdRps are rapid and highly processive enzymes but display a fairly low delity resulting in
high mutation rates (Ng et al., 2008). This high error rate leads
to signicant differences of replicated genomes from the parental genome generating quasispecies or cloud of mutants, a
phenomenon that has explained the evolution of replicating
RNA molecules (Domingo et al., 2002; Domingo et al., 1980;
Eigen, 1971). Most of the nucleotide changes in FMDV occur
in the capsid-coding region and lead to antigenic variation.
Some mutations may occur under immune pressure (Borrego
et al., 1993), whereas others become xed even in the absence
of immune pressure (Domingo et al., 1993).
In addition to variation caused by mutation, FMDV has
been shown to undergo RNA recombination in tissue culture
and in eld isolates (Jackson et al., 2007; King et al., 1985;
Wilson et al., 1988).
Antigenic variation is more common in the eld and increases with time, probably as the result of repeated exposure
and immune selective pressure of a highly diverse population
of infected and vaccinated host species (Martinez et al., 1992;
Vosloo et al., 1996).
Pathogenesis
FMDV infects a large variety of cloven-hoofed animals including many wild animals such as antelope, camel, deer,
elephant, elk, giraffe, and llama. However, most pathogenesis
studies have been focused on cattle, swine, sheep, and goats,
given the serious economic consequences that an FMD outbreak may pose to the livestock industry. The ability of these
viruses to infect such a variety of animal species challenges the
analysis of the complex interactions between this agent and
the host (Arzt et al., 2011a,b).
331
Carrier State
Similar to many other viruses, FMDV has evolved mechanisms
to persist in the natural host. In general, the acute phase of
infection is resolved within 14 days; however, some animals,
mostly ruminants, experience a long asymptomatic chronic
infection that can occur in both vaccinated and nonvaccinated
animals (Alexandersen et al., 2002c). These animals are referred to as carriers or persistently infected animals and by
denition those are animals from whom infectious virus can
be recovered from esophagealpharyngeal uids at 28 days or
later after infection (Sutmoller et al., 1968). However, it is not
clear whether carrier animals transmit infection to nave animals or what are the mechanism(s) that mediate the establishment and maintenance of such a state (Moonen and
Schrijver, 2000; Salt, 1993; Sutmoller and Casas, 2002;
Sutmoller et al., 1968; Woodbury, 1995).
The carrier state has been documented for cattle, African
buffalo, water buffalo, and to a lesser extent in sheep, goats,
and other wild ruminants (Sutmoller and Casas, 2002). In
cattle, FMDV can be detected in the epithelium of the pharynx
and soft palate and in the light zones of the germinal centers in
lymphatics of the pharyngeal region after the viremic period
(Juleff et al., 2008; Zhang and Kitching, 2001).
Studies in swine have shown that viral RNA could be detected in tissues at 28 days or longer postinfection, after viremia
had been resolved (Mezencio et al., 1999; Mohamed et al.,
2011; Zhang et al., 2009); however, as no infectious virus could
be recovered, by denition those animals were not considered
carriers. More recently, Rodriguez-Calvo et al. (2011) have
proposed a pseudopersistence state in swine. Infectious FMDV
C-S8c1 was isolated from different lymphoid tissues and the
coronary band epithelia at 17 days postinfection; however,
more studies are required in this species to evaluate if transmission to nave animals is possible at later times.
Little is known about the mechanism that is involved in
FMDV persistence, but involvement of the innate and adaptive
responses have been suggested (Alexandersen et al., 2002c;
Baxt and Mason, 1995; Childerstone et al., 1999; GuzylackPiriou et al., 2006; Mason et al., 1993; Mason et al., 1994);
332
Table 1
FMDV factors
pro
Affected process
Viral counter-mechanism
eIF-4G-1 cleavage (de los Santos et al., 2006, 2007; Devaney et al., 1988;
Kirchweger et al., 1994)
2B 2C and or 2BC
3A
Membrane rearrangements,
secretion and trafcking, and
autophagy
3B
3Cpro
Virulence Factors
Virulence factors enable the virus to establish a niche for
effective colonization and successfully evade the immune
system. Several FMDV NS proteins and RNA regions of the
genomic UTRs are known to disrupt or hijack cellular factors
ultimately favoring virus replication and dissemination in the
host (see Table 1).
Nonstructural Proteins
Virulence of Lpro was determined by developing a leaderless
virus (Piccone et al., 1995a) that was found to be highly attenuated in both cattle and swine (Brown et al., 1996; Chinsangaram et al., 1998; Mason et al., 1997). Studies targeted to
understand the attenuating effect of the leaderless virus demonstrated that Lpro is involved in blocking the innate immune
response by interfering with translation and transcription of
type I interferon (IFN-/) (Chinsangaram et al., 2001; Chinsangaram et al., 1999; de los Santos et al., 2006; de los Santos
et al., 2007). Although blocking of host translation is primarily
Untranslated Regions
The 5 UTR of FMDV is more than 1300 bases in length (Forss
et al., 1984) and folds in complex secondary and tertiary
structures that are involved in many aspects of viral replication
and translation (see Section The Agent). Many host cellular
proteins have been found to interact with the 5 UTR and
include PTBP, ITAF45, PCBP2, and nucleolin (Andreev et al.,
2007; Luz and Beck, 1990; Pacheco and Martinez-Salas, 2010;
Pilipenko et al., 2000). These proteins regulate IRES activity
providing cell type specicity and determining virus spread,
and some are cleaved during infection (Rodriguez-Pulido et al.,
2007). Other IRES-binding proteins, such as Gemin5, downregulate translation, but this effect is neutralized by Lpro
(Pacheco et al., 2009; Pineiro et al., 2012). An additional host
factor that binds specic sequences at the 5 UTR is the RNA
helicase A (RHA), which is required for viral replication
(Lawrence and Rieder, 2009).
The RNA region located between the two AUG initiation
codons (inter AUG) has been shown to be critical for the
initiation of viral translation (Lopez de Quinto and MartinezSalas, 1999; Piccone et al., 1995a) although this effect can be
333
Innate Immunity
Foot-and-mouth disease virus is susceptible to interferon
IFNs are the rst line of the host innate immune defense
against viral infection in mammals (Ank et al., 2006; Basler
and Garcia-Sastre, 2002; Frese et al., 2002). Pretreatment of
cell cultures with all three types of IFN (I, II, and III) (Fensterl
334
Adaptive Immunity
Humoral responses
It is well established that the clearance of FMDV occurs
through an early potent secretion of neutralizing antibodies
starting from day 4 after viral infection. The early B-cell response to FMDV infection in cattle is characterized by the
T-cell response
Swine develop severe but transient lymphopenia and lymphoid depletion in all the lymphoid organs during the acute
phase of FMDV infection. All T-cell subsets, as well as B cells,
are affected and depletion of lymphocytes correlates with the
appearance of viremia (Bautista et al., 2003; Diaz-San Segundo
et al., 2006). In addition, the function of T cells during this
early stage of infection is signicantly impaired. Thus, FMDV
rapidly induces an immune-depressed state in infected swine
that recovers by 47 days after infection when viremia is
abating. These early events provide very favorable conditions
for the virus to both spread systemically and shed into the
environment. Although lymphopenia is a well-characterized
event in swine, the mechanisms involved are not completely
understood. It has been reported that infection of lymphocytes
is a possible cause of lymphopenia in both swine and cattle
(Diaz-San Segundo et al., 2006; Joshi et al., 2009). However,
other groups have failed to detect productive infection of
peripheral blood mononuclear cells during the course of FMD
(Bautista et al., 2003). Nfon et al. (2008) have proposed that
lymphopenia in swine can be caused by an increase in the
amount of systemic IFN during FMDV infection. However, this
IFN production was not reproducible for all FMDV serotypes.
Finally, it is possible that the diminished T-cell responses
could be related to the elevated amounts of IL-10 produced by
the cDCs during infection (Diaz-San Segundo et al., 2009;
Ostrowski et al., 2005), as IL-10 has been reported to have a
role in inducing immunosuppression in vivo (Brooks et al.,
2006). Similarly, lymphopenia and inhibition of T-cell response to mitogen has also been demonstrated in cattle (Joshi
et al., 2009; Perez-Martin et al., 2012), although immunocompetency throughout the FMDV infection has been also
reported (Windsor et al., 2011). Apparently, strain- and species-specic immune responses may account for the differences in the observed responses.
Disease Outbreaks
In Disease-Free Countries
FMD was rst described in Italy in 1546 (Fracastorius, 1546)
and subsequently outbreaks were reported in France, Germany, and the UK in the from the seventeenth to the nineteenth centuries (Mahy, 2004). The earliest reports of FMD in
South America, North America, Asia, and Africa were in the
nineteenth century. In the United States, the rst FMD outbreak was reported in 1870 and subsequently there were eight
additional outbreaks with the last occurring in 1929. During
this period, disease control consisted of inhibition of animal
335
336
In Enzootic Countries
FMD is currently enzootic in many Asian, African, and MiddleEastern countries. Many of these countries do little to control
the disease because of the lack of resources. In 2013 alone
numerous outbreaks have occurred in China, Russia, Taiwan,
Tanzania, Zimbabwe, Botswana, and other countries. Of particular concern is the spread of some serotypes to geographical
areas in which these viruses have not previously been reported
and therefore the susceptible animal population has no immunity. For example, the movement of the SAT-2 virus from
Southern Africa to Saudi Arabia in 2000 was the rst report of
this serotype in Saudi Arabia. More recently in 2012, SAT-2
was reported in Egypt and caused a large outbreak in cattle.
veterinary services. Since FMDV replicates and spreads extremely rapidly it is essential that infected animals are detected
very quickly requiring both vigilance on the part of the livestock owner as well as knowledge of disease signs. Unfortunately, even in developed countries with presumably
knowledgeable livestock owners and a trained veterinary service, FMD outbreaks may still go undetected until the disease
has spread beyond the initial site of infection. This can partially be due to infection of sheep or goats that often do not
show easily detectable disease signs, due to a delay in reporting the index case, or due to a lack of reporting because of
illegal feeding of swine with improperly treated swill (Mahy,
2004). In the 2001, UK FMD outbreak the rst infected animals were pigs on a farm in Northumberland that were not
reported for approximately 3 weeks and in the mean time
resulted in the subsequent infection of sheep on the neighboring farms that were moved to various parts of the country
without showing apparent clinical sings (Scudamore and
Harris, 2002).
Diagnostics
An essential component of a disease control strategy is the use
of diagnostic assays to rapidly conrm or eliminate clinically
suspect animals. For FMD this is especially important as there
are a number of diseases including swine vesicular disease,
vesicular stomatitis, and vesicular exanthema of swine, which
cause vesicular lesions in swine and cattle that cannot be distinguished from FMD (Bachrach, 1968). After positive diagnosis of FMD, it is also necessary to identify the serotype and
strain of the virus as this information is necessary to choose
the appropriate antigen to use in vaccination-to-slaughter or
vaccination-to-live campaigns. Sensitive diagnostic assays are
also needed to distinguish infected animals from vaccinated
animals and perform epidemiological surveillance to conrm
the nave status of animals in the eld in order to allow for
resumption of international trade.
Currently, the OIE suggests the use of a number of diagnostic techniques depending on the type of eld samples
obtained. The recommended tissue of choice is epithelium
or vesicular uid, but other samples including serum or
esophagealpharyngeal (OP) uids can also be used. Virus
isolation, virus neutralization, reverse-transcription polymerase chain reaction (RT-PCR), enzyme-linked immunosorbent assay (ELISA), or complement xation assays can be used
to identify FMDV. More recently, lateral ow devices are being
developed to allow for rapid pen-side testing.
The need for rapid diagnosis is critical. Currently, FMD is
conrmed by ELISA, which takes approximately 34 h. A
negative result must be conrmed by virus isolation in tissue
culture, which can take up to 4 days and is not compatible
with a rapid response. Therefore, more recently RT-PCR and
real-time RT-PCR assays have been developed. Results from
the later assay can be obtained in 2 h (Callahan et al., 2002).
To differentiate infected animals from vaccinated animals a
number of tests have been developed. These are all based on
the premise that infected or convalescent animals have antibodies to the viral NS proteins as well as the viral structural
proteins, whereas vaccinated animals should only have
Vaccines
The current FMD vaccine is an inactivated whole-virus preparation that is formulated with various adjuvants before use.
As FMDV is an antigenically variable virus, different vaccines
are required for each serotype and often different vaccines are
necessary to protect against various strains or subtypes within
a serotype. The vaccine is produced by infection of suspension
cultures of BHK-21 cells with live virus and therefore production requires a high-containment facility. In-depth reviews
by Doel (Doel, 2003) and Barteling (Barteling and Cassimi,
2004) discuss the history, production, and testing of inactivated FMD vaccines.
Various countries have established regional FMD vaccine
banks that maintain vaccines against circulating viruses (Doel,
2003; Grubman and Baxt, 2004). The United States, Canada,
and Mexico in 1982 established the North American FMD
Vaccine Bank which is located at the Plum Island Animal
Disease Center (PIADC) off the coast of Long Island, NY and is
jointly administered. Initially, vaccines were stored as formulated antigen that only had approximately a 1-year shelf life.
More recently, vaccine banks store concentrated antigen in the
gaseous phase of liquid nitrogen (Doel, 2003) to increase
antigen shelf life (Doel and Pullen, 1990). However, to be
used in the eld the concentrated antigen has to be shipped
back to the manufacturer for formulation and returned to the
country where the outbreak is occurring. To maintain concentrated FMD antigen that will be protective against circulating FMDV strains it is necessary to continually monitor virus
in the eld and determine if these strains are sufciently related to available vaccine antigen. If not appropriate, new
vaccine strains have to be produced.
Although inactivated FMD vaccines have been effective in
eliminating FMDV from Western Europe and some countries
in South America, there are a number of concerns with their
use and as a result vaccination has often not been used as part
of an FMD disease control approach. (1) As already mentioned
production of inactivated FMD vaccines requires expensive
high-containment facilities and effective virus inactivation.
Unfortunately, the 2007 FMD outbreak in the UK was the
result of escape of live virus from the Pirbright FMD facility.
(2) Vaccine production requires passage of live virus in BHK21 cells. There is evidence that passage of virus in cell culture
can result in the selection of antigenic variants with altered
receptor binding, antigenic structure, and virulence (Bolwell
et al., 1989). (3) Depending on the purity of the vaccine
337
338
(2013) attempted to enhance stability of baculovirusexpressed FMDV A22 empty capsids and also reduce expression of the toxic 3Cpro. The mutated capsids were more
stable than the WT capsids to both heat and acid and 3C
expression and catalytic activity was reduced. Two of the four
cattle vaccinated twice with WT empty capsids and an oil adjuvant and three of the four animals inoculated with mutant
capsids were protected from challenge with homologous
virulent virus (Porta et al., 2013).
Other investigators have used viral vectors, including poxvirus, pseudorabies virus, and replication-defective human
adenovirus (Ad5), as delivery vehicles (Grubman and Baxt,
2004; Zhang et al., 2011). Thus far, the most efcacious viralvectored delivery vehicle is the Ad5 system. The Ad5-FMDV
A24 (Ad5-A24) vector constructed by Grubman and colleagues
(Moraes et al., 2001) is protective, after one inoculation, as
early as 7 days postvaccination in both swine (Moraes et al.,
2002) and cattle (Grubman et al., 2010; Pacheco et al., 2005).
More recent studies with second-generation vectors containing
the NS protein 2B coding region demonstrated enhanced efcacy in challenge studies in swine (Pena et al., 2008) and
cattle (Moraes et al., 2011). Furthermore, by changing the
route and sites of inoculation the protective dose could be
signicantly reduced (Grubman et al., 2012b). The US Department of Agriculture (USDA) in collaboration with the US
Department of Homeland Security and GenVec Inc. have
produced this vaccine on the US mainland in BSL2 facilities
and tested it in cattle following the requirements of the Center
for Veterinary Biologics of the Animal Plant and Health Inspection Service, USDA, which included safety testing of the
vaccine in cattle at three sites on the US mainland. In June
2012 this vaccine was granted a conditional license for inclusion in the US National Veterinary Vaccine Stockpile for use in
cattle in the United States in the event of an emergency
situation.
Live-attenuated vaccines
A number of reviews have described early attempts to develop
live-attenuated FMD vaccines (Bachrach, 1968; Brooksby,
1982; Mason and Grubman, 2009). These vaccines are economically cost effective to produce, should cause only mild or
no disease, and theoretically can induce both adaptive and
cell-mediated immune responses. Live-attenuated FMD viruses
were developed by passage of WT virus in nonpermissive hosts
including mice, rabbits, and embryonated eggs until their
virulence for cattle was attenuated. However, although this
approach has been successful in the development of very
effective vaccines against yellow fever and polio, it has not
been successful against FMD. Field studies in various countries
demonstrated that although the attenuated strains could induce a degree of protection in a particular species it was often
virulent in other susceptible species. In addition, there is
concern that attenuated viruses created in this manner can
revert to virulence.
More recently, scientists have used reverse genetics to mutate selected portions of the viral genome. McKenna et al.
(1995) removed a portion of the region of VP1 required for
binding to cells. This virus did not induce disease in inoculated swine or cattle and protected cattle from challenge with
virulent FMDV. In another approach Piccone et al. (1995a)
Antivirals/Biotherapeutics
Inactivated and Ad5-FMD vaccines can only induce complete
protective immunity by 7 days postvaccination (Golde et al.,
2005; Moraes et al., 2002). Thus, before 7 days vaccinated
animals exposed to virulent FMDV are still susceptible to the
disease. As FMDV replicates and spreads very rapidly it is important, especially in an outbreak in an FMD-free country, to
339
Acknowledgments
Concluding Remarks
A wealth of new information has been obtained on FMDV at
the molecular level, including many of the functions of the
viral-encoded proteins, the interaction of the virus with the
host, the pathogenesis of the disease, and the effect of infection on the host immune response. This information and
the tools of reverse genetics and immunology have allowed us
to develop new approaches to more rapidly detect and
340
References
Acharya, R., Fry, E., Stuart, D., et al., 1989. The three-dimensional structure of footand-mouth disease virus at 2.9A resolution. Nature 337 (6209), 709716.
Ahl, R., Rump, A., 1976. Assay of bovine interferons in cultures of the porcine cell
line IB-RS-2. Infection and Immunity 14 (3), 603606.
Alexandersen, S., Brotherhood, I., Donaldson, A.I., 2002a. Natural aerosol
transmission of foot-and-mouth disease virus to pigs: Minimal infectious dose
for strain O1 Lausanne. Epidemiology and Infection 128 (2), 301312.
Alexandersen, S., Donaldson, A.I., 2002b. Further studies to quantify the dose of
natural aerosols of foot-and-mouth disease virus for pigs. Epidemiology and
Infection 128 (2), 313323.
Alexandersen, S., Zhang, Z., Donaldson, A.I., 2002c. Aspects of the persistence of
foot-and-mouth disease virus in animals the carrier problem. Microbes and
Infection 4 (10), 10991110.
Alexandersen, S., Zhang, Z., Donaldson, A.I., Garland, A.J.M., 2003. The
pathogenesis and diagnosis of foot-and-mouth disease. Journal of Comparative
Pathology 129, 136.
Alexandersen, S., Zhang, Z., Reid, S.M., Hutchings, G.H., Donaldson, A.I., 2002d.
Quantities of infectious virus and viral RNA recovered from sheep and cattle
experimentally infected with foot-and-mouth disease virus O UK 2001. Journal of
General Virology 83 (Pt 8), 19151923.
Almeida, M., Rieder, E., Chinsangaram, J., et al., 1998. Construction and evaluation
of an attenuated vaccine for foot-and-mouth disease: Difculty adapting the
leader proteinase-deleted strategy to the serotype O1 virus. Virus Research 55
(1), 4960.
Ambros, V., Baltimore, D., 1980. Purication and properties of a HeLa cell enzyme
able to remove the 5-terminal protein from poliovirus RNA. Journal of Biological
Chemistry 255 (14), 67396744.
Ambros, V., Pettersson, R.F., Baltimore, D., 1978. An enzymatic activity in
uninfected cells that cleaves the linkage between poliovirion RNA and the 5
terminal protein. Cell 15 (4), 14391446.
Andreev, D.E., Fernandez-Miragall, O., Ramajo, J., et al., 2007. Differential factor
requirement to assemble translation initiation complexes at the alternative start
codons of foot-and-mouth disease virus RNA. RNA 13 (8), 13661374.
Ank, W., West, H., Paludan, S.R., 2006. IFN-lambda: Novel antiviral cytokines.
Journal of Interferon & Cytokine Research 26, 373379.
Arias, A., Perales, C., Escarmis, C., Domingo, E., 2010. Deletion mutants of
VPg reveal new cytopathology determinants in a picornavirus. PLoS One 5,
e10735.
Arzt, J., Baxt, B., Grubman, M.J., et al., 2011b. The pathogenesis of foot-and-mouth
disease II: Viral pathways in swine, small ruminants, and wildlife; myotropism,
chronic syndromes, and molecular virus-host interactions. Transboundary and
Emerging Diseases 58 (4), 305326.
Arzt, J., Juleff, N., Zhang, Z., Rodriguez, L.L., 2011a. The pathogenesis of foot-andmouth disease I: Viral pathways in cattle. Transboundary and Emerging Diseases
58 (4), 291304.
Arzt, J., Pacheco, J.M., Rodriguez, L.L., 2010. The early pathogenesis of foot-andmouth disease in catte after aerosol inoculation. Identication of the nasopharynx
as the primary site of infection. Veterinary Pathology 47, 10481063.
Bablanian, G.M., Grubman, M.J., 1993. Characterization of the foot-and-mouth
disease virus 3C protease expressed in Escherichia coli. Virology 197 (1),
320327.
Bachrach, H.L., 1968. Foot-and-mouth disease. Annual Review of Microbiology 22,
201244.
Bachrach, H.L., Moore, D.M., McKercher, P.D., Polatnick, J., 1975. Immune and
antibody responses to an isolated capsid protein of foot-and-mouth disease
virus. Journal of Immunology 115 (6), 16361641.
Baranowski, E., Sevilla, N., Verdaguer, N., et al., 1998. Multiple virulence
determinants of foot-and-mouth disease virus in cell culture. Journal of Virology
72 (8), 63626372.
Barteling, S.J., Cassimi, N.I., 2004. Very fast (and safe) inactivation of foot-andmouth disease virus and enteroviruses by combination of binary ethyleneimine
and formaldehyde. Developmental Biology (Basel) 119, 449455.
Barton, D.J., O'Donnell, B.J., Flanegan, J.B., 2001. 5 cloverleaf in poliovirus RNA
is a cis-acting replication element required for negative-strand synthesis. EMBO
Journal 20 (6), 14391448.
Basler, C.F., Garcia-Sastre, A., 2002. Viruses and the type I interferon antiviral
system: Induction and evasion. International Reviews of Immunology 21,
305337.
Bautista, E.M., Ferman, G.S., Golde, W.T., 2003. Induction of lymphopenia and
inhibition of T cell function during acute infection of swine with foot and mouth
disease virus (FMDV). Veterinary Immunology and Immunopathology 92 (12),
6173.
Bautista, E.M., Ferman, G.S., Gregg, D., et al., 2005. Constitutive expression of
alpha interferon by skin dendritic cells confers resistance to infection by footand-mouth disease virus. Journal of Virology 79, 48384847.
Baxt, B., Mason, P.W., 1995. Foot-and-mouth disease virus undergoes restricted
replication in macrophage cell cultures following Fc receptor-mediated
adsorption. Virology 207 (2), 503509.
Beard, C.W., Mason, P.W., 2000. Genetic determinants of altered virulence of
Taiwanese foot-and-mouth disease virus. Journal of Virology 74 (2), 987991.
Belsham, G.J., 2013. Inuence of the Leader protein coding region of foot-andmouth disease virus on virus replication. Journal of General Virology 94 (Pt 7),
14861495.
Belsham, G.J., Brangwyn, J.K., 1990. A region of the 5 noncoding region of footand-mouth disease virus RNA directs efcient internal initiation of protein
synthesis within cells: Involvement with the role of L protease in translational
control. Journal of Virology 64 (11), 53895395.
Belsham, G.J., McInerney, G.M., Ross-Smith, N., 2000. Foot-and-mouth
disease virus 3C protease induces cleavage of translation initiation factors
eIF4A and eIF4G within infected cells. Journal of Virology 74 (1),
272280.
Berger, H.G., Straub, O.C., Ahl, R., Tesar, M., Marquardt, O., 1990. Identication of
foot-and-mouth disease virus replication in vaccinated cattle by antibodies to
non-structural virus proteins. Vaccine 8 (3), 213216.
Bergmann, I.E., de Mello, P.A., Neitzert, E., Beck, E., Gomes, I., 1993. Diagnosis of
persistent aphthovirus infection and its differentiation from vaccination response
in cattle by use of enzyme-linked immunoelectrotransfer blot analysis with
bioengineered nonstructural viral antigens. American Journal of Veterinary
Research 54 (6), 825831.
Bergmann, I.E., Malirat, V., Auge de Mello, P., Gomes, I., 1996. Detection of footand-mouth disease viral sequences in various uids and tissues during
persistence of the virus in cattle. American Journal of Veterinary Research 57 (2),
134137.
Bergmann, I.E., Malirat, V., Neitzert, E., et al., 2000. Improvement of a
serodiagnostic strategy for foot-and-mouth disease virus surveillance in cattle
under systematic vaccination: A combined system of an indirect ELISA 3ABC
with an enzyme-linked immunoelectrotransfer blot assay. Archives of Virology
145, 473489.
Berryman, S., Brooks, E., Burman, A., et al., 2012. Foot-and-mouth disease virus
induces autophagosomes during cell entry via a class III phosphatidylinositol 3kinase-independent pathway. Journal of Virology 86 (23), 1294012953.
Berryman, S., Clark, S., Monaghan, P., Jackson, T., 2005. Early events in integrin
alphavbeta6-mediated cell entry of foot-and-mouth disease virus. Journal of
Virology 79 (13), 85198534.
Birtley, J.R., Knox, S.R., Jaulent, A.M., et al., 2005. Crystal structure of foot-andmouth disease virus 3C protease. New insights into catalytic mechanism
and cleavage specicity. Journal of Biological Chemistry 280 (12),
1152011527.
Bolwell, C., Brown, A.L., Barnett, P.V., et al., 1989. Host cell selection of antigenic
variants of foot-and-mouth disease virus. Journal of General Virology 70 (Pt 1),
4557.
Borca, M.V., Fernandez, F.M., Sadir, A.M., Braun, M., Schudel, A.A., 1986. Immune
response to foot-and-mouth disease virus in a murine experimental model:
Effective thymus-independent primary and secondary reaction. Immunology 59
(2), 261267.
Borrego, B., Novella, I.S., Giralt, E., Andreu, D., Domingo, E., 1993. Distinct
repertoire of antigenic variants of foot-and-mouth disease virus in the presence
or absence of immune selection. Journal of Virology 67 (10), 60716079.
Brooksby, J.B., 1982. Portraits of viruses: Foot-and-mouth disease virus.
Intervirology 18 (12), 123.
Brooks, D.G., Trilo, M.J., Edelmann, K.H., et al., 2006. Interleukin-10 determines
viral clearance or persistence in vivo. Nature Medicine 12 (11), 13011309.
Brown, C.C., Meyer, R.F., Olander, H.J., House, C., Mebus, C.A., 1992. A
pathogenesis study of foot-and-mouth disease in cattle, using in situ
hybridization. Canadian Journal of Veterinary Research 56 (3), 189193.
Brown, C.C., Piccone, M.E., Mason, P.W., McKenna, T.S., Grubman, M.J., 1996.
Pathogenesis of wild-type and leaderless foot-and-mouth disease virus in cattle.
Journal of Virology 70 (8), 56385641.
Brown, F., 1992. New approaches to vaccination against foot-and-mouth disease.
Vaccine 10 (14), 10221026.
Brown, J.K., McAleese, S.M., Thornton, E.M., et al., 2006. Integrin-alphavbeta6, a
putative receptor for foot-and-mouth disease virus, is constitutively expressed in
ruminant airways. Journal of Histochemistry and Cytochemistry 54 (7), 807816.
Burrows, R., 1968. Excretion of foot-and-mouth disease prior to the development of
lesions. Veterinary Record 82, 387388.
Caliguiri, L.A., Tamm, I., 1968. Action of guanidine on the replication of poliovirus
RNA. Virology 35 (3), 408417.
Callahan, J.D., Brown, F., Osorio, F.A., et al., 2002. Use of a portable real-time
reverse transcriptase-polymerase chain reaction assay for rapid detection of footand-mouth disease virus. Journal of the American Veterinary Medical Association
220 (11), 16361642.
Cheneau, Y., Rweyemamu, M.M., Astudillo, V., Lubroth, J., 2003. Global initiatives
for the progressive control and eradication of foot-and-mouth disease. In: Vicari,
B.D.a.M. (Ed.), Foot and Mouth Disease: Control Strategies. Paris: Elsevier,
pp. 247257.
Chen, W., Yan, W., Du, Q., et al., 2004. RNA interference targeting VP1 inhibits
foot-and-mouth disease virus replication in BHK-21 cells and suckling mice.
Journal of Virology 78 (13), 69006907.
Childerstone, A.J., Cedillo-Baron, L., Foster-Cuevas, M., Parkhouse, R.M., 1999.
Demonstration of bovine CD8 T-cell responses to foot-and-mouth disease
virus. Journal of General Virology 80 (Pt 3), 663669.
Chinsangaram, J., Koster, M., Grubman, M.J., 2001. Inhibition of L-deleted footand-mouth disease virus replication by alpha/beta interferon involves doublestranded RNA-dependent protein kinase. Journal of Virology 12, 54985503.
Chinsangaram, J., Mason, P.W., Grubman, M.J., 1998. Protection of swine by live
and inactivated vaccines prepared from a leader proteinase-decient serotype A12
foot-and-mouth disease virus. Vaccine 16 (16), 15161522.
Chinsangaram, J., Moraes, M.P., Koster, M., Grubman, M.J., 2003. Novel viral
disease control strategy: Adenovirus expressing alpha interferon rapidly protects
swine from foot-and-mouth disease. Journal of Virology 77, 16211625.
Chinsangaram, J., Piccone, M.E., Grubman, M.J., 1999. Ability of foot-and-mouth
disease virus to form plaques in cell culture is associated with suppression of
alpha/beta interferon. Journal of Virology 73 (12), 98919898.
Clarke, B.E., Sangar, D.V., 1988. Processing and assembly of foot-and-mouth
disease virus proteins using subgenomic RNA. Journal of General Virology 69
(Pt 9), 23132325.
Collen, T., Pullen, L., Doel, T.R., 1989. T cell-dependent induction of antibody
against foot-and-mouth disease virus in a mouse model. Journal of General
Virology 70 (Pt 2), 395403.
Cornell, C.T., Kiosses, W.B., Harkins, S., Whitton, J.L., 2006. Inhibition of protein
trafcking by coxsackievirus B3: Multiple viral proteins target a single organelle.
Journal of Virology 80, 66376647.
Cottam, E.M., Wadsworth, J., Shaw, A.E., et al., 2008. Transmission pathways of
foot-and-mouth disease virus in the United Kingdom in 2007. PLoS Pathogens 4
(4), e1000050.
Curry, S., Abrams, C.C., Fry, E., et al., 1995. Viral RNA modulates the acid
sensitivity of foot-and-mouth disease virus capsids. Journal of Virology 69 (1),
430438.
Curry, S., Fry, E., Blakemore, W., et al., 1996. Perturbations in the surface structure
of A22 Iraq foot-and-mouth disease virus accompanying coupled changes in host
cell specicity and antigenicity. Structure 4 (2), 135145.
Curry, S., Fry, E., Blakemore, W., et al., 1997. Dissecting the roles of VP0 cleavage
and RNA packaging in picornavirus capsid stabilization: The structure of empty
capsids of foot-and-mouth disease virus. Journal of Virology 71 (12),
97439752.
Dawe, P.S., Flanagan, F.O., Madekurozwa, R.L., et al., 1994a. Natural transmission
of foot-and-mouth disease virus from African buffalo (Syncerus caffer) to cattle in
a wildlife area of Zimbabwe. Veterinary Record 134 (10), 230232.
Dawe, P.S., Sorensen, K., Ferris, N.P., et al., 1994b. Experimental transmission of
foot-and-mouth disease virus from carrier African buffalo (Syncerus caffer) to
cattle in Zimbabwe. Veterinary Record 134 (9), 211215.
Devaney, M.A., Vakharia, V.N., Lloyd, R.E., Ehrenfeld, E., Grubman, M.J., 1988.
Leader protein of foot-and-mouth disease virus is required for cleavage of the
p220 component of the cap-binding protein complex. Journal of Virology 62
(11), 44074409.
341
Dias, C.C., Moraes, M.P., Diaz-San Segundo, F., de los Santos, T., Grubman, M.J.,
2011. Porcine type I interferon rapidly protects swine against challenge with
multiple serotypes of foot-and-mouth disease virus. Journal of Interferon and
Cytokine Research 31, 227236.
Dias, C.C., Moraes, M.P., Weiss, M., et al., 2012. Novel antiviral therapeutics to
control foot-and-mouth disease. Journal of Interferon and Cytokine Research 32,
462473.
Diaz-San Segundo, F., Dias, C.C., Moraes, M.P., et al., 2013a. Venezuelan equine
encephalitis replicon particles can induce rapid protection against foot-and-mouth
disease. Journal of Virology 87, 54475460.
Diaz-San Segundo, F., Montiel, N., de los Santos, T., Grubman, M., 2013b.
Understanding the Mechanisms of Interferon-Induced Protection against Footand-Mouth Disease. Hong Kong: iConcept Press.
Diaz-San Segundo, F., Moraes, M.P., de los Santos, T., Dias, C.C.,
Grubman, M.J., 2010. Interferon-induced protection against foot-and-mouth
disease virus infection correlates with enhanced tissue-specic innate immune
cell inltration and interferon-stimulated gene expression. Journal of Virology 84,
20632077.
Diaz-San Segundo, F., Rodriguez-Calvo, T., de Avila, A., Sevilla, N., 2009.
Immunosuppresion during acute infection with foot-and-mouth disease virus in
swine is mediated by IL-10. PLoS One 4, e5659.
Diaz-San Segundo, F., Salguero, F.J., de Avila, A., et al., 2006. Selective
lymphocyte depletion during the early stage of the immune response to foot-andmouth disease virus infection in swine. Journal of Virology 80, 23692379.
Diaz-San Segundo, F., Weiss, M., Perez-Martin, E., et al., 2012. Inoculation of swine
with foot-and-mouth disease SAP-mutant virus induces early protection against
disease. Journal of Virology 86, 13161327.
Daz-San Segundo, F., Weiss, M., Perez-Martn, E., et al., 2011. Antiviral activity of
bovine type III interferon against foot-and-mouth disease virus. Virology 413,
283292.
Doedens, J.R., Kirkegaard, K., 1995. Inhibition of cellular protein secretion by
poliovirus proteins 2B and 3A. EMBO Journal 14 (5), 894907.
Doel, T.R., 2003. FMD vaccines. Virus Research 91 (1), 8199.
Doel, T.R., Pullen, L., 1990. International bank for foot-and-mouth disease vaccine:
Stability studies with virus concentrates and vaccines prepared from them.
Vaccine 8, 473478.
Domingo, E., Baranowski, E., Escarmis, C., Sobrino, F., 2002. Foot-and-mouth
disease virus. Comparative Immunology, Microbiology and Infectious Diseases
25 (56), 297308.
Domingo, E., Davila, M., Ortin, J., 1980. Nucleotide sequence heterogeneity of the
RNA from a natural population of foot-and-mouth-disease virus. Gene 11 (34),
333346.
Domingo, E., Diez, J., Martinez, M.A., et al., 1993. New observations on antigenic
diversication of RNA viruses. Antigenic variation is not dependent on immune
selection. Journal of General Virology 74 (Pt 10), 20392045.
Donaldson, A.I., 1987. Foot-and-mouth disease: The principal features. Irish
Veterinary Journal 41, 325327.
Dunn, C.S., Donaldson, A.I., 1997. Natural adaption to pigs of a Taiwanese isolate
of foot-and-mouth disease virus. Veterinary Record 141 (7), 174175.
Eigen, M., 1971. Self organization of matter and the evolution of biological
macromolecules. Naturwissenschaften 58 (10), 465523.
Ellard, F.M., Drew, J., Blakemore, W.E., Stuart, D.I., King, A.M., 1999. Evidence for
the role of His-142 of protein 1C in the acid-induced disassembly of foot-andmouth disease virus capsids. Journal of General Virology 80 (Pt 8), 19111918.
Fajardo, T.J., Rosas, M.F., Sobrino, F., Martinez-Salas, E., 2012. Exploring IRES
region accessibility by interference of foot-and-mouth disease virus infectivity.
PLoS One 7, e41382.
Falk, M.M., Grigera, P.R., Bergmann, I.E., et al., 1990. Foot-and-mouth disease
virus protease 3C induces specic proteolytic cleavage of host cell histone H3.
Journal of Virology 64 (2), 748756.
Falk, M.M., Sobrino, F., Beck, E., 1992. VPg gene amplication correlates with
infective particle formation in foot-and-mouth disease virus. Journal of Virology
66 (4), 22512260.
Fensterl, V., Sen, G.C., 2009. Interferons and viral infections. Biofactors 35, 1420.
Ferrer-Orta, C., Agudo, R., Domingo, E., Verdaguer, E., 2009. Structural insights into
replication initiation and elongation processes by the FMDV RNA-dependent RNA
polymerase. Current Opinion in Structural Biology 19, 752758.
Ferrer-Orta, C., Arias, A., Agudo, R., et al., 2006. The structure of a protein primerpolymerase complex in the initiation of genome replication. EMBO Journal 25,
880888.
Forss, S., Strebel, K., Beck, E., Schaller, H., 1984. Nucleotide sequence and genome
organization of foot-and-mouth disease virus. Nucleic Acids Research 12 (16),
65876601.
342
Fowler, V.L., Barnett, P.V., 2012. Progress in the development of DNA vaccines
against foot-and-mouth disease. Expert Review of Vaccines 11, 481493.
Fowler, V.L., Bashiruddin, J.B., Maree, F.F., et al., 2011. Foot-and-mouth disease
marker vaccine: Cattle protection with a partial VP1 G-H loop deleted virus
antigen. Vaccine 29 (46), 84058411.
Fracastorius, H., 1546. De sympathia et antipathia rerum liber unus. De contagione
et contagiosis morbis et eorum curatione liber I, Venice, Heirs of L.A. Junta.
Frese, M., Schwarzle, V., Barth, K., et al., 2002. Interferon-gamma inhibits
replication of subgenomic and genomic hepatitis C virus RNAs. Hepatology 35,
694703.
Fry, E.E., Lea, S.M., Jackson, T., et al., 1999. The structure and function of a footand-mouth disease virus-oligosaccharide receptor complex. EMBO Journal 18
(3), 543554.
Giraudo, A.T., Beck, E., Strebel, K., et al., 1990. Identication of a nucleotide
deletion in parts of polypeptide 3A intwo independent attenuated aphthovirus
strains. Virology 177, 780783.
Gladue, D.P., O'Donnell, V., Baker-Branstetter, R., et al., 2013. Foot-and-mouth
disease virus modulates cellular vimentin for virus survival. Journal of Virology
87 (12), 67946803.
Gladue, D.P., O'Donnell, V., Baker-Branstetter, R., et al., 2012. Foot-and-mouth
disease virus nonstructural protein 2C interacts with Beclin1, modulating virus
replication. Journal of Virology 86 (22), 1208012090.
Golde, W.T., Pacheco, J.M., Duque, H., et al., 2005. Vaccination against foot-andmouth disease virus confers complete clinical protection in 7 days and partial
protection in 4 days: Use in emergency outbreak response. Vaccine 23,
57755782.
Grubman, M.J., 2003. New approaches to rapidly control foot-and-mouth disease
outbreaks. Expert Review of Anti-infective Therapy 1 (4), 579586.
Grubman, M.J., Baxt, B., 2004. Foot-and-mouth disease. Clinical Microbiology
Reviews 17 (2), 465493.
Grubman, M.J., de los Santos, T., 2012a. Foot-and-mouth disease virus L peptidase.
In: Rawlings, G.S.N.D. (Ed.), Handbook of Proteolytic Enzymes, third ed.
Waltham, MA: Elsevier Ltd.
Grubman, M.J., Diaz-San Segundo, F., Dias, C.C.A., et al., 2012b. Use of
replication-defective adenoviruses to develop vaccines and biotherapeutics
against foot-and-mouth disease. Future Virology 7, 767778.
Grubman, M.J., Moraes, M., Schutta, C., et al., 2010. Adenovirus serotype 5vectored foot-and-mouth disease subunit vaccines: The rst decade. Future
Virology 5, 5164.
Grubman, M.J., Morgan, D.O., Kendall, J., Baxt, B., 1985. Capsid intermediates
assembled in a foot-and-mouth disease virus genome RNA-programmed cell-free
translation system and in infected cells. Journal of Virology 56 (1), 120126.
Grubman, M.J., Zellner, M., Bablanian, G., Mason, P.W., Piccone, M.E., 1995.
Identication of the active-site residues of the 3C proteinase of foot-and-mouth
disease virus. Virology 213 (2), 581589.
Guarne, A., Tormo, J., Kirchweger, R., et al., 1998. Structure of the foot-and-mouth
disease virus leader protease: A papain-like fold adapted for self-processing and
eIF4G recognition. EMBO Journal 17 (24), 74697479.
Gulevich, A.Y., Yusupova, R.A., Drygin, Y.F., 2002. VPg unlinkase, the
phosphodiesterase that hydrolyzes the bond between VPg and picornavirus RNA:
A minimal nucleic moiety of the substrate. Biochemistry (Mosc) 67 (6),
615621.
Guzylack-Piriou, L., Bergamin, F., Gerber, M., McCullough, K.C., Summereld, A.,
2006. Plasmacytoid dendritic cell activation by foot-and-mouth disease virus
requires immune complexes. European Journal of Immunology 36 (7),
16741683.
He, C., Klionsky, D.J., 2009. Regulation mechanisms and signaling pathways of
autophagy. Annual Review of Genetics 43, 6793.
Herold, J., Andino, R., 2001. Poliovirus RNA replication requires genome
circularization through a protein-protein bridge. Molecular Cell 7 (3),
581591.
Hyde, J.L., Blackwell, J.H., Callis, J.J., 1975. Effect of pasteurization and evaporation
on foot-and-mouth disease virus in whole milk from infected cows. Canadian
Journal of Comparative Medicine 39, 305309.
Jackson, A.L., O'Neill, H., Maree, F., et al., 2007. Mosaic structure of foot-andmouth disease virus genomes. Journal of General Virology 88 (Pt 2),
487492.
Jackson, T., Ellard, F.M., Ghazaleh, R.A., et al., 1996. Efcient infection of cells in
culture by type O foot-and-mouth disease virus requires binding to cell surface
heparan sulfate. Journal of Virology 70 (8), 52825287.
Joo, Y.-S., Ann, S.-H., Kim, O.-K., Lubroth, J., Sur, J.-H., 2002. Foot-and-mouth
disease eradication efforts in the Republic of Korea. Canadian Journal of
Veterinary Research 66, 122124.
Joshi, G., Sharma, R., Kakker, N.K., 2009. Phenotypic and functional characterization
of T-cells and in vitro replication of FMDV serotypes in bovine lymphocytes.
Vaccine 27 (48), 66566661.
Juleff, N., Windsor, M., Lefevre, E.A., et al., 2009. Foot-and-mouth disease virus can
induce a specic and rapid CD4 T-cell-independent neutralizing and isotype
class-switched antibody response in naive cattle. Journal of Virology 83,
36263636.
Juleff, N., Windsor, M., Reid, E., et al., 2008. Foot-and-mouth disease virus persists
in the light zone of germinal centres. PLoS One 3 (10), e3434.
King, A.M., McCahon, D., Saunders, K., Newman, J.W., Slade, W.R., 1985. Multiple
sites of recombination within the RNA genome of foot-and-mouth disease virus.
Virus Research 3 (4), 373384.
Kirchweger, R., Ziegler, E., Lamphear, B.J., et al., 1994. Foot-and-mouth disease
virus leader proteinase: Purication of the Lb form and determination of its
cleavage site on eIF-4 gamma. Journal of Virology 68 (9), 56775684.
Kitching, P., 1992. Foot-and-mouth disease. In: Andrews, A.H., Blowey, R.W., Boyd,
H., Eddy, R.G. (Eds.), Bovine Medicine: Diseases and Husbandry of Cattle.
Oxford: Blackwell Science Inc., pp. 537543.
Kitching, P., Alexandersen, S., 2002. Clinical variation in foot-and-mouth disease:
Pigs. Revue Scientique et Technique (International Ofce of Epizootics) 21,
513518.
Kleid, D.G., Yansura, D., Small, B., et al., 1981. Cloned viral protein vaccine for
foot-and-mouth disease: Responses in cattle and swine. Science 214 (4525),
11251129.
Kleina, L.G., Grubman, M.J., 1992. Antiviral effects of a thiol protease
inhibitor on foot-and-mouth disease virus. Journal of Virology 66 (12),
71687175.
Knipe, T., Rieder, E., Baxt, B., Ward, G., Mason, P.W., 1997. Characterization of
synthetic foot-and-mouth disease virus provirions separates acid-mediated
disassembly from infectivity. Journal of Virology 71 (4), 28512856.
Kozak, M., 1978. How do eucaryotic ribosomes select initiation regions in
messenger RNA? Cell 15, 11091123.
Kuhn, R., Luz, N., Beck, E., 1990. Functional analysis of the internal translation
initiation site of foot- and-mouth disease virus. Journal of Virology 64 (10),
46254631.
Lannes, N., Python, S., Summereld, A., 2012. Interplay of foot-and-mouth disease
virus, antibodies and plasmacytoid dendritic cells: Virus opsonization under nonneutralizing conditions results in enhanced interferon-alpha responses. Veterinary
Research 43, 64.
Lawrence, P., Rieder, E., 2009. Identication of RNA helicase A as a new host factor
in the replication cycle of foot-and-mouth disease virus. Journal of Virology 83
(21), 1135611366.
Lawrence, P., Schafer, E.A., Rieder, E., 2012. The nuclear protein Sam68 is cleaved
by the FMDV 3C protease redistributing Sam68 to the cytoplasm during FMDV
infection of host cells. Virology 425 (1), 4052.
Lea, S., Abu-Ghazaleh, R., Blakemore, W., et al., 1995. Structural comparison of two
strains of foot-and-mouth disease virus subtype O1 and a laboratory antigenic
variant, G67. Structure 3 (6), 571580.
Lea, S., Hernandez, J., Blakemore, W., et al., 1994. The structure and antigenicity of
a type C foot-and-mouth disease virus. Structure 2 (2), 123139.
Li, Z., Yi, Y., Yin, X., Zhang, Z., Liu, J., 2008. Expression of foot-and-mouth disease
virus capsid proteins in silkworm-baculovirus expression system and its
utilization as a subunit vaccine. PLoS One 3, e2273.
Loefer, F., Frosch, P., 1897. Summarischer Bericht uber die Ergebnisse der
Untersuchungen zur Erforschung der Maul- und Klauenseuche. Zentralblatt
fr Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 22,
257259.
Lopez de Quinto, S., Martinez-Salas, E., 1999. Involvement of the aphthovirus RNA
region located between the two functional AUGs in start codon selection.
Virology 255, 324336.
Lubroth, J., Grubman, M.J., Burrage, T.G., Newman, J.F., Brown, F., 1996. Absence
of protein 2C from claried foot-and-mouth disease virus vaccines provides the
basis for distinguishing convalescent from vaccinated animals. Vaccine 14 (5),
419427.
Luz, N., Beck, E., 1990. A cellular 57 kDa protein binds to two regions of the
internal translation initiation site of foot-and-mouth disease virus. FEBS Letters
269 (2), 311314.
Mahy, B.W., 2004. Overview of foot-and-mouth disease and its impact as a
re-emergent viral infection. In: Domingo, F.S.a.E. (Ed.), Foot-and-Mouth
Disease: Current Perspectives. Cambridge: Horizon Bioscience, pp. 437446
(Chapter 17).
Martn-Acebes, M., Gonzlez-Magaldi, M., Sandvig, K., Sobrino, F., Armas-Portela,
R., 2007. Productive entry of type C foot-and-mouth disease virus into
343
Moraes, M.P., Mayr, G.A., Grubman, M.J., 2001. pAd5-Blue: Direct ligation system
for engineering recombinant adenovirus constructs. BioTechniques 31,
10541056.
Moraes, M.P., Mayr, G.A., Mason, P.W., Grubman, M.J., 2002. Early protection
against homologous challenge after a single dose of replication-defective human
adenovirus type 5 expressing capsid proteins of foot-and-mouth disease virus
(FMDV) strain A24. Vaccine 20 (1112), 16311639.
Nayak, A., Goodfellow, I.G., Belsham, G.J., 2005. Factors required for the
Uridylylation of the foot-and-mouth disease virus 3B1, 3B2, 3B3 peptides by the
RNA-dependent RNA polymerase (3Dpol) in vitro. Journal of Virology 79,
76987706.
Neff, S., Sa-Carvalho, D., Rieder, E., et al., 1998. Foot-and-mouth disease virus
virulent for cattle utilizes the integrin alpha(v)beta3 as its receptor. Journal of
Virology 72 (5), 35873594.
Netherton, C., Moffat, K., Brooks, E., Wileman, T., 2007. A guide to viral inclusions,
membrane rearrangenments, factories, and viroplasm produced during virus
replication. Advances in Virus Research 70, 101182.
Nfon, C.K., Ferman, G.S., Toka, F.N., Gregg, D.A., Golde, W.T., 2008. Interferonalpha production by swine dendritic cells is inhibited during acute infection with
foot-and-mouth disease virus. Viral Immunology 21, 6877.
Nfon, C.K., Toka, F.N., Kenney, M., Pacheco, J.M., Golde, W.T., 2010. Loss of
plasmacytoid dendritic cell function coincides with lymphopenia and
viremia during foot-and-mouth disease virus infection. Viral Immunology 23,
2941.
Ng, K.K., Arnold, J.J., Cameron, C.E., 2008. Structure-function relationships among
RNA-dependent RNA polymerases. Current Topics in Microbiology and
Immunology 320, 137156.
Nishiura, H., Omori, R., 2010. An epidemiological analysis of the foot-and-mouth
disease epidemic in Miyazaki, Japan 2010. Transboundary and Emerging
Diseases 57, 396403.
Nugent, C.I., Johnson, K.L., Sarnow, P., Kirkegaard, K., 1999. Functional coupling
between replication and packaging of poliovirus replicon RNA. Journal of
Virology 73 (1), 427435.
O'Donnell, V., Larocco, M., Baxt, B., 2008. Heparan sulfate-binding foot-and-mouth
disease virus enters cells via caveola-mediated endocytosis. Journal of Virology
82 (18), 90759085.
O'Donnell, V., LaRocco, M., Duque, H., Baxt, B., 2005. Analysis of foot-and-mouth
disease virus internalization events in cultured cells. Journal of Virology 79 (13),
85068518.
O'Donnell, V., Pacheco, J.M., Gregg, D., Baxt, B., 2009. Analysis of foot-and-mouth
disease virus integrin receptor expression in tissues from naive and infected
cattle. Journal of Comparative Pathology 141 (23), 98112.
O'Donnell, V.K., Pacheco, J.M., Henry, T.M., Mason, P.W., 2001. Subcellular
distribution of the foot-and-mouth disease virus 3A protein in cells infected with
viruses encoding wild-type and bovine-attenuated forms of 3A. Virology 287 (1),
151162.
O'Donnell, V., Pacheco, J.M., LaRocco, M., et al., 2011. Foot-and-mouth disease
virus utilizes an autophagic pathway during viral replication. Virology 410 (1),
142150.
van Ooij, M., Polacek, C., Glaudemans, D., et al., 2006. Polyadenylation of genomic
RNA and initiation of antigenomic RNA in a positive-strand RNA virus are
controlled by the same cis-element. Nucleic Acids Research 34, 29532965.
Ostrowski, M., Vermeulen, M., Zabal, O., et al., 2005. Impairment of thymusdependent responses by murine dendritic cells infected with foot-and-mouth
disease virus. Journal of Immunology 175, 39713979.
Pacheco, A., Lopez de Quinto, S., Ramajo, J., Fernandez, N., Martinez-Salas, E.,
2009. A novel role for Gemin5 in mRNA translation. Nucleic Acids Research 37
(2), 582590.
Pacheco, A., Martinez-Salas, E., 2010. Insights into the biology of IRES elements
through riboproteomic approaches. Journal of Biomedicine and Biotechnology
2010, 458927.
Pacheco, J.M., Brum, M.C., Moraes, M.P., Golde, W.T., Grubman, M.J., 2005.
Rapid protection of cattle from direct challenge with foot-and-mouth disease
virus (FMDV) by a single inoculation with an adenovirus-vectored FMDV subunit
vaccine. Virology 337, 205206.
Pacheco, J.M., Henry, T.M., O'Donnell, V.K., Gregory, J.B., Mason, P.W., 2003.
Role of nonstructural proteins 3A and 3B in host range and pathogenicity of
foot-and-mouth disease virus. Journal of Virology 77 (24), 1301713027.
Parida, S., 2009. Vaccination against foot-and-mouth disease virus: Strategies and
effectiveness. Expert Review of Vaccines 8, 347365.
Park, J.H., Lee, K.H., Ko, Y.J., et al., 2012. Diagnosis and control measures of the
2010 outbreak of foot-and-mouth disease a type in the Republic of Korea.
Transboundary and Emerging Diseases 60, 188192.
344
Pathak, H.B., Oh, H.S., Goodfellow, I.G., Arnold, J.J., Cameron, C.E., 2008.
Picornavirus genome replication: Roles of precursor proteins and rate-limiting
steps in oril-dependent VPg uridylylation. Journal of Biological Chemistry 283,
3067730688.
Paul, A.V., van Boom, J.H., Filippov, D., Wimmer, E., 1998. Protein-primed RNA
synthesis by puried poliovirus RNA polymerase. Nature 393 (6682), 280284.
Pega, J., Bucafusco, D., Di, G., et al., 2013. Early adaptive immune response in the
respiratory tract of foot-and-mouth disease virus-infected cattle. Journal of
Virology 87, 24892495.
Pena, L., Moraes, M.P., Koster, M., et al., 2008. Delivery of a foot-and-mouth
disease virus empty capsid subunit antigen with nonstructural protein 2B
improves protection of swine. Vaccine 26, 56895699.
Perez-Martin, E., Weiss, M., Diaz-San Segundo, F., et al., 2012. Bovine type III
interferon signicantly delays and reduces the severity of foot-and-mouth disease
in cattle. Journal of Virology 86 (8), 44774487.
Piccone, M.E., Pacheco, J.M., Pauszek, S.J., et al., 2010. The region between the
two polyprotein initiation codons of foot-and-mouth disease virus is critical for
virulence in cattle. Virology 396 (1), 152159.
Piccone, M.E., Pauszek, S., Pacheco, J., et al., 2009. Molecular characterization of a
foot-and-mouth disease virus containing a 57-nucleotide insertion in the 3
unstranslated region. Archives of Virology 154, 671676.
Piccone, M.E., Rieder, E., Mason, P.W., Grubman, M.J., 1995a. The foot-and-mouth
disease virus leader proteinase gene is not required for viral replication. Journal
of Virology 69 (9), 53765382.
Pierschbacher, M.D., Ruoslahti, E., 1984a. Cell attachment activity of bronectin can
be duplicated by small synthetic fragments of the molecule. Nature 309 (5963),
3033.
Pierschbacher, M.D., Ruoslahti, E., 1984b. Variants of the cell recognition site of
bronectin that retain attachment-promoting activity. Proceedings of the National
Academy of Sciences USA 81 (19), 59855988.
Pilipenko, E.V., Maslova, S.V., Sinyakov, A.N., Agol, V.I., 1992. Towards
identication of cis-acting elements involved in the replication of enterovirus and
rhinovirus RNAs: A proposal for the existence of tRNA-like terminal structures.
Nucleic Acids Research 20 (7), 17391745.
Pilipenko, E.V., Pestova, T.V., Kolupaeva, V.G., et al., 2000. A cell cycle-dependent
protein serves as a template-specic translation initiation factor. Genes and
Development 14 (16), 20282045.
Pilipenko, E.V., Poperechny, K.V., Maslova, S.V., et al., 1996. Cis-element, oriR,
involved in the initiation of () strand poliovirus RNA: A quasi-globular multidomain RNA structure maintained by tertiary (kissing) interactions. EMBO
Journal 15 (19), 54285436.
Pineiro, D., Ramajo, J., Bradrick, S.S., Martinez-Salas, E., 2012. Gemin5 proteolysis
reveals a novel motif to identify L protease targets. Nucleic Acids Research 40
(11), 49424953.
Pluimers, F.H., Akkerman, A.M., van der Wal, P., Dekker, A., Bianchi, A., 2002.
Lessons from the foot and mouth disease outbreak in the Netherlands in 2001.
Revue Scientique et Technique (International Ofce of Epizootics) 21,
711721.
Porta, C., Xu, X., Loureiro, S., et al., 2013. Efcient production of foot-and-mouth
disease virus empty capsids in insect cells following down regulation of 3C
protease activity. Journal of Virological Methods 187, 406412.
Rai, D.K., Schafer, E.A., Singh, K., et al., 2013. Repeated exposure to 5D9, an
inhibitor of 3D polymerase, effectively limits the replication of foot-and-mouth
disease virus in host cells. Antiviral Research 98 (3), 380385.
Ray, D.K., Bhattacharyya, U.K., Chowdhury, B., Dasgupta, P., Bhattacharyya, A.K.,
1989. Studies on a severe outbreak of foot-and-mouth disease in regularly
vaccinated cross-exotic dairy cattle in West Bengal (India). Indian Journal of
Animal Health 28, 5055.
Reid, E., Juleff, N., Gubbins, S., et al., 2011. Bovine plasmacytoid dendritic cells are
the major source of type I interferon in response to foot-and-mouth disease virus
in vitro and in vivo. Journal of Virology 85 (9), 42974308.
Ridgen, R.C., Carrasco, C.P., Summereld, A., McCullough, K.C., 2002. Macrophage
phagocytosis of foot-and-mouth disease virus may create infectious carriers.
Immunology 106, 537548.
Robinson, L., Windsor, M., McLaughlin, K., et al., 2011. Foot-and-mouth disease
virus exhibits an altered tropism in the presence of specic immunoglobulins,
enabling productive infection and killing of dendritic cells. Journal of Virology 85
(5), 22122223.
Rodriguez, L., Grubman, M.J., 2009. Foot-and-mouth disease virus vaccines.
Vaccine 27, 9094.
Rodriguez-Calvo, T., Diaz-San Segundo, F., Sanz-Ramos, M., Sevilla, N., 2011. A
replication analysis of foot-and-mouth disease virus in swine lymphoid tissue
might indicate a putative carrier state in pigs. Veterinary Research 42, 22.
Rodriguez-Pulido, M., Serrano, P., Saiz, M., Martinez-Salas, E., 2007. Foot-andmouth disease virus infection induces proteolytic cleavage of PTB, eIF3a,b, and
PABP RNA-binding proteins. Virology 364, 466474.
Rosas, M.F., Martinez-Salas, E., Sobrino, F., 2003. Stable expression of antisense
RNAs targeted to the 5 non-coding region confers heterotypic inhibition to footand-mouth disease virus infection. Journal of General Virology 84 (Pt 2),
393402.
Rowlands, D.J., Sangar, D.V., Brown, F., 1974. A comparative chemical and
serological study of the full and empty particles of foot-and-mouth disease virus.
Journal of General Virology 26, 227238.
Rozovics, J.M., Semler, B.L., 2010. Genomic replication I and II. In: Ehrenfeld, E.,
Domingo, E., Roos, R.P. (Eds.), The Picornaviruses. Washington, DC: ASM
Press, pp. 107140.
Rozovics, J.M., Virgen-Slane, R., Semler, B.L., 2011. Engineered picornavirus VPgRNA substrates: Analysis of a tyrosyl-RNA phosphodiesterase activity. PLoS One
6 (3), e16559.
Rweyemamu, M.M., Terry, G., Pay, T.W., 1979. Stability and immunogenicity of
empty particles of foot-and-mouth disease virus. Archives of Virology 59 (12),
6979.
Ryan, M.D., King, A.M., Thomas, G.P., 1991. Cleavage of foot-and-mouth disease
virus polyprotein is mediated by residues located within a 19 amino acid
sequence. Journal of General Virology 72 (Pt 11), 27272732.
Sa-Carvalho, D., Rieder, E., Baxt, B., et al., 1997. Tissue culture adaptation of footand-mouth disease virus selects viruses that bind to heparin and are attenuated
in cattle. Journal of Virology 71 (7), 51155123.
Sagedahl, A., Giraudo, A.T., De Mello, P.A., et al., 1987. Biochemical
characterization of an aphthovirus type C3 strain Resende attenuated for cattle by
serial passages in chicken embryos. Virology 157, 366374.
Saiz, M., Gomez, S., Martinez-Salas, E., Sobrino, F., 2001. Deletion or substitution
of the aphthovirus 3 NCR abrogates infectivity and virus replication. Journal of
General Virology 82 (Pt 1), 93101.
Sakamoto, K., Yoshida, K., 2002. Recent outbreaks of foot and mouth disease in
countries of east Asia. Revue Scientique et Technique (International Ofce of
Epizootics) 21, 459463.
Salt, J.S., 1993. The carrier state in foot and mouth disease An immunological
review. British Veterinary Journal 149 (3), 207223.
Salt, J.S., Mulcahy, G., Kitching, R.P., 1996. Isotype-specic antibody responses to
foot-and-mouth disease virus in sera and secretions of carrier and non-carrier
cattle. Epidemiology and Infection 117 (2), 349360.
de los Santos, T., de Avila Botton, S., Weiblen, R., Grubman, M.J., 2006. The leader
proteinase of foot-and-mouth disease virus inhibits the induction of beta
interferon mRNA and blocks the host innate immune response. Journal of
Virology 80 (4), 19061914.
de los Santos, T., Diaz-San Segundo, F., Grubman, M.J., 2007. Degradation of
nuclear factor kappa B during foot-and-mouth disease virus infection. Journal of
Virology 81 (23), 1280312815.
de los Santos, T., Wu, Q., de Avila Botton, S., Grubman, M.J., 2005. Short hairpin
RNA targeted to the highly conserved 2B nonstructural protein coding region
inhibits replication of multiple serotypes of foot-and-mouth disease virus.
Virology 335 (2), 222231.
Sanz-Parra, A., Sobrino, F., Ley, V., 1998. Infection with foot-and-mouth disease
virus results in a rapid reduction of MHC class I surface expression. Journal of
General Virology 79 (Pt 3), 433436.
Scudamore, J.M., Harris, D.M., 2002. Control of foot and mouth disease: Lessons
from the experience of the outbreak in Great Britain in 2001. Revue Scientique
et Technique (International Ofce of Epizootics) 21, 699710.
Sorensen, J.H., Mackay, D.K., Jensen, C.O., Donaldson, A.I., 2000. An integrated
model to predict the atmospheric spread of foot-and-mouth disease virus.
Epidemiology and Infection 124 (3), 577590.
Strebel, K., Beck, E., 1986. A second protease of foot-and-mouth disease virus.
Journal of Virology 58 (3), 893899.
Strohmaier, K., Franze, R., Adam, K.H., 1982. Location and characterization of the
antigenic portion of the FMDV immunizing protein. Journal of General Virology
59 (Pt 2), 295306.
Sumption, K., McLaws, M., Bartels, C., et al., 2012. The progressive control
pathway for FMD (PCP-FMD): A tool for developing sustainable long term
national and regional FMD control. FAO/OIE Global Conference on Foot and
Mouth Disease Control.
Sutmoller, P., Barteling, S.S., Olascoaga, R.C., Sumption, K.J., 2003. Control and
eradication of foot-and-mouth disease. Virus Research 91 (1), 101144.
Sutmoller, P., Casas, O.R., 2002. Unapparent foot and mouth disease infection (subclinical infections and carriers): Implications for control. Revue Scientique et
Technique 21 (3), 519529.
Sutmoller, P., McVicar, J.W., Cottral, G.E., 1968. The epizootiological importance of
foot-and-mouth disease carriers. I. Experimentally produced foot-and-mouth
disease carriers in susceptible and immune cattle. Archiv fr die gesamte
Virusforschung 23, 227235.
Taboga, O., Tami, C., Carrillo, E., et al., 1997. A large-scale evaluation of peptide
vaccines against foot-and-mouth disease: Lack of solid protection in cattle and
isolation of escape mutants. Journal of Virology 71 (4), 26062614.
Tesar, M., Berger, H.G., Marquardt, O., 1989. Serological probes for some foot-andmouth disease virus nonstructural proteins. Virus Genes 3 (1), 2944.
Toka, F.N., Nfon, C., Dawson, H., Golde, W.T., 2009. Natural killer cell dysfunction
during acute infection with foot-and-mouth disease virus. Clinical and Vaccine
Immunology 16, 17381749.
Uddowla, S., Hollister, J., Pacheco, J.M., Rodriguez, L.L., Rieder, E., 2012. A safe
foot-and-mouth disease vaccine platform with two negative markers for
differentiating infected from vaccinated animals. Journal of Virology 86 (21),
1167511685.
Vagnozzi, A., Stein, D.A., Iversen, P.L., Rieder, E., 2007. Inhibition of foot-andmouth disease virus infections in cell cultures with antisense morpholino
oligomers. Journal of Virology 81, 1166911680.
Vakharia, V.N., Devaney, M.A., Moore, D.M., Dunn, J.J., Grubman, M.J., 1987.
Proteolytic processing of foot-and-mouth disease virus polyproteins expressed in
a cell-free system from clone-derived transcripts. Journal of Virology 61 (10),
31993207.
Vivier, E., Raulet, D.H., Moretta, A., et al., 2011. Innate or adaptive immunity? The
example of natural killer cells. Science 331, 4449.
Vosloo, W., Bastos, A.D., Kirkbride, E., et al., 1996. Persistent infection of African
buffalo (Syncerus caffer) with SAT-type foot-and-mouth disease viruses: Rate of
xation of mutations, antigenic change and interspecies transmission. Journal of
General Virology 77 (Pt 7), 14571467.
Wang, D., Fang, L., Bi, J., et al., 2011a. Foot-and-mouth disease virus leader
proteinase inhibits dsRNA-induced RANTES transcription in PK-15 cells. Virus
Genes 42 (3), 388393.
Wang, D., Fang, L., Li, K., et al., 2012. Foot-and-mouth disease virus 3C protease
cleaves NEMO to impair innate immune signaling. Journal of Virology 86 (17),
93119322.
Wang, D., Fang, L., Li, P., et al., 2011b. The leader proteinase of foot-and-mouth
disease virus negatively regulates the type I interferon pathway by acting as a
viral deubiquitinase. Journal of Virology 85 (8), 37583766.
Wilson, V., Taylor, P., Desselberger, U., 1988. Crossover regions in foot-and-mouth
disease virus (FMDV) recombinants correspond to regions of high local
secondary structure. Archives of Virology 102 (12), 131139.
345
Windsor, M.A., Carr, B.V., Bankowski, B., et al., 2011. Cattle remain
immunocompetent during the acute phase of foot-and-mouth disease virus
infection. Veterinary Research 42 (1), 108.
Woodbury, E.L., 1995. A review of the possible mechanisms for the persistence of
foot-and-mouth disease virus. Epidemiology and Infection 114 (1), 113.
Wu, Q., Brum, M.C.S., Caron, L., Koster, M., Grubman, M.J., 2003. Adenovirusmediated type I interferon expression delays and reduces disease signs in cattle
challenged with foot-and-mouth disease virus. Journal of Interferon and Cytokine
Research 23 (7), 359368.
Yang, P.C., Chu, R.M., Chung, W.B., Sung, H.T., 1999. Epidemiological
characteristics and nancial costs of the 1997 foot-and-mouth disease epidemic
in Taiwan. Veterinary Record 145 (25), 731734.
Yoon, H., Yoon, S.S., Wee, S.H., Kim, Y.J., Kim, B., 2012. Clinical manifestations
of foot-and-mouth disease during the 2010/2011 epidemic in the Republic of
Korea. Transboundary and Emerging Diseases 59, 517525.
Zhang, J., Tarbet, E.B., Toro, H., Tang, D.C., 2011. Adenovirus-vectored drugvaccine duo as a potential driver for conferring mass protection against
infectious diseases. Expert Review of Vaccines 10, 15391552.
Zhang, Z., Ahmed, R., Paton, D., Bashiruddin, J.B., 2009. Cytokine mRNA responses
in bovine epithelia during foot-and-mouth disease virus infection. Veterinary
Jounral 179 (1), 8591.
Zhang, Z., Kitching, R.P., 2001. The localization of persistent foot and mouth
disease virus in the epithelial cells of the soft palate and pharynx. Journal of
Comparative Pathology 124 (23), 8994.
Zhang, Z.D., Hutching, G., Kitching, P., Alexandersen, S., 2002. The effects of
gamma interferon on replication of foot-and-mouth disease virus in persistently
infected bovine cells. Archives of Virology 147 (11), 21572167.
Zhao, Q., Pacheco, J.M., Mason, P.W., 2003. Evaluation of genetically engineered
derivatives of a Chinese strain of foot-and-mouth disease virus reveals a novel
cell-binding site which functions in cell culture and in animals. Journal of
Virology 77 (5), 32693280.
Zhu, J., Weiss, M., Grubman, M.J., de los Santos, T., 2010. Differential gene
expression in bovine cells infected with wild type and leaderless foot-and-mouth
disease virus. Virology 404 (1), 3240.
Ziegler, E., Borman, A.M., Kirchweger, R., Skern, T., Kean, K.M., 1995. Foot-andmouth disease virus Lb proteinase can stimulate rhinovirus and enterovirus
IRES-driven translation and cleave several proteins of cellular and viral origin.
Journal of Virology 69 (6), 34653474.
Glossary
Antibiotic resistance A form of drug resistance in which
certain microorganisms could survive after exposure to one
or more antibiotic treatment.
Foodborne illness Any disease resulting from the
consumption of food contaminated by pathogens, viruses,
parasites, or toxins.
Prebiotics Nondigestible food ingredients that stimulate
the growth or activity of bacteria (probiotics) in the
digestive system and eventually benet the host.
Introduction
Antibiotics are antimicrobial compounds that can inhibit and
even destroy bacterial and fungal growth. Some compounds,
such as aminoglycosides and penicillins, are isolated from
living organisms, whereas others, such as oxazolidinones,
quinolones, and sulfonamides, are produced by chemical
synthesis. Accordingly, antibiotics can be classied based on
their origin as natural origin, semisynthetic origin, or synthetic
origin. Most of the common antibiotics used today are semisynthetic modications of a variety of natural compounds.
These antibiotics are used in both human medicine and animal agriculture to reduce incidences of diseases. They are
usually administered by injection or orally via feed and water.
Antibiotics used for growth promotion in livestock and
poultry not only allow the growth of healthier and more
productive farm animals through improved weight gain and
feed conversion efciency, but they are also effective against
animal diseases (Dibner and Richards, 2005). However, lowdose or specic employment of antibiotic as growth promoters
that may involve bacterial antibiotic resistance and the replacement of these antibiotics with some natural products are
under pressure.
Antibiotics widely administered in preharvest farm animals
also help to reduce foodborne pathogens and prevent foodborne illness, which causes high morbidity and mortality rates
worldwide. Currently, broad-spectrum antibiotics are commonly employed as feed additives for the preslaughter inhibition of foodborne pathogens. Owing to difculties in
determining specic agents targeting specic pathogen at the
farm animal level, antibiotics have been shown to lower
foodborne illness, and thus reduce morbidity and mortality, in
humans (Callaway et al., 2003). Other nonantibiotic antimicrobials are also used in foodborne pathogen prevention.
These strategies include vaccination and the use of bacteriocins, bacteriophages, enzymes, probiotics, prebiotics, and
organic acids.
As an essential strategy for controlling animal diseases,
antibiotics have been employed in agricultural farming for
therapeutic purposes. Multiple antibiotics have been approved
346
doi:10.1016/B978-0-444-52512-3.00187-X
Table 1
347
Country
Year
Livestock
Australia
Belgium
Canada
Denmark
2006
2009
2008
2010
Finland
2009
France
2010
Germany
Japan
2005
2004
Kenya
Netherlands
2004
2009
New Zealand
2009
Norway
South Africa
Sweden
Switzerland
2010
2004
2010
2005
USA
UK
2010
2010
Poultry
348
In-feed enzymes
Feed enzymes have been employed extensively in both livestock and poultry feed for more than 15 years, especially in
wheat- or barley-based diets (Choct, 2002). In-feed enzymes
are usually produced by fermentation of fungi and bacteria,
after which these are used to stimulate growth as additives in
animal feeds. Several studies have investigated the effectiveness of in-feed enzymes as a substitute for antibiotic growth
promoters for improving nutrient absorption and digestibility,
gaining body weight, and animal performance. Based on recent studies, it was demonstrated that in-feed enzymes often
have activities in promoting digestion of feed components that
are normally poorly digested or totally undigested in agricultural animals (Hedemann et al., 2009). The mechanism by
which in-feed enzymes promote digestion of feed components
is believed to involve the breakdown of those hard-to-digest
chemical components in the grains and meals such as nonstarch polysaccharides, especially arabinoxylans and beta-glucans, phytates, and proteins (Gerard et al., 2011). Added
routinely to the feed of livestock and poultry, these enzymes
are efcient at maximizing feed conversion efciency, and
more importantly they have no or very few side effects. As a
consequence, numerous researchers are now focusing on improving the quality of existing enzymes, intending to broaden
the range of feed ingredients in which they could be used as
alternative growth promoters.
Probiotics
Similar to competitive exclusion products, probiotics are dened as directly fed mono- or mixed cultures of living
microorganisms that can compete with undesired microbes
and benet the host by improving the properties of the indigenous microbiota (Fuller, 1992). Available probiotics can
be divided into two main categories. One category is colonizing species such as Lactobacillus, Lactococci, and Enterococcus;
the other is free-owing noncolonizing species, which include
both Bacillus and Saccharomyces cerevisiae. These benecial
microbes are able to ameliorate the overall health of animal by
improving the gut microbial balance; however, their exact
mechanism is still under investigation. One major hypothesis
for their actions could involve their inuence on intestinal
metabolic activities, including the improvement of bacteriocins, propionic acid, and vitamin B12 production, and increasing the villous length and nutrient absorption (Christina
et al., 2009). Other possible mechanisms include competitive
exclusion of pathogenic microorganisms and their immunostimulatory activities.
Probiotics are also effective in helping boost weight gain
and feed conversion rates in newborn animals. However,
several questions about the active strains, the maximum dosage, the effective delivery system, and the potential risks remain unanswered and need to be further investigated. One
more potential danger of using live probiotics refers to their
antibiotic resistance. A report from the Scientic Committee
on Animal Nutrition (2001) concerning the safety of probiotic
products found that Lactobacillus plantarum and Pediococcus
acidilactici were tetracycline-resistant. As a consequence, the
use of probiotics could possibly put the whole food chain and
the environment at risk. Moreover, the permanent establishment of probiotics in animal gastrointestinal tracts is difcult.
Several studies have indicated that gut microora are active
and efcient in preventing new organisms from colonizing
and becoming established (Jonsson and Conway, 1992). Finally, the high cost and high dosage of administration required for probiotics for growth promotion might also be a
serious drawback to their widespread application in animal
agriculture.
349
Bioactive phytochemicals
A variety of plant-derived agents are employed worldwide as
feed additives in farm animals. As a substitute for antibiotics,
these plant-derived compounds also exert production-enhancing effects, including the improvement of dairy weight
gain, enhancement of feed conversion efciency, and increasing milk and egg production (Halldor, 2012). As the secondary metabolites of owering plants, essential oils have been
used as nonantibiotic antimicrobials as animal feed additives
for the purpose of both growth stimulation and bacterial inhibition (Hammer and Carson, 2011). Para-thymol, an isomeride of thymol, with higher antibacterial activity and lower
volatility, has been found to be safer and exerts even
better growth-promoting effects than thymol and carvacrol
(Peng et al., 2011). Other bioactive phytochemicals patented
worldwide include isoavone, produced by Fabaceae family,
diaryheptanoid from the bark of the Japanese shrub alder
Alnus pendula, Curcuma aromatica Salisb extracted from ginger,
saponin extracted from yucca, alkaloids from plume poppy,
and lignocellulose obtained from Magnolia, all of which have
been claimed to effectively modulate gut microora, improve
immune function, and promote both absorption and digestion of nutrients by livestock and poultry (Halldor, 2012).
Prebiotics
Prebiotics are nondigestible feed ingredients that are able to
provide selective stimulatory effects on both the growth
and metabolic activity of certain gut microora, including
the probiotics mentioned above. Their effects are based on the
nature of the compound, but essentially they could exert the
same or similar actions as probiotics. Unlike probiotics, which
are foreign microorganisms introduced into the gut competing
with colonic communities which have already become established, the chief advantage of employing prebiotics in improving gut function is that their target bacteria are already
commensal with the large intestine (Macfarlane et al., 2008).
However, prebiotics cannot be effective if the targeted benecial bacteria are not in the gut due to, for example, antibiotic
therapy or intestinal diseases. One potential area of future
research would be examining the combined effect of both
probiotics and prebiotics, known as synbiotics, for the replacement of antibiotic growth promotants (Louise, 2009).
Organic acids
Some evidence has shown that in the presence of organic
acids, mainly short-chain fatty acids such as acetic, butyric, and
propionic acids, there is signicant increased growth of gut
350
Poultry
Antibiotics have been put into widespread use in poultry farms
for disease prevention and treatment since the 1940s. Campylobacteriosis in humans is frequently acquired via the consumption of undercooked poultry meat contaminated with
Campylobacter jejuni, identied and isolated from multiple
farm animals but most commonly in poultry meat products
Cattle
EHEC causes infection and various diseases, especially
hemorrhagic colitis, in humans with a relatively low infectious
dose (Lee and Greig, 2010). EHEC is mainly harbored in the
gastrointestinal tracts of healthy cattle and is shed in their
feces. The major source of EHEC was traced to ruminant manure, but undeniably, EHEC was also identied in some
nonruminant farm animals including swine and fowl due to
the cross-contamination spread by ruminant manure. But,
since bovine manure is the major source of EHEC contamination in the farm environment and animal meat products,
effective preharvest control targeting reduced prevalence and
quantity of fecal EHEC excretion by live cattle is crucial. EHEC
does not typically exhibit the drug resistance to the use of
multiple antibiotics which is frequently found in enteropathogenic E. coli and other foodborne pathogens like
Campylobacter and Salmonella, though the use of ionophores
does not show signicant inuence on the prevalence of EHEC
(Edrington et al., 2003; LeJeune and Kauffman, 2006). However, it has been shown that almost all EHEC isolates are
Table 2
351
Antibiotics
Arsanilic acid
Avilamycin
Avoparcin
Bacitracin
Bambermycins
Chlortetracycline
Lincomycin
Oxytetracycline
Penicillin
Roxarsone
Spiramycin
Avoparcin
Tylosin
Virginiamycin
75120
510
7.515
450
120
10100
24
550
250
2346
520
7.515
10110
425
5
None
None
None
None
None
None
03
None
None
None
None
None
None
Table 3
Antibiotics
Bacitracin zinc
Bambermycins
Chlortetracytcline
Laidlomycin
Lasalocid
Monensin
Oxytetracycline
Tylosin
Virginiamycin
3570
15
350
510
1030
530
75
810
1025
None
None
2
None
None
None
None
None
None
Swine
Antibiotics and other antimicrobial agents have been widely
used as preharvest feed additives in the swine industry since
the early 1950s. In addition to effectively stimulating swine
growth rates and improving reproductive performance, preharvest use of antibiotics is also able to reduce the populations
of foodborne pathogens including Campylobacter, EHEC, Listeria, and Salmonella. Currently, preslaughter use of carbadox,
cephalosporins, lincosamides, macrolides, penicillins, pleuromutilins, polypeptides, quinolones, sulfonamides, and tetracyclines is cleared by the Food and Drug Administration in
swine feed (Morrison, 2001). Among these approved antibiotics, the feeding of chlortetracycline and tylosin decreased
fecal shedding in swine articially infected with EHEC, and the
feeding of spectinomycin in pigs under 4 weeks old and
weighing less than 15 lb effectively controlled the infectious
Bacteriocins
Bacteriocins are proteins or peptides with antimicrobial activities produced by certain bacteria for the purpose of inhibiting the growth of their competitive bacterial strains in the
environment. Such antimicrobial proteins are able to inhibit
the growth of several major foodborne pathogens including
EHEC, Salmonella, and Listeria (Stahl et al., 2004; Patton et al.,
352
Table 4
Antibiotics
Apramycin
Arsanilic acid
Bacitracin methylene disalicyrate
Bacitracin zinc
Bambermycins
Carbadox
Chlortetracycline
Lincomycin
Oxytetracycline
Penicillin
Roxarsone
Tiamulin hydrogen fumerate
Tilmicosin
Tylosin
Virginiamycin
150
4590
1030
2040
24
50
450
40200
22
1050
182
35200
181363
10110
425
Disease control
Feed efciency and growth
Feed efciency and growth
Feed efciency
Growth
Disease control
Disease control
Disease control
Disease control
Feed efciency and growth
Disease control
Disease control
Disease control
Feed efciency, growth, and disease control
Disease control
28
5
None
None
None
42
None
None
5
None
5
27
7
None
None
2007). The application of bacteriocin isolated from Lactobacillus salivarius and Paenibacillus polymyxa in chicken intestinal
tracts has been shown to induce a dramatic reduction in
broiler chicken cecal Campylobacter colonization (Svetoch and
Stern, 2010). Nisin has already been found to be effective in
spoilage bacteria reduction in meat and milk, and encapsulated nisin is able to inhibit the growth of L. monocytogenes (da
Silva Malheiros et al., 2010), although nisin's preharvest application is still under research. However, under the basic
principle of bacteriocin, by protecting bacteriocins from ruminal or gastric degradation, once reaching the lower gut, bacteriocins exert their antimicrobial activities by disrupting the
cell membranes of target foodborne pathogens. Owing to their
nontoxic characteristics on eukaryotic host cells, bacteriocins
are considered safe for consumption of meat and meat
products.
Bacteriophages
Because they are highly specic in recognizing and injecting
disrupting DNA into a host bacterium, bacteriophages can be
active against specic bacterial strains. Specicity allows bacteriophages to be used against targeted foodborne pathogens
in a mixed population without disturbing the composition of
normal gut microora. In 2007, a phage spray produced by
Omnilytics (Salt Lake City, UT), specically against EHEC in
preharvest live cattle, was approved by the FDA. Other studies
have also tested the short-term reduction of Salmonella colonization in poultry and swine (Callaway et al., 2008). Several
researchers have also tested the oral consumption of large
doses of bacteriophages and found it to be harmless to animals. Owing to their rapid replication and high level of specicity, bacteriophages can serve as a potential preharvest
strategy against foodborne pathogens in agricultural animals.
However, the efcacy of bacteriophages against infecting bacteria should be tested in the lab before application. The specicity of bacteriophages is also a disadvantage when a need to
target multiple pathogens or causative agents of disease is not
conrmed (Inal, 2003). In addition, compared to antibiotics,
bacteriophages are more complex organisms that are able
to transfer genes between bacteria and induce pathogenic
mutation. Only by careful selection of strictly lytic bacteriophages and sequencing their hereditary materials can crossgene transfer be prevented (Inal, 2003). In comparison with
antibiotics, the administration of bacteriophages requires
trained personnel, which makes the application of bacteriophages much more difcult for farmers.
Chlorate
Chlorate is the analog of nitrate reductase, both of which can
catalyze the conversion from nitrate to nitrite for the anaerobic
respiration of Salmonella and E. coli. The accumulation of
chlorite, degraded from chlorate, in the cytoplasm is able to
kill bacteria (Stewart, 1988). Some studies have demonstrated
that chlorate administered in drinking water signicantly reduces EHEC populations in both cattle and sheep in the
rumen, intestine, cecum, and feces (Callaway et al., 2003). In
addition, preliminary studies examining the use of chlorate in
broilers and in turkeys have also yielded promising results
(Byrd et al., 2003; Moore et al., 2006). Addition of chlorate to
swine diets reduced experimentally inoculated Salmonella and
EHEC fecal and intestinal populations (Anderson et al., 2001a,
b). Currently, chlorate has been licensed as a product but
needs evaluation in its application.
Vaccination
Vaccination is the method of inhibiting pathogens by inducing
the defense mechanisms of animals' own immune systems.
Some specic vaccination has already shown great efcacy in
reducing the levels of foodborne pathogens in agricultural
farm animals. Vaccines against Salmonella strains have been
developed for use in swine and dairy cattle (House et al.,
2001). More recently, a vaccine designed to inhibit fecal EHEC
in cattle has also been developed (Fox et al., 2009). Based on
these research efforts, the use of vaccination in preslaughter
reduction of foodborne pathogens seems to hold promise.
Vaccines made from any one bacteria serovar cannot confer
cross-protection against another serovar, no matter how much
antigenic similarity there is between them, but more than
2500 serovars of Salmonella are found in animals and humans.
Campylobacter jejuni, Campylobacter hyointestinalis, Campylobacter
353
354
the effective and common antibiotics are being used as therapeutic intervention in poultry diseases (Hofacre, 2006).
Necrotic enteritis is the most common infectious disease in
modern poultry farms and can result in huge nancial losses.
Clostridium perfringens is the major causative bacteria of necrotic
enteritis. However, the occurrence of this disease is always
associcated with the outbreak coccidial infection, which induces
the gut to be more susceptible to C. perfringens (Dahiya et al.,
2006). Tetracycline, streptomycin, neomycin, bacitracin, and
avilamycin in feed are the four most common antibiotics targeting necrotic enteritis (Wages, 2001). Control of C. perfringens
infection together with prevention of coccidiosis could be accomplished by adding antibiotics such as virginiamycin (20 g
ton1), bacitracin (50 g ton1), and lincomycin (2 g ton1) to
feed (Wages, 2001). The ionophore classes of anticoccidial
compounds are also effective in preventing coccidial infections.
In addition, probiotics administration is also used as an effective method to both prevent and treat clinical necrotic enteritis.
Controlling respiratory disease in poultry is important to
ensure maximum economic prots. Respiratory disease in
poultry is induced by several complex factors including viral
presence, stress, and dietary changes, but Mycoplasma gallisepticum infection is responsible for most respiratory diseases
in poultry (Animal Health National Program, 2007). A variety
of antibiotics such as tylosin, tiamulin, tilmicosin, aivlosin,
tetracyclines (mainly doxycycline, chlortetracycline, and oxytetracycline), spiramycin, erythromycin, gentamicin and ketasamycin, neomycin, and colistin are used, both alone and in
various combinations, to control and cure respiratory disease
in poultry (Loehren et al., 2008). But uoroquinolones
(enrooxacin, danooxacin, noroxacin, umequin, etc.) are
used in the withdrawal phase.
Gangrenous dermatitis is caused by contamination of more
than one type of bacteria including Clostridium septicum,
Staphylococcus aureus, and E. coli (Li et al., 2010). Owing to the
involvement of various bacterial pathogens in gangrenous
dermatitis, broader-spectrum antibiotics are needed for the
treatment and control of this disease. Preferred effective antibiotics include erythromycin, penicillin, and tetracycline, especially oxytetracycline (Wages, 2001).
Pasteurella multocida is the causal agent of fowl cholera (Siti
and Robert, 2000). This contagious bacterial disease usually
results in high morbidity and mortality rates. Sulfonamides are
commonly used for early treatment (Wages, 2001). Sulfaquinoxaline sodium, together with sulfamethazine and sulfadimethoxine in feed or water, is commonly used to control fowl
cholera in poultry (Loehren et al., 2008). Tetracycline and
noroxacin administered via feed and water or administered
parenterally are also helpful in controlling fowl cholera. And
combination streptomycin-dihydrostreptomycin injection is
effective in ducks.
Other useful antibiotics include lincomycin, virginiamycin,
spectinomycin, tylosin, and erythromycin, which are mainly
used as gram-positive antimicrobials. In addition, gentamicin
and ceftiofur are the most commonly used in in ovo
injectable antibiotics (Loehren et al., 2008). In the case of
protozoan diseases, which include coccidiosis caused by
Eimeria and histomoniasis caused by Histomonas meleagridis,
coccidiostats and histomonostats in the form of feed additives
are used as effective antimicrobials (Wages, 2001).
Conclusion
Antimicrobial substances, especially antibacterial agents, are
commonly employed worldwide to improve the performance,
health, and production of livestock, dairy cattle, and poultry.
These agents are used to protect against illness, help reduce
signicant agricultural losses, and prevent foodborne infections in humans. For the subtherapeutic use of antimicrobials, preharvest treatment for both promotion of
animal growth and inhibition of colonization and crosscontamination of foodborne pathogens have drawn great
attention because of the urgency of the situation as well as the
effectiveness of antibiotics in human disease treatment.
However, some agents used in animal agriculture belong to
classes also employed in human medicine, such as macrolides,
penicillins, sulphonamides, and tetracyclines. This dual use of
antibiotics and the common concern of multiple antibiotic
resistance in human pathogens and the potential impact of
antibiotic residues in food on public health are controversial
355
and have raised concerns. As a result, efforts to develop alternatives such as plant-derived antimicrobial agents and biopreservatives are underway. Although the thoughtful and
measured therapeutic use of antibiotics or other effective
antimicrobials is essential to livestock producers, regulatory
bodies, and consumers, narrow-spectrum antibiotics remain
the rst choice, and a comprehensive understanding of the use
of narrow-spectrum antibiotics in preharvest-level farm animal
production, along with proper guidance from the veterinary
profession, are vital to solving this complex issue.
References
Alaeldein, M.A., 2013. Use of a competitive exclusion product (Aviguards) to
prevent Clostridium perfringens colonization in broiler chicken under induced
challenge. Pakistan Journal of Zoology 45 (2), 371376.
Amy, R.S., Lisa, Y.L., Shawn, M., Polly, W., 2007. What do we feed to foodproduction animals? A review of animal feed ingredients and their potential
impacts on human health. Environmental Health Perspectives 115 (5),
663670.
Anderson, R.C., Buckley, S.A., Callaway, T.R., et al., 2001a. Effect of sodium
chlorate on Salmonella sv. Typhimurium concentrations in the pig gut. In:
Lindberg, J.E., Ogle, B. (Eds.), Digestive Physiology of Pigs. Wallingford, Oxon,
UK: CABI Publishing, pp. 308310.
Anderson, R.C., Buckley, S.A., Callaway, T.R., et al., 2001b. Effect of sodium
chlorate on Salmonella Typhimurium concentrations in the weaned pig gut.
Journal of Food Protection 64, 255258.
Andersson, D.I., Hughes, D., 2010. Antibiotic resistance and its cost: Is it possible
to reverse resistance? Nature Reviews Microbiology 8 (4), 260271.
Angulo, F.J., 2004. Impacts of antimicrobial growth promoter termination in
Denmark. In: Proceedings of the 53rd Western Poultry Disease Conference,
pp.1619. Sacramento, CA: Western Poultry Disease Conference.
Animal Health National Program, 2007. Development of alternative
approaches to antibiotics for controlling bacterial respiratory pathogens in
poultry. In: Annual Report of U.S. Dept. of Agriculture. Washington, DC: U.S.
Dept. of Agriculture
Apley, M., 2001. Animal husbandry and disease control: Cattle. In: FDA-CVM's
Public Meeting Use of Antimicrobial Drugs in Food Animals and the
Establishment of of Regulatory Thresholds on Antimicrobial Resistance. Silver
Spring, MD: U.S. Food and Drug Administration.
Apley, M.D., Coetzee, J.F., 2006. Antimicrobial drug use in cattle. In: Gigure, S.,
Prescott, J.F., Baggot, J.D., Walker, R.D., Dowling, P.M. (Eds.), Antimicrobial
Therapy in Veterinary Medicine, fourth ed. Oxford: Blackwell, pp. 485506.
Barrett, D.C., 2000. Cost-effective antimicrobial drug selection for the management
and control of respiratory disease in European cattle. Veterinary Record 146 (19),
545550.
Besser, T.E., Goldoft, M., Pritchett, L.C., et al., 2000. Multiresistant Salmonella
Typhimurium DT104 infections of humans and domestic animals in the Pacic
Northwest of the United States. Epidemiology & Infection 124, 193200.
Biswas, D., Wideman, N.E., O'Bryan, C.A., et al., 2012. Pasteurized blueberry
(vaccinium corymbosum) juice inhibits growth of bacterial pathogens in milk but
allows survival of probiotic bacteria. Journal of Food Safety 32 (2), 204209.
Bordin, M., D'Atri, F., Guillemot, L., Citi, S., 2004. Histone deacetylase inhibitors
upregulate the expression of tight junction proteins. Molecular Cancer Research
2, 692701.
Burch, D.G.S., Duran, C.O., Aarestrup, F.M., 2008. Guidelines for antimicrobial use
in swine. In: Guardabassi, L., Williamson, R., Kruse, H. (Eds.), Guide to
Antimicrobial Use in Animals. Oxford: Blackwell, pp. 102125.
Byrd, J.A., Anderson, R.C., Callaway, T.R., et al., 2003. Effect of experimental
chlorate product administration in the drinking water on Salmonella Typhimurium
contamination of broiler. Poultry Science 82, 14031406.
356
Hofacre, C.L., 2006. Antimicrobial drug use in poultry. In: Gigure, S., Prescott, J.F.,
Baggot, J.D., Walker, R.D., Dowling, P.M. (Eds.), Antimicrobial Therapy in
Veterinary Medicine, fourth ed. Oxford: Blackwell, pp. 545553.
House, J.K., Ontiveros, M.M., Blackmer, N.M., et al., 2001. Evaluation of an
autogenous Salmonella bacterin and a modied live Salmonella serotype
Choleraesuis vaccine on a commercial dairy farm. American Journal of Veterinary
Research 62 (12), 18971902.
Huyghebaert, G., Ducatelle, R., Van Immerseel, F., 2011. An update on alternatives
to antimicrobial growth promoters for broilers. Veterinary Jounral 187, 182188.
Inal, J.M., 2003. Phage therapy: A reappraisal of bacteriophages as antibiotics.
Archivum Immunologiae et Therapiae Experimentalis 51 (4), 237244.
Irwin, K., Smith, D.R., Ebako, G.M., et al., 2003. Guidelines for the Prudent of
Antibiotics in Food Animals. Lincoln, NE: University of Nbraska-Lincoln.
Joint Expert Advisory Committee on Antibiotic Resistance (JETACAR) Report, 1999.
The use of antibiotics in food-producing animals: antibiotic-resistant bacteria in
animals and humans. Report of the Joint Expert Technical Advisory Committee
on Antibiotic Resistance (JETACAR), October 1999. Canberra, ACT: Department
of Health.
Jonsson, E., Conway, P., 1992. Probiotics for pigs. In: Fuller, R. (Ed.), Probiotics:
The Scientic Basis. London: Chapman and Hall, pp. 259316.
Jung, H.J., Park, Y., Sung, W.S., et al., 2007. Fungicidal effect of pleurocidin by
membrane-active mechanism and design of enantiomeric analogue for proteolytic
resistance. Biochimica et Biophysica Acta 1768, 14001405.
Kandasamy, S., Green, B.B., Benjamin, A.L., Kerr, D.E., 2011. Between-cow variation
in dermal broblast response to lipopolysaccharide reected in resolution of
inammation during Escherichia coli mastitis. Journal of Dairy Science 94 (12),
59635975.
Lee, M.B., Greig, J.D., 2010. A review of gastrointestinal outbreaks in schools:
Effective infection control interventions. Journal of School Health 80 (12), 588598.
LeJeune, J., Kauffman, M., 2006. Bovine E. coli O157 supershedders: Mathematical
myth or meaningful monsters? In: Proceedings of the 2006 VTEC Conference.
Melbourne, Austalia: Cambridge Scholars Press.
Leleu, S., Herman, L., Heyndrickx, M., et al., 2011. Effects on Salmonella shell
contamination and trans-shell penetration of coating hens' eggs with chitosan.
International Journal of Food Microbiology 145 (1), 4348.
Li, G., Lillehoj, H., Lee, K.W., et al., 2010. An outbreak of gangrenous dermatitis in
commercial broiler chickens. Avian Pathology 39 (4), 247253.
Loehren, U., Ricci, A., Cummings, T.S., 2008. Guidelines for antimicrobial use in
poultry. In: Guardabassi, L., Williamson, R., Kruse, H. (Eds.), Guide to
Antimicrobial Use in Animals. Oxford: Blackwell, pp. 126142.
Louise, M., 2009. The Use of Prebiotics and Probiotics in Pigs. Agricultural
Research Council Livestock Business Division: Animal Production. Available
at: http://www.sapork.biz/the-use-of-prebiotics-and-probiotics-in-pigs-a-a-review/
(accessed 05.05.14).
Macfarlane, S.B., Jacobs, M., Kaaya, E.E., 2008. In the name of global health:
Trends in academic institutions. Journal of Public Health Policy 29 (4),
383401.
Mehdi, T., Majid, T., Sayed, A.T., 2011. Effect of probiotic and prebiotradic as
antibiotic growth promoter substitutions on productive and carcass traits of
broiler chicks. In: 2011 International Conference on Food Engineering and
Biotechnology IPCBEE vol.9. Singapore: IACSIT Press.
Meng, J., Doyle, M.P., Zhao, J., Zhao, S., 2008. Enterohemorrhagic Escherichia coli.
In: Doyle, M.P., Beuchat, L.R. (Eds.), Food Microbiology: Fundamentals and
Frontiers. Washington, DC: ASM Press, pp. 249269.
Moore, R.W., Byrd, J.A., Knape, K.D., et al., 2006. The effect of an experimental
chlorate product on Salmonella recovery of turkeys when administered prior to
feed and water withdrawal. Poultry Science 85, 21012105.
Mora, A., Blanco, J.E., Blanco, M., et al., 2005. Antimicrobial resistance of Shiga
toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains
isolated from humans, cattle, sheep and food in Spain. Research in Microbiology
156, 793806.
Morrison, B., 2001. Animal husbandry and disease control: Swine. In: Public Meeting
Use of Antimicrobial Drugs in Food Animals and the Establishment of
Regulatory Thresholds on Antimicrobial Resistance. Silver Spring, MD: FDA-CVM.
Nachamkin, I., 2008. Campylobacter jejuni. In: Doyle, M.P., Beuchat, L.R. (Eds.),
Food Microbiology: Fundamentals and Frontiers. Washington, DC: ASM Press,
pp. 237248.
Page, S.W., Gautier, P., 2012. Use of antimicrobial agents in livestock. Revue
Scientique et Technique (International Ofce of Epizootics) 31 (1), 145188.
Pattison, M., 2008. Poultry Diseases, sixth ed. Edinburgh: Elsevier.
Patton, B.S., Dickson, J.S., Lonergan, S.M., Cutler, S.A., Stahl, C.H., 2007.
Inhibitory activity of Colicin E1 against Listeria monocytogenes. Journal of Food
Protection 70 (5), 12561262.
Peng, L., He, Z., Chen, W., Holzman, I.R., Lin, J., 2007. Effects of butyrate on
intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier.
Pediatric Research 61, 3741.
Peng, X., Zhou, G., Jiang, Z., 2011. Application of Para-Thymol, Salts Ramication
Thereof or Esters Ramication Thereof in Animal Feed Additive. CN102132764A.
Peter, H., John, H., 2004. Antibiotic Growth-Promoters in Food Animals. USA: Food
and Agriculture Organization.
Radostits, O.M., Gay, C., Hinchcliff, K., Constable, P., 2007. Veterinary Medicine: A
Textbook of the Diseases of Cattle, Horses, Sheep, Pigs, and Goats, tenth ed.
Edinburgh: Elsevier.
Rerat, M., Albini, S., Jaquier, V., Hussy, D., 2012. Bovine respiratory disease:
Efcacy of different prophylactic treatments in veal calves and antimicrobial
resistance of isolated Pasteurellaceae. Preventive Veterinary Medicine 103 (4),
265273.
Saif, Y.M., Fadly, A.M., Glisson, J.R., et al., 2008.Diseases of Poultry, twelth ed.
Ames, Iowa: Wiley-Blackwell.
Schauber, J., Svanholm, C., Termn, S., et al., 2003. Expression of the cathelicidin
LL-37 is modulated by short-chain fatty acids in colonocytes: Relevance of
signaling pathways. Gut 52, 735741.
da Silva Malheiros, P., Daroit, D.J., Brandelli, A., 2010. Food applications of
liposome-encapsulated antimicrobial peptides. Trends in Food Science &
Technology 21, 284292.
Singh, B.R., 2009. Salmonella vaccines for animals and birds and their future
perspective. Open Vaccine Journal 2, 100112.
Siti, M., Robert, H., 2000. The immunogenicity and pathogenicity of Pasteurella
multocida isolated from poultry in Indonesia. Veterinary Microbiology 72 (1),
2736.
Stahl, C.H., Callaway, T.R., Lincoln, L.M., Lonergan, S.M., Genovese, K.J., 2004.
Evaluation of colicins for inhibitory activity against Escherichia coli strains
responsible for post-weaning diarrhea and edema disease in swine. Antimicrobial
Agents and Chemotherapy 48 (8), 31193121.
Stewart, V.J., 1988. Nitrate respiration in relation to facultative metabolism in
enterobacteria. Microbiological Reviews 52, 190232.
Svetoch, E.A., Stern, N.J., 2010. Bacteriocins to control Campylobacter spp. in
poultry A review. Poultry Science 89 (8), 17631768.
Swaminathan, B., Cabanes, D., Zhang, W., Cossart, P., 2008. Listeria
monocytogenes. In: Doyle, M.P., Beuchat, L.R. (Eds.), Food Microbiology:
Fundamentals and Frontiers. Washington, DC: ASM Press, pp. 457491.
357
Teshome, H.R., Richard, K.K., Charlies, S.W., Akwasi, A.A., 2007. Antibiotic Use in
Animal Production: Environmental Concerns. Lincoln, NE: University of
NebraskaLincoln Extension, RP196.
Turgis, M., Han, J., Caillet, S., Lacroix, M., 2009. Antimicrobial activity of mustard
essential oil against Escherichia coli O157:H7 and Salmonella typhi. Food
Control 20, 10731079.
Vugia, D., Cronquist, A., Hadler, J., et al., 2007. Preliminary FoodNet data on the
incidence of infection with pathogens transmitted commonly through food 10
states. Morbidity and Mortality Weekly Report 56, 336339.
Wages, D., 2001. Animal husbandry and disease control: Poultry. In: Public Meeting
Use of Antimicrobial Drugs in Food Animals and the Establishment of
Regulatory Thresholds on Antimicrobial Resistance. Silver Spring, MD:
FDA-CVM.
Wagner, S., Erskine, R., 2006. Antimicrobial drug use in bovine mastitis. In:
Gigure, S., Prescott, J.F., Baggot, J.D., Walker, R.D., Dowling, P.M. (Eds.),
Antimicrobial Therapy in Veterinary Medicine, fourth ed. Oxford: Blackwell,
pp. 507517.
Wang, Y., Xu, Z., Bach, S.J., McAllister, T.A., 2009. Sensitivity of Escherichia coli to
seaweed (ascophyllum nodosum) phlorotannins and terrestrial tannins. Asian
Australasian Journal of Animal Science 22 (2), 238245.
Wells, J.E., Berry, E.D., Varel, V.H., 2005. Effects of common forage phenolic acids
on Escherichia coli O157:H7 viability in bovine feces. Applied and Environmental
Microbiology 71, 79747979.
Woerner, D.R., Ransom, J.R., Sofos, J.N., et al., 2006. Determining the prevalence
of Escherichia coli O157 in cattle and beef from the feedlot to the cooler. Journal
of Food Protection 69, 28242827.
World Health Organization, 2000. WHO Global principles for the containment of
antimicrobial resistance in animals intended for food. In: Document WHO/CDS/
CSR/ APH/2000.4, pp. 123. Geneva, Switzerland: WHO.
World Health Organization, 2004. Proceedings of the Joint FAO/OIE/WHO expert
workshop on non-human antimicrobial usage and antimicrobial resistance:
Scientic assessment. In: Document WHO/CDS/DIP/ZFK/04.20, pp 171.
Geneva, Switzerland: WHO.
Zimmerman, J., Karriker, L., Ramirez, A., Schwartz, K., Stevenson, G., 2012.
Diseases of Swine, tenth ed. Ames, IA: Wiley-Blackwell.
Glossary
Adducts A chemical compound that forms from the
addition of two or more substances. The product of an
addition reaction.
Bioavailability The degree to which a drug or other
substance becomes available to the target tissue after
administration.
Carcinogenicity The ability or tendency to produce
cancer.
Fatty degeneration The accumulation of fat globules
within the cells of an organ, such as the liver or heart,
358
mycotoxicoses are rare in animal production, and chronic exposure to low levels of mycotoxins is responsible for reduced
productivity and increased susceptibility to infectious diseases
(Oswald et al., 2005).
Toxigenic Fungi
The name fungi is given to a group of living organisms including microfungi (molds and yeasts) and macrofungi
(mushrooms). Filamentous microfungi (molds) are the ones
that produce mycotoxins. Yeasts are not known to produce
mycotoxins, although they are of considerable interest in the
food industry. Unlike plants, fungi do not contain chlorophyll,
do not accumulate starch, and do not have cellulose in their
cell walls. However, they resemble animal cells for being able
to store glycogen, and contain chitin, a polymer that is a
glucose derivative. Thus, all fungi live a heterotrophic existence
in nature, either as parasites or saprobes, dependent on living
or dead organic matter for their nutrients.
There are a number of essential phases in the life of a
fungus: spore germination, mycelium vegetative growth,
spore-bearing development, spores production, liberation, and
dispersal. The reproductive structures of fungi, called spores
(propagules), are able to reproduce and generate new cells in
favorable environmental conditions. According to their origin,
spores can be sexual or asexual. Fungi are classied according
to their morphology and chemistry and, more recently, to their
molecular biology. One of the most current core features show
four groups in the Kingdom fungi: Chytridiomycota, Zygomycota, Basidiomycota, and Ascomycota. Micotoxigenic species are mostly found in the Ascomycota Division; however,
mushrooms are found within the Basidiomycota Division
(macrofungi), producers of mycetisms.
The main mycotoxin-producing fungi species belong to the
genera Aspergillus, Penicillium, Fusarium, Alternaria, Claviceps,
Myrothecium, Stachybotrys, Phoma, Trichotecium, Cephalosporium,
Trichoderma, Cladosporium, and Pithomyces. However, the
doi:10.1016/B978-0-444-52512-3.00200-X
OCH3
Aflatoxin B1
OCH3
OCH3
Aflatoxin G2
Aflatoxin G1
Aflatoxin B2
OCH3
359
COOH
HOOC
COOH
O
C
H NH C
C
H2
OH
OH
CH3
CH3
CI
CH3
O
OH
NHR3
CH3
CH3
H3C
OH
OH
O
HO
O
HOOC
COOH
Ochratoxin A
Zearalenone
Fumonisin B1
OH
O
H3C
CH3
OH
CH3
H3C
OH
OH
O
O O
O
O
H3C
Deoxynivalenol
H3C
O
CH3
CH3
T-2 toxin
Table 1
Main toxigenic fungi, mycotoxins, and respective biological effects in susceptible species
Fungi species
Mycotoxin
Biological activity
Aatoxins
All species
DON (Vomitoxin)
Swine
Toxin T-2
Fusarium verticillioides
Fumonisins
Ocratoxin A
Nefrotoxicity
Zearalenone
Estrogenic
360
Penicillium
Aspergillus
Conidia
Phialides
Conidia
Vesicle
Phialides
Conidiophore
Metulae
Branch
Conidiophore
Columnar
Radiate
Fusarium
Microconidia
Phialide
Microconidia
Microconidia in chain
Foot cell
Macroconidia
Figure 2 Microscopic structures fungi of genera Aspergillus, Penicillium, and Fusarium.
Aatoxins
Aatoxins are produced by fungi in the genus Aspergillus,
mainly species A. avus and A. parasiticus. These toxins were
discovered in 1960, after an outbreak in turkeys in England
(Turkey X disease). In this outbreak, thousands of birds died
after the intake of Brazilian peanut meal. Nowadays, 20
similar compounds are called aatoxins, although the most
important types are aatoxins B1, B2, G1, and G2. Aatoxin B1
(AFB1) is the most frequent type naturally found in cereals,
and the one with the greatest toxigenic power, followed by G1,
B2, and G2. Aatoxin M1 (AFM1), a detoxication product
present in milk as a result of AFB1 biotransformation, is also as
toxic as AFB1.
Water
Storage time
Temperature
Microbial interaction
Substrate
Mechanical damage
Fungal genetics
Insect damage
pH
Fungal loads
361
Toxin production
Figure 3 Factors affecting fungal growth and production of mycotoxins.
Table 2
Temperature and minimal water activity (aw) on fungal growth and mycotoxin production by mean toxigenic fungi
Fungi
Temperature (1C)
Minimum Aw for
Toxin
Range
Optimum
Growth
Toxin production
Aspergillus avus
Aspergillus parasiticus
Aspergillus ochraceus
Penicillium verrucosum
Penicillium expansum
1045
1242
1035
031
2530
33
32
25
20
25
0.780.80
0.780.82
0760.81
0.81
0.830.85
0.830.87
0.87
0.830.87
0.830.90
0.99
Fusarium verticillioides
237
1530
0.87
0.90
F. graminearum
535
2426
0.90
0.99a
F. poae
239
2228
0.89
0.98a
Aatoxins type B
Aatoxins types B, G
Ochratoxin A
Ochratoxin A
Patulin
Fumonisins
Zearalenone
Moniliformin
Zearalenone
DON, DAS
Moniliformin
T-2, DAS Nivalenol
Aatoxins are characterized by their high toxicity. All domestic and laboratory species are sensitive to the acute toxic,
mutagenic, or carcinogenic effects of these compounds, whose
target organ is the liver. Aatoxins are also a great public
health concern, as they are involved in the etiology of liver
cancer in humans following the ingestion of contaminated
foodstuffs.
The genus Aspergillus and their toxins are distributed
worldwide in foodstuffs and animal feed, but may predominantly be found in tropical and subtropical climates.
Plants get contaminated by means of contact with fungal
spores in the environment, mainly in the soil, during harvesting and drying. The use of inadequate agricultural practices
362
Ochtatoxin A
OT belongs to a large family of mycotoxins that encompasses
more than 20 different metabolites among which ochratoxin A
(OTA) is the most naturally occurring and the most toxic one.
OTs are produced by Aspergillus species, mainly by A. ochraceus
and A. westerdijkiae, which are usually found on coffee, cocoa,
spices, and dried fruits in tropical regions of the globe. Many
Penicillium species also produce OTs, such as Penicillium verrucosum, which develops on cereals during storage in temperate regions of the world, and P. nordicum, which is found on
cheese and fermented meat. One of the main features of OTs is
that they are not degraded during most food-processing steps,
such as fermentation and cooking, and they are thus frequently encountered in food and feed. Cereals, wine, beer, and
pork meat are, in this order of importance, the main sources of
human exposure to OTs. In addition, another important feature of OTs is that they readily bind to proteins and therefore
have also been detected in milk.
OTs are composed of a pentaketide dihydroisocoumarin
moiety linked to the amino acid phenylalanine by an amide
bond at C7. There is a chlorine atom on one of the hydroisocoumarin rings that strongly contributes to toxicity.
Ochratoxin B, which is the dechlorinated form of OTA, is at
least 10 times less toxic than OTA.
Fumonisins
Fumonisins constitute a large family of mycotoxins mainly
produced by F. verticillioides, Fusarium proliferatum and other
Fusarium species. These fungi species are important pathogens
of corn responsible for Fusarium kernel rot or pink ear rot.
Fumonisins have also been isolated from cultures of Alternaria
alternata and Aspergillus niger and mainly contaminate grapes.
Contamination can occur at different stages, such as crop
growth, harvesting, or storage, depending on temperature and
humidity. However, development of Fusarium species mainly
occurs before harvest or in the early periods of storage, when
humidity levels are still high (aw40.9). Human exposure to
fumonisins is of greater importance in countries of South
America, Asia, and Africa due to weather and storage conditions, and to higher consumption of maize-based products,
as well.
The fumonisin family encompasses 28 structurally related
metabolites that can be classied in four series: A, B, C, and P.
All of them share a long carbon chain backbone with an
amine, but have different hydroxyl, methyl, and tricarboxylic
acid side chains (Figure 4). The A series has an acetylated
terminal amine group in C2 position, whereas B and C series
have free amino groups, and P series have a 3-hydroxypiridinium moiety at this position. C series differ from the
rest in that their acyl chain is condensed with glycine instead
of an alanine residue, and these compounds have a C19
backbone chain instead of C20. One particular feature of
COOH
HOOC
O
R2
OH
R4
H3C
CH3
CH3
O
R1
NHR3
HOOC
COOH
A1
A2
B1
B2
B3
B4
C1
C3
C4
R1
R2
R3
R4
OH
H
OH
H
OH
H
OH
OH
H
OH
OH
OH
OH
H
H
OH
H
H
CH2CO
CH2CO
CH3
CH3
CH3
CH3
CH3
CH3
H
H
H
H
H
H
H
H
H
H
Zearalenone
These are a group of mycotoxins produced by several Fusarium
species, such as Fusarium graminearum, Fusarium culmorum,
Fusarium crookwellense, Fusarium equiseti, Fusarium cerealis, and
Fusarium semitectum. In fact, they are produced by most of the
toxigenic Fusarium species and therefore they are usually
detected in combination with other fusariotoxines, such as
trichothecenes and fumonisins. As they are produced by
Fusarium species, zearalenones are mostly encountered in
temperate and warm countries on cereal crops, especially on
corn, as well as on wheat, oats, and soybean. Production of
these mycotoxins mainly takes place in the eld, but may also
occur during improper cereal storage. Human exposure to
zearalenones is essentially caused by consumption of contaminated raw maize and, to a lesser extent, of corn- and
wheat-derived products, and beer. The main concern related to
exposure to zearalenones is due to the fact that they are one of
the most potent families of nonsteroidal naturally occurring
estrogens. Zearalenones have a resorcinol moiety fused to a
14-member macrocyclic lactone. There are six major members
of this family: zearalenone, -zearalenol, -zearalenol, -zearalanol, -zearalanol, and zearalanone (Figure 5).
HO
363
Me
O
O
HO
O
Zearalenone
HO
Me
HO
Me
HO
HO
OH
OH
-Zearalenol
-zearalenol
Fusarium species
HO
HO
Me
Me
O
O
HO
HO
OH
-zearalanol
(taleranol)
OH
-Zearalanol
(zeranol)
HO
Me
O
O
HO
O
Zearalanone
Trichothecenes
Trichothecenes represent a large family of over 150 secondary
metabolites produced worldwide by fungi of different and
taxonomically unrelated genera. Fusarium species are the most
commonly occurring of trichothecene-producing fungi. These
species are important plant pathogens that particularly contaminate cereals such as wheat, barley, oats, and maize. They
are also responsible for Fusarium Head Blight disease, which
causes important crop losses worldwide. All trichothecenes are
sesquiterpenes, which share a common structural backbone
made of a tricyclic nucleus, called trichothecene and, usually, a
double bond at C-9,10, and an epoxide at C-12,13 (Figure 6).
The latter is considered to be very important for toxicity. Based
on differences in the position and number of hydroxylations,
and the number and complexity of esterications as well, trichothecenes can be classied in four groups: type A, B, C, and
D. Types A and B are the most commonly occurring, and they
are generally produced by Fusarium species, with Fusarium
sporotrichoides and Fusarium poae producing type A trichothecenes, whereas F. graminearum and F. culmorum produce type B
trichothecenes.
Type A trichothecenes lack a ketide group at C-8 position.
The most representative mycotoxins of Type A trichothecene
group are T-2 toxin, its hydrolyzed derivate, HT-2, and diacetoxyscirpenol. Type B trichothecenes have a ketide group at
C-8 position. Deoxynivalenol (DON), nivalenol (NIV) and
their acetylated derivatives (3-acetyldeoxynivalenol, 15-acetyldeoxynivalenol, and fusarenone X, respectively) are the most
commonly occurring and the best-characterized mycotoxins of
this group.
364
H3C
Group A trichothecenes
10
11
R1
R1
R2
R3
R4
R5
T-2 toxin
OH
OAc
OAc
Isovaleroxy
HT-2 toxin
OH
OH
OAc
Diacetoxyscirpenol
OH
OAc
OAc
Isovaleroxy
H
Monoacetoxyscirpenol
OH
OH
OAc
Trichodermol
(Roridin C)
OH
13
12
R5
R2
CH3
R4
CH2
R3
10
H3C
11
R1
Group B trichothecenes
13
R1
R2
Nivalenol
OH
Monoacetylnivalenol
(fusarenon-X)
OH
Diacetylnivalenol
Deoxynivalenol
(vomitoxin)
12
7
R4
CH3
R2
CH2
R3
R4
OH
OH
OH
OAc
OH
OH
OH
OAc
OAc
OH
OH
OH
OH
R3
Figure 6 Chemical structures of trichothecenes types A and B.
F. graminearum, in tropical to temperate regions; F. poae, in coldtemperate climate, and Fusarium sporotrichioides in cold climates.
Table 3 shows the results of some studies on aatoxin,
fumonisin, and ochratoxin levels in feedstuffs and animal feed
in countries worldwide. These results indicate that a large
percentage of samples show mycotoxin concentrations that
may potentially affect animal productivity. Besides, mycotoxins residues may accumulate in animal tissues or be shed in
milk or eggs of animals that ingested feed containing mycotoxins. Foods of animal origin contaminated with residues are
additional sources of exposure to humans who ingest these
products.
Corn is the main cereal used in animal feed that is susceptible to contamination by toxigenic fungi, although other
products may also show fungi and mycotoxins, such as sorghum, cotton meal, and soybean meal, as well as prepared
feed. It is important to emphasize that the production of
Table 3
North America
South America
Central Europe
Southern Europe
South Asia
Oceania
Region
North Asia
365
Type of mycotoxin
AFLA
ZEN
DON
FUM
OTA
AFLA
ZEN
DON
FUM
OTA
AFLA
ZEN
DON
FUM
OTA
AFLA
ZEN
DON
FUM
OTA
AFLA
ZEN
DON
FUM
OTA
AFLA
ZEN
DON
FUM
OTA
AFLA
ZEN
DON
FUM
OTA
Soybean meal
Wheat/bran
Finished feed
17
74
857
533
1
2
75
37
2.966
16
1
47
1.028
1.308
ND
3
61
468
2.035
4
13
292
1.062
2.111
ND
197
25
60
626
8
1
173
50
1.796
ND
ND
8
179
NA
1
ND
44
61
12
ND
ND
2
98
NA
7
ND
NA
101
291
ND
ND
22
56
18
1
2
NA
58
NA
10
1
16
50
NA
1
1
34
782
NA
ND
ND
68
501
70
13
ND
10
848
89
16
1
NA
452
116
ND
ND
31
799
41
ND
ND
212
1.463
9
2
ND
430
2.407
32
ND
7
157
1.125
1.111
NA
2
115
33
1.569
3
ND
56
533
131
2
3
13
158
1.505
1
5
213
741
1.026
1
91
25
34
310
21
ND
74
100
179
2
Abbreviations: AFLA, Aatoxins (a sum of aatoxin B1, aatoxin B2, aatoxin G1, and aatoxin G2 content); DON, deoxynivalenol; FUM, fumonisins (a sum of fumonisin B1 and
fumonisin B2); ND, not detect; NA, not available; OTA, ochratoxin A; and ZEN, Zearalenone.
Source: Reproduced from Rodrigues, I., Handi, J., Binder, E.M., 2011. Mycotoxin occurrence in commodities, feeds and feed ingredients sourced in the Middle East and Africa. Food
Additives and Contaminants B 4, 168179 and Rodrigues, I., Naehrer, K., 2012. A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feed. Toxins 4,
663675.
366
Table 4
Country
Mycotoxin
Austria
Deoxynivalenol (DON)
500
1000
50
50
20
5000
100
1000
25
1000
2000
20
50
10
20
50
20
20
500
80
100
500
5
300
10
20
10
20
20
50
5
10
1 000 000
8 000
100
500
250
60 000
5000
20 000
50 000
20
300
100
1 000
20
10
1 000
1 000
200
0
1.5
20
50
100
200
300
200
100
20
5 000
(Continued )
Brazil
Canada
Chile
China
Cuba
Egypt
Japan
Mexico
Sweden
United States
Zearalenone
Total AFa
Total AFa
DON
Toxin T-2
DON
Toxin T-2
Diacetoxyscirpenol
AFB1
Total AFa
AFB1
AFB1
Ochratoxin A
Fumonisins
Toxin T-2
Zearalenone
Vomitoxin
Total AFa
DON
AFB1
Total AFa
AFB1
Rye Ergot
DON
Zearalenone
Ochratoxin A
Fumonisins
AFB1
Ochratoxin A
Toxin T-2
Diacetoxyscirpenol
AFB1
AFB1
Zearalenone
DON
AFB1
AFB1
Ochratoxin A
Total AFa
DON
Table 4
367
Continued
Country
Mycotoxin
O
O
OCH3
Aflatoxin B1
Epoxidation
Protein
O
O
OCH3
Aflatoxin-8,9-epoxide
DNA
Acute toxicity
O
O
HO
Mutagenicity
carcinogenicity
O
N
HN
H2N
OCH3
Aflatoxin B1-N7-guanine
including cattle, lambs, and pigs. In humans, the most important effect of aatoxins is the hepatocellular carcinoma.
This disease represents more than 80% of primary malignant
tumors of the liver, and it is the 7th to 9th most common type
of cancer affecting men and women worldwide, respectively.
The particular sensitivity of birds to aatoxins is related to
the quick absorption by their gastrointestinal system. After
being absorbed, AFB1 immediately binds to albumin and
spreads to the tissues, mainly the liver, where it is biotransformed by the liver microsomal system. Biotransformed
derivatives may bind to intracellular constituents, such as DNA
and RNA, and alter protein synthesis functions. In terms of
commercial poultry, ducks are the most susceptible species,
followed by turkeys, geese, pheasants, and chickens. Dose-response may be different in individuals of the same species, and
may vary according to breed, sex, age, and feed composition,
among other factors. In many species, males are more susceptible than females, and in general, young animals are more
susceptible than adult ones.
Toxic effects of aatoxins depend on the dose and period of
exposure and these factors will determine the occurrence of
acute or chronic intoxications. Acute toxic syndrome is related
to the ingestion of feedstuffs with high concentrations of aflatoxins, and the following effects may be observed shortly
after ingestion: quick deterioration of general condition, loss
of appetite, acute hepatitis (Figure 10), jaundice, hemorrhage,
and death. The most evident clinical sign of chronic aatoxicosis is a decrease in the growth rate of young animals due to
prolonged, continuous, or intermittent ingestion of feed contaminated with low levels of aatoxins. Although this is the
main form of intoxication in natural conditions, diagnosis is
difcult and economic losses may be considerable. Aatoxicosis in monogastric animals like broilers and pigs is a highly
relevant problem because of the economic impact related to
mortality, low feed conversion, increased production costs,
and negative effects on public health related to human consumption of aatoxin residues in the viscera of exposed
animals.
AFB1 negatively affects chicken (Gallus domesticus) growth,
and the effect is more severe during the development of young
animals. Serum proteins, succinate dehydrogenase, and glutamate dehydrogenase are sensitive early indicators of this
more severe intoxication. Decrease in serum albumin may be
used as an early and suitable indicator of the deleterious effects
of this mycotoxin in developing chickens. Broilers fed for 35
days with diets containing different levels of AFB1, had reduced weight gain and histological changes in the liver of birds
that received more than 500 mg kg1 aatoxin per day. Turkeys
submitted to the same treatment showed low weight gain and
368
O
O
OH
OCH3
Aflatoxicol
O
OCH3
Aflatoxin B1
O
O
OH
OH
O
Aflatoxin M1
OCH3
OH
O
Aflatoxin P1
OCH3
Aflatoxin Q1
(a)
(b)
1
(a)
369
(b)
Figure 11 Photomicrographs of quail's livers showing (a) normal architecture of parenchyma and (b) intense vacuolar degeneration of hepatic
cells and trabecular disorder, after dietary exposure to 100 mg kg 1 of AFB1. Haematoxylin and eosin, bar=60 mm.
production. Toxic effects of aatoxin in laying hens also include a dose-dependent decrease in egg production and egg
quality with increased susceptibility to salmonellosis, candidiasis, and coccidiosis. AFB1 can have either direct or indirect
effects, or both, on the functionality of the gastrointestinal
tract of laying hens fed diets containing 0.6, 1.2, or 2.5 mg
kg1 AFB1 for 2 weeks (Applegate et al., 2009).
Aatoxins are also able to affect the immune system.
Immunosuppressing effects demonstrated in domestic birds
and other laboratory animals involve aplasia of thymus and
bursa of Fabricius, reduction in the number and activity of T
cells, decrease in antibody response, suppression of phagocytic
activity, and reduction in humoral components, such as complement (C4), interferon, and immunoglobulins IgG and IgA.
All these changes associated with the exposure of animals to
feed contaminated with aatoxins contribute to the occurrence
of concomitant infections caused by viral and bacterial agents.
Concentrations of approximately 300 mg kg1 AFB1 in the
feed of monogastric animals may lead to immunosuppression
without any apparent clinical effects. Also, the ingestion of the
toxin may be responsible for morbidity or mortality in the
ock due to secondary infections. Signs observed in the animals often included signicant decrease in T cells, albumins,
and globulins.
Aatoxins poisoning in turkeys cause inappetence, reduced
spontaneous activity, unsteady gait, recumbence, anemia, and
death. In the postmortem examination, body condition was
adequate most of the times, but generalized congestion and
edema were observed. Liver and kidneys were congested, enlarged, and rm. Aatoxins in doses equal or greater than
200 mg kg1 affected turkey performance during a period of 1
42 days. The effect of those toxins on body weight, feed consumption, relative weight of gizzard and liver, mortality, and
total protein and cholesterol levels in serum was dependent on
the dose. Turkey poults were very sensitive to aatoxin poisoning, and inadequate mycotoxicological management may
cause important economic losses in turkey production.
Chronic exposure of Japanese quails to diets containing
AFB1 adversely affected their performance, especially feed intake, egg weight, and percent eggshell. Intense vacuolar
370
Ochratoxin A
Although OT were rst isolated from the species A. ochraceus
(previously known as Aspergillus alutaceus), these toxins may be
produced by several species in the genera Aspergillus and
Penicillium. The ochratoxin group has 7 components, but only
OTA has been found worldwide as a natural contaminant of
grains. The kidneys are the target organs of OTA, which
interferes in the synthesis of macromolecules in cells of the
renal parenchyma, including DNA, RNA, and proteins. Besides, it affects renal carbohydrate metabolism, damaging the
epithelium of the proximal tubules (Figure 12) and causing
osmotic diuresis by means of decreased absorption of electrolytes and increased excretion of water.
OTA causes a series of adverse effects in most domestic
animals. In pigs, it is the causative agent of mycotoxic porcine
nephropathy. Similarly, in humans, it is recognized as the
etiological agent of the Balkan endemic nephropathy. In
poultry, OTA is considered to be the most potent mycotoxin,
showing high lethality rates. LD50 for broilers is approximately
2.1 mg kg1 of body weight, whereas LD50 for AFB1 is 6.8 mg
kg1. Ochratoxicosis in swine is observed as decreased weight
gain, as well as polydipsia, polyuria, and renal lesions. Doses
of 200 mg kg1 of OTA in the feed were enough for the animals
to present nephropathy, leading to negative impact in feed
conversion and weight gain. Mortality may reach 90% in
affected lots.
Natural occurrence of outbreaks in turkey breeding facilities due to the presence of OTA in animal feed showed levels
ranging from 0.2 to 16.0 mg kg1, with a mortality rate of
59%, and decrease in feed consumption of 20%. Outbreaks
involving laying hens were characterized by decreased egg
production, low quality of eggshell, and nephropathy. In
broilers, these authors observed low growth rate and feed efciency, little pigmentation of the carcasses, and nephropathy.
In experimental trials, broilers given more than 2.0 mg kg1
OTA in their feed showed decreased weight gain, relative
increase in kidney and liver weight, decreased serum levels of
total proteins, albumins, globulins, and cholesterol, and
increased creatinine and uric acid concentrations.
In broilers fed diets containing 2.0 mg kg1 OTA, a signicant reduction in the breaking strength of large intestines was
observed, along with increased relative weight of the organ. This
nding is important when considering the possible rupture of
intestines during poultry processing, which would lead to fecal
contamination of the carcass. Male broilers fed diets containing
400 and 800 mg kg1 OTA showed signicant decrease in body
and thymus weight, feed consumption, feed conversion ratio,
and thyroxin concentration. OTA-treated groups developed
anemia manifested by a signicant decrease in red cell counts
(37%), packed cell volume percentage, and hemoglobin concentration. White cell counts, humoral immune response, and
cell-mediated immunity were also signicantly reduced. The
greatest concentrations of OTA (2 and 4 mg kg1) ever given to
broilers produced signicant depression in growth rate, reduced
feed consumption, and poor feed conversion efciency and
immune response (Verma et al., 2004).
Fumonisins
Fumonisins comprise the latest group of mycotoxins discovered. Since their isolation in 1988, these toxins have been
associated with previously known animal diseases, such as
Figure 12 Photomicrographs of broiler's kidneys showing normal architecture of tubular (C) and tubular ephithelium hyperplasia after intoxication
with ochratoxin A (OA). Haematoxylin and eosin, bar 180 mm (Courtesy of Dr. David Ledoux, University of Missouri, USA).
Palmitoyl-CoA + serine
Serine palmitoyltransferase
3-keto-sphinganine
3-keto-sphinganine redutase
Acyl-CoA
Sphinganine
N-Acyl-transferase
-CoA
Sphinganine
reductase
FB1
Dihydroxyceramide
Acyl CoA
CoA
N-Acyl-transferase
Ceramide
(Sphingosine + fatty acid)
Choline
phosphatase
Sphinganine
One or more
sugars
FB1
Degradation
Sphingomyelin
Glycosphingolipids
371
372
Zearalenone
Zearalenone was rst detected after hyperestrogenism symptoms appeared in swine fed moldy maize. These include prolonged estrus, anestrus, changes in libido, infertility, increased
incidence of pseudo pregnancy, increased udder or mammary
gland development, and abnormal lactation. The toxin is also
related to the following secondary complications: stillbirths,
abortions, mastitis, vulvovaginitis, and rectal or vaginal prolapses (Figure 14).
Endocrine disruption related to zearalenone is attributed to
both genomic and nongenomic effects. First, zearalenone
competes effectively with endogenous steroid estrogens, such
as 17-estradiol for the specic binding sites of estrogen receptors, with no preference between the two isomers, estrogen
receptor-, and estrogen receptor-. Estrogen receptors are
found in many different organs, such as the uterus, the
mammary glands, the bones, the liver, and the brain, where
zearalenone can, therefore, have an impact. Relative binding
afnities of the main metabolites are as follows: zearalanol4-zeralenol4-zearalanol4zearalenone4-zearalenol. The -isomers are approximately 10-fold more active
than the rest because of the position of the hydroxyl group.
Differences in production of or isomers explain differences
in sensitivity between species. For instance, pigs produce more
-ZEL, whereas poultry species produce more -zearalenol.
The estrogenic potency of zearalenone shows species-specic differences, and pigs, especially gilts, are considered to be
the most susceptible animal species, whereas poultry and ruminants show a higher tolerance to zearalenone-contaminated
feeds. Mechanistic studies showed that zearalenone interacts
not only with estrogen receptors, but also inuences the activity of enzymes involved in the steroidogenesis in the liver
and in the reproductive organs. In vivo and ex vivo experiments
show that zearalenone and its metabolites impair oocyte
maturation and embryonic development, but do not cause
Deoxynivalenol
DON is also known as vomitoxin due to its emetic effects after
acute exposure. In addition to that, symptoms caused by acute
exposure are similar to those observed after ionization: abdominal pain, salivation, diarrhea, vomiting, leukocytosis, and
gastrointestinal hemorrhage. Chronic exposure to DON causes
feed refusal due to alterations of serotogenic activity of both
the peripheral and central nervous system. Other effects related
to chronic ingestion of DON are weight loss, growth retardation, intestinal irritation, disruption of immune response,
and death. Toxicity of DON is caused by the same molecular
mechanisms of the other trichothecenes. Immune modulation induced by DON has been extensively studied, and it has
been shown that inammation arises from mitogen-activated
kinase activation, followed by activation of the prostaglandinendoperoxide synthase 2, and a consecutive increase of prostaglandins, which triggers the production of inammatory
cytokines.
Swine and other monogastric animals show the greatest
sensitivity to trichotecenes, followed by birds. NIV and DON
induce feed refusal and weight loss, show similar toxicities and
a combined concentration lower than 0.4 mg kg1 is described
as acceptable for swine, which is a relatively susceptible
species.
Recently, DON has been shown to maintain inammation
by favoring the Th-17-related immune response, which could
be associated with chronic inammatory intestinal diseases
(Cano et al., 2013). The intestine is, in fact, one of the most
sensitive organs to DON exposure. Low doses of this toxin can
induce morphological and histological impairment of intestinal epithelial cells, and alter intestinal permeability (Pinton
et al., 2012). DON toxicity has, thus, repercussions on the
neuroendocrine system, the intestinal system, and the immune
system. The immune system appears to be the most sensitive
to DON concentrations, followed by the neuroendocrine system, and nally, by the intestinal system. Among farm species,
373
Prevention of Mycotoxicoses
Every effort must be made to reduce the occurrence of mycotoxins. This is a complex task that requires an integrated
understanding of crop biology, agronomy, fungal ecology,
harvesting methods, storage conditions, food and feed processing and technology, and detoxication strategies. There are
a number of approaches that can be followed to minimize
mycotoxin contamination in the food and feed chains. They
involve prevention of fungal growth and therefore mycotoxin
formation, as well as strategies to reduce or eliminate mycotoxins from contaminated food commodities.
374
Detoxication Methods
Detoxication methods may be the physical removal of contaminated grains, or removal of the toxin by polar solvents,
destruction by heat, or degradation by chemical substances or
microorganisms. Although these methods may be effective,
they are extremely expensive and therefore not economically
viable. Heat is one physical method considered as able to
decrease FB1 concentration in corn grains from 87% to 100%.
However, temperature has to be approximately 150220 1C,
leading to a possible loss of nutritional content. Simply
washing the grains with water and sodium carbonate solution
may reduce fumonisin concentration in corn. Initial cleaning
of the corn in mills led to a 40% reduction in the concentration of aatoxins, and 32% in fumonisins (Scudamore and
Patel, 2000). However, these techniques have little applicability for large amounts of grain, as used in animal feed
plants.
In the animal industry, one of the most used strategies to
reduce the exposure to mycotoxins is to decrease their bioavailability by including various mycotoxin adsorbing agents in
the compound feed, which leads to a reduction in mycotoxin
uptake, as well as in the distribution to the blood and target
organs. A diverse variety of substances have also been investigated as potential mycotoxin-detoxyfying agents. Depending on their mode of action, these feed additives may act
by reducing the bioavailability of the mycotoxins or by degrading them or transforming them into less toxic metabolites.
Another strategy is the degradation of mycotoxins into
nontoxic metabolites by using biotransformation agents, such
as bacteria/fungi or enzymes. Substances that do not directly
interact with mycotoxins, i.e., antioxidant agents, immunostimulatory agents, are not considered sensu stricto as mycotoxin-detoxifying agents. However, such compounds may be
very efcient in the reduction of the toxicity of some
mycotoxins.
There is a wide variety of chemical products that may be
applied to high-moisture stored hay in order to control microbial growth. Among these products, ammonia may be
highlighted. Besides acting in the control of fungi by increasing
pH, it also affects the brous portion of the forage, solubilizing
Chemical Adsorbents
The use of adsorbent substances is the most common strategy
to prevent the toxic effects of mycotoxins that are already
formed in foods. Several minerals have been evaluated,
probably because of there are easy to incorporate in feeds,
without the need for any special equipment. The main
mechanism of adsorption of these materials is related to
charges exchanged between the adsorbent substance and the
mycotoxin. However, as mycotoxin structures are different, the
efcacy of chemical adsorbents is not similar for all of them.
One of the most important characteristic of adsorption is
the physical structure of the adsorbent, that is, the total charge
and total distribution, the size of the pores, and the accessible
surface area. However, the property of the adsorbent molecules, the type of mycotoxin, as well as the polarity, solubility, size, shape and, in the case of ionized compounds,
charge distribution and dissociation constants also have an
important role. Therefore, the efcacy of the whole adsorption
process has to be analyzed in relation to the particular properties of the adsorbent (Huwig et al., 2001). The most used
chemical adsorbents are activated charcoal, aluminum silicates, and mannan oligosaccharides (MOS).
Activated charcoal
Activated charcoal is an insoluble, very porous powder with
large surface in relation to its mass (5003500 m2 g1),
formed by the pyrolysis of organic material. It has been used as
an antidote against poisoning since the nineteenth century.
Therefore, it may also inactivate mycotoxins. In an aqueous
solution, it may adsorb most of the mycotoxins efciently,
considering that different activated charcoals have little or
no effect against mycotoxins. This may be due to the fact
that activated charcoal is a relatively unspecic adsorbent
and, therefore, essential nutrients may also be adsorbed, particularly if their concentration in feed is much greater than
that of mycotoxins. In studies with goats, however, it was
observed that high doses of activated charcoal were benecial
in acute intoxications caused by the ingestion of large amounts
of aatoxin. The adsorption of chemical substances by
vegetable charcoal depends on several factors: size of the
pores, surface area, chemical nature of the xenobiotic compound, dose of the vegetable charcoal, pH, and gastrointestinal content.
375
Mannan oligosaccharides
MOS are derived from the cell wall of yeasts (Saccharomyces
cerevisiae) and have a high degree of antigenicity, mainly due
to the mannan and glucan components. MOS may be used as
aatoxin adsorbents because they reduce the problems caused
by mycotoxins normally found in low-quality maize. MOS
have the ability to bind to different pathogens in the gastrointestinal tract and therefore prevent that they colonize it. In
vitro studies showed that commercial MOS adsorbed AFB1 and
zearalenone (Devegowda et al., 1998), and the addition of
esteried glucomannan in the diet of broilers was effective to
neutralize the toxic effects of naturally aatoxin-contaminated
diets.
Microbiological Strategies
Microorganisms with ability to bind with mycotoxins
Biological decontamination methods are being widely studied and may be a very promising choice, provided that they
are efcient, specic and environmentally correct. Of all
kinds of microorganisms available and that may be used for
aatoxin removal from a contaminated medium, yeast and
lactic acid bacteria (LAB) are the most studied and promising
ones.
Saccharomyces cerevisiae was originally used in animal feeds
as growth promoters; however, these organisms have showed to
be also useful against aatoxin contamination because of the
ability of its cell wall to bind to the mycotoxin. The adsorbent
effect of S. cerevisiae is attributed to the esteried glucomannan,
which is extracted from the yeast cell wall. Shetty and Jespersen
(2006) showed that most of the yeast strains bound to more
than 15% of AFB1, and the bond with toxin was highly strainspecic.
In the poultry industry, S. cerevisiae has been used as a
general performance promoter in poultry feed, and showed
benecial effects against the exposure to aatoxin.
Regarding LAB, El-Nezami et al. (1998) found some
strains of Lactobacillus (Lactobacillus rhamnosus GG and Lactobacillus rhamnosus LC-705) that were able to bind efciently
with large amounts (up to 80%) of AFB1 in the medium.
Peltonen et al. (2001) studied 15 types of Lactobacillus and ve
types of Bidobacterium, and found binding with AFB1 ranging
from 5.6% to 59.7%. A minimum concentration of 2 109
CFU ml1 of Lactobacillus and Propionibacterium is required to
bind to 50% of the AFB1, and binding is greater when LAB
concentration reaches 1010 CFU ml1. The binding effect is
dependent on the temperature, once the efciency in aatoxin
removal is greater at 37 1C than at 4 1C and 25 1C. Grampositive bacteria are best sequesters of aatoxin from the
medium than Gram-negative ones, with removal rates of 80
20%, respectively, suggesting that the ability to remove the
toxin is dependent on the structure of the cell wall (Bolognani
et al., 1997).
Data available today show that bacterial viability is not a
requisite for the removal of the toxin, and that the adsorption
process occurs rapidly, once nonviable cells were more efcient, and there was no difference in the intervals analyzed.
Therefore, it is necessary to study new bacterial cells, to have
greater understanding of the mechanism of action of these
376
References
Accensi, F., Pinton, P., Callu, P., et al., 2006. Ingestion of low doses of
deoxynivalenol does not affect hematological, biochemical or immune responses
of piglets. Journal Animal Science 84, 19351942.
Applegate, T.J., Schatzmayr, G., Pricket, K., Troche, C., Jiang, Z., 2009. Effect of
aatoxin culture on intestinal function and nutrient loss in laying hens. Poultry
Science 88, 12351241.
Asrani, R.K., Katoch, R.C., Gupta, V.K., et al., 2006. Effects of feeding Fusarium
verticillioide (formerly Fusarium moniliforme) culture material containing known
levels of fumonisin B9 in Japanese quail (Coturnix coturnix japonica). Poultry
Science 85, 11291135.
Benitz, J., 2002. Manejo integrado de micotoxinas utilizando el concepto del
anlisis de peligro y puntos de control crticos. Revista Industria Avcola 2,
2430.
Bolognani, F., Rumney, C.J., Rowland, I.R., 1997. Inuence of carcinogen binding
by lactic acid-producing bacteria on tissue distribution and in vivo mutagenicity
of dietary carcinogens. Food Chemical Toxicology 35, 535545.
Butkeraitis, P., Oliveira, C.A.F., Ledoux, D.R., et al., 2004. Effect of dietary fumonisin
B1 on laying Japanese quail. British Poultry Science 45, 798801.
Cano, P., Seeboth, J., Meurens, F., et al., 2013. Deoxynivalenol as a new factor
in the persistence of intestinal inammatory diseases: An emerging hypothesis
through possible modulation of Th17-mediated response. Plos One 8,
e53647.
Del Bianchi, M., Oliveira, C., Albuquerque, R., Guerra, J., Correa, B., 2005. Effects
of prolonged oral administration of aatoxin B and fumonisin B in broiler
chickens. Poultry Science 84, 18351840.
Devegowda, G.M., Raju, V.L.N., Swamy, H.V.L.N., 1998. Mycotoxins: Novel
solutions for their counteraction. Feedstuffs 70, 1216.
Diaz, D.E., 2005. The Mycotoxin Blue Book. Nottingham: University Press.
EFSA, 2004. Opinion of the scientic panel on contaminants in the food chain on a
request from the commission related to Zearalenone as undesirable substance in
animal feed. EFSA Journal 89, 135.
El-Nezami, H., Kankaanpa, P., Salminen, S., Ahokas, J., 1998. Physicochemical
alterations enhance the ability of dairy strains of lactic acid bacteria to
remove aatoxin from contaminated media. Journal Food Protection 61,
466468.
Geisen, R., 1998. PCR methods for the detection of mycotoxin producing fungi. In:
Bridge, P.D., Arora, K.K., Reddy, C.A., Elander, R.P. (Eds.), Applications of PCR
in Micology, rst ed. Cambridge: CAB International, pp. 243266.
Gompertz, O.F., Gambale, W., Paula, C.R., Corra, B., 2008. Caractersticas gerais
dos fungos. In: Trabulsi, L.R., Alterthum, F. (Eds.), Microbiologia. So Paulo,
SP: Atheneu, pp. 479491.
Grenier, B., Bracarense, A.P., Schwartz, H.E., et al., 2012. The low intestinal and
hepatic toxicity of hydrolyzed fumonisin B1 correlates with its inability to alter the
metabolism of sphingolipids. Biochemical Pharmacology 83, 14651473.
Grenier, B., Oswald, I.P., 2011. Mycotoxin co-contamination of foods and feeds:
Meta-analysis of publications describing toxicological interactions. World
Mycotoxin Journal 4, 285313.
Haschek, W.M., Gumprecht, L.A., Smith, G., Tumbleson, M.E., Constable, P.D.,
2001. Fumonisin toxicosis in swine: An overview of porcine pulmonary edema
and current perspectives. Environmental Health Perspectives 109, 251257.
Huwig, A., Freimund, S., Kappeli, O., Dutler, H., 2001. Mycotoxin detoxication of
animal feed by different adsorbents. Toxicology Letters 122, 179188.
Jespersen, L., 2003. Occurrence and taxonomic characteristics of strains of
Saccharomyces cerevisiae predominant in African indigenous fermented foods
and beverages. FEMS Yeast Research 3, 191200.
Jones, F.T., Hagler, W.H., Hamilton, P.B., 1982. Association of low levels of
aatoxin in feed with productivity losses in commercial broiler operations.
Poultry Science 61, 861868.
Kubena, L.F., Harvey, R.B., Buckley, S.A., Bailey, R.H., Rottinghaus, G.E., 1999.
Effects of long-term feeding of diets containing moniliformin, supplied by
Fusarium fujikuroi culture material, and fumonisin, supplied by Fusarium
moniliforme culture material, to laying hens. Poultry Science 78, 14991505.
Larsen, J.C., Hunt, J., Perrin, I., Ruckenbauer, P., 2004. Workshop on trichothecenes
with a focus on DON: Summary report. Toxicology Letters 153, 122.
Lombaert, G.A., DeVries, J.W., Trucksess, M.W., Jackson, L.P., 2002. Methods for
the Determination of Deoxynivalenol and Other Trichothecenes in Foods. New
York, NY: Kluwer Academic/Plenum Publishers.
Moshtaghian, J., Parsons, C.M., Leeper, R.W., Harrison, P.C., Koelkebeck, K.W.,
1991. Effect of sodium aluminosilicate on phosphorus utilization by chicks and
laying hens. Poultry Science 70, 955962.
Oswald, I.P., Marin, D.E., Bouhet, S., et al., 2005. Immunotoxicological risk of
mycotoxin for domestic animals in Europe. Food Additives and Contaminants 22,
354360.
Peltonen, K., El-Nezami, H., Haskard, C., Ahokas, J., Salminen, S., 2001. Aatoxin
B1 binding by dairy strains of lactic acid bacteria and bidobacteria. Journal
Dairy Science 84, 21522156.
Phillips, T.D., Sarr, A.B., Grant, P.G., 1995. Selective chemisorption and
detoxication of aatoxin by phyllosilicate clay. Natural Toxins 3, 204213.
Pinton, P., Accensi, F., Beauchamp, E., et al., 2008. Ingestion of deoxynivalenol
(DON) contaminated feed alters the pig vaccinal immune responses. Toxicology
Letters 177, 215222.
Pinton, P., Tsybulskyy, D., Lucioli, J., et al., 2012. Toxicity of deoxynivalenol and
its acetylated derivatives on the intestine: Differential effects on morphology,
barrier function, tight junctions proteins and MAPKinases. Toxicological Sciences
130, 180190.
Prathapkumar, S.H., Rao, V.S., Paramkishan, R.J., Bhat, R.V., 1997. Disease
outbreak in laying hens arising from the consumption of fumonisin-contaminated
food. British Poultry Science 38, 475479.
Scudamore, K.A., Patel, S., 2000. Survey for aatoxins, ochratoxin A, ZON and
fumonisins in maize imported into the United Kingdom. Food Additives and
Contaminants 17, 407416.
Shetty, P.H., Jespersen, L., 2006. Saccharomyces cerevisiae and lactic acid bacteria
as potential mycotoxin decontaminating agents. Trends in Food Science and
Technology 17, 4855.
377
Verma, J., Johri, T.S., Swan, B.K., Ameena, S., 2004. Effect of graded levels of
aatoxin and their combination on the performance and immune response of
broilers. British Poultry Science 45, 512518.
Relevant Websites
http://irmm.jrc.ec.europa.eu/EURLs/EURL_mycotoxins/legislation/Pages/index.aspx
European Commission Joint Research Centre.
http://www.mycotoxins.org/
European Mycotoxin Awareness Network.
http://www.fao.org/docrep/x5036e/x5036E00.htm#Contents
Food and Agriculture Organization (Mycotoxin Prevention and Control in
Foodgrains).
http://www.fda.gov/ICECI/ComplianceManuals/CompliancePolicyGuidanceManual/
ucm074703.htm
U.S. Food and Drug Administration (Action Levels for Aatoxins in Animal
Feeds).
http://www.mycotoxicology.org/
VICAM Mycotoxicology Newsletter.
Glossary
Aerobic Requiring the presence of air or free oxygen
for life.
Cell-mediated immunity Immunity dependent on the
recognition of antigen by effector T cells.
Granuloma Inltration of a dense, macrophage-rich mass
of cells.
Humoral immune response Antibody-mediated immunity.
Polymerase chain reaction test (PCR) Biotechnology to
amplify specic portions of deoxyribonucleic acid (DNA)
The Disease
Bovine tuberculosis (bTB) is a chronic bacterial disease caused
by the slow-growing, obligate intracellular bacterium Mycobacterium bovis. This pathogen has a worldwide distribution
and, in several countries, bTB remains a major health problem
in domestic livestock. The disease costs US$3 billion annually
in global agricultural losses (Garnier et al., 2003) and it is
considered within the four most important cattle diseases
globally (Finlay et al., 2012).
Mycobacterium bovis is primarily a pathogen of cattle but it
can also infect other mammals including badgers, possums,
deer, goats, sheep, and camelids (Pollock and Neill, 2002;
Scantlebury et al., 2004; Skuce et al., 2012). The bacterium is
also able to affect humans, which makes bTB a relevant
zoonosis that can spread through inhalation of infectious
droplets and by ingestion of raw milk (Thoen and Barletta,
2006). In developed countries, eradication programs have signicantly reduced the prevalence of this disease but, in some
cases, reservoirs in wildlife make complete eradication difcult.
bTB primarily involves the respiratory system and associated lymph nodes. Infected individuals shed M. bovis in respiratory secretions, feces and milk, and occasionally in urine
and vaginal secretions or semen, with large numbers of organisms shed in the late stages of infection. Most of the
transmission occurs via aerosol circulation between animals
that are in close proximity (Cassidy, 2006; Skuce et al., 2012);
however, indirect transmission through ingestion of contaminated feed has also been demonstrated (Neill et al., 1994;
Okafor et al., 2011). Interestingly, Collins and Granje (1983)
reported that, in experimentally infected calves, the minimum
dose required to establish infection by the respiratory tract was
up to 1000 times less than via the oral route. However, the oral
route is likely most important in calves nursing infected cows
(Neill et al., 1994).
At present, M. bovis infection in cattle rarely appears as
clinical disease. Instead, it is detected in apparently healthy
animals, responding to any of the available diagnostic tests
(Collins, 2006; Skuce et al., 2012). When clinical signs are
378
present they are nonspecic and, as bTB is a chronic debilitating disease, symptoms generally take months to develop.
Loss of body condition, inappetence, and progressive emaciation may occur in advanced cases and respiratory signs may
include chronic moist cough (especially during exercise) and
thoracic abnormalities at auscultation. Lymph nodes may be
enlarged, affecting contiguous blood vessels, airways, or the
digestive tract. Mammary and reproductive tract involvement
is rare and is usually accompanied by enlargement of associated lymph nodes (Divers and Peek, 2008).
bTB has a signicant impact due to the cost of ofcial
control programs and represents an obstacle to domestic and
international trade. Being a zoonotic pathogen, M. bovis has
implications in human health, particularly in the developing
world, although human disease due to this mycobacterium is
now signicantly less common than in the past decades (Biet
et al., 2005; Robinson et al., 2012).
doi:10.1016/B978-0-444-52512-3.00194-7
described as acid-fast, and as once stained, it resists decolonization with acidied organic solvents (Lawn and Zumla,
2011).
The waxy coat confers the distinctive characteristics of the
genus: acid fastness, extreme hydrophobicity, resistance to
environmental exposure, and distinctive immunological
properties. It also contributes to the slow growth rate of some
Mycobacteria by restricting the uptake of nutrients
(Palomino, 2007).
On the basis of genomic analysis, this group has been
divided into two separate clusters, corresponding to the traditional fast-growing mycobacteria, represented by nonpathogenic environmental isolates, and the slow-growing
mycobacteria, containing most of the overt pathogens (Harris
and Barleta, 2001). Slow-growing mycobacteria of importance
in human and veterinary medicine are found in two major
complexes: Mycobacterium tuberculosis and Mycobacterium
avium. The M. tuberculosis complex includes M. tuberculosis, M.
bovis, M. africanum, and M. microti. Mycobacterium tuberculosis
causes tuberculosis in man, primates, dogs, and other animals.
Mycobacterium bovis causes tuberculosis in cattle, domestic and
wild ruminants, man and other primates, and swine and other
animals (Eglund, 2002).
The most relevant member of the slow-growing group, M.
tuberculosis, is an obligate intracellular pathogen that can infect
several animal species, although human beings are the principal hosts. It is an aerobic, acid-fast, nonmotile, nonencapsulated, nonspore-forming bacillus that grows most
successfully in tissues with high oxygen content, such as the
lungs. Compared with the cell walls of other bacteria, the
lipid-rich cell wall is relatively impermeable to basic dyes
unless combined with phenol (Lawn and Zumla, 2011).
However, the M. avium complex (MAC) consists of genetically similar bacteria including, among others, M. avium
subsp. avium and M. avium subsp. paratuberculosis, which is the
causative agent of Johne's disease in cattle. Microorganisms in
this complex are opportunistic pathogens present in multiple
locations; although human exposure to MAC is ubiquitous,
most individuals rarely develop infection (St. Amand et al.,
2005). Relevant to animal health, Mycobacterium paratuberculosis, a pathogen for ruminants, is an obligate parasite
unable to replicate in the environment (Eglund, 2002).
The unique cell wall in the Mycobacterium group enables the
organism to persist in the environment and contributes to its
resistance to low pH, high temperature, and chemical agents
(Manning, 2001). M. bovis can survive for several months in
the environment, particularly in cold, dark, and moist conditions. At room temperature, the survival time varies from 18
to 330 days, depending on the exposure to sunlight and the
organism is infrequently isolated from soil or pastures grazed
by infected cattle.
At the molecular level, the genetic conguration of Mycobacteria, in particular M. tuberculosis, has been the subject of
extensive research. The sequencing of the M. tuberculosis genome has been a major advance to better understand the
biology of the bacterium. Findings have allowed the subsequent identication of specic antigens for the development
of diagnostics tests, multivalent vaccines, and biomarkers for
tuberculosis (Lawn and Zumla, 2011). The discovery of
genomic diversity help determine the factors involved in
379
cellular growth and metabolism, virulence genes, and antibiotic resistance (Lamrabet and Drancourt, 2012).
Although there are many M. tuberculosis strains, studies of
the phylogeny and ecology of M. tuberculosis have revealed six
main strain lineages that are associated with particular geographical regions (Cole et al., 1998; Lawn and Zumla, 2011).
However, recent advances in mycobacterial genomics suggest
that the amount of sequence variation in the M. tuberculosis
genome might have been underestimated (Ford et al., 2012)
and that some genetic diversity have important phenotypic
consequences. Indeed, the use of whole genome sequencing
has shown signicant heterogeneity in bacterial populations,
even between strains with identical MIRU/VNTR, or RFLP
patterns (Ford et al., 2012).
As indicated by Rehren et al. (2007), the M. bovis and M.
tuberculosis genomes show 499% identity at the nucleotide
level. However, distinct phenotypes, virulence, and host range
differentiate both pathogens, suggesting that distinctive
mechanisms of gene expression might be involved in determining the differences between both bacteria (Rehren et al.,
2007; Garnier et al., 2003).
380
Diagnosis
Diagnostic tests for tuberculosis can be divided into two categories: those detecting the organism and those that evaluate
the host response to infection. The rst category includes,
among others, smear and acid-fast stain, bacteriologic culture,
and polymerase chain reaction test (PCR), which amplies one
or more specic DNA sequences, generating thousands to
millions of copies (Bekmurzayeva et al., 2013). However, indirect diagnostic is based on clinical signs, gross and microscopic pathology, and cellular and humoral immune
responses (Maas et al., 2013).
The microscopic demonstration of acid-fast bacilli in direct
smears from clinical samples or tissues stained with the Ziehl/
Neelsen stain, a uorescent acid-fast stain, or immunoperoxidase techniques provides a presumptive diagnosis. However,
conrmation requires additional testing. Bacteriologic culture
remains one of the most important methods for tuberculosis
diagnosis, despite the prolonged incubation time and the
signicant decontamination and biocontainment requirements (Robbe-Austerman et al., 2013). Bacteriologic culture
has high specicity and sensitivity and some modied automated mycobacterial radiometric culture devises, including the
BACTEC system (Becton Dickinson Laboratories, Sparks, MD,
USA), have been designed for human clinical laboratories.
Among other advantages, these devises use liquid culture that
provides a greater sensitivity. The two automated systems most
commonly used are the BACTEC MGIT 960 System, which
uses the MGIT 960 media (MGIT), and the BACTEC 460 TB
System, which uses BACTEC 12B media (BACTEC). Although
381
these media systems are comparable, the MGIT typically recovered more mycobacteria other than M. tuberculosis complex
than the BACTEC, but had higher contamination rates (NRC,
2003; Robbe-Austerman et al., 2013).
For more rapid identication, several PCR-based methods
have been developed and assays targeting M. tuberculosis-specic sequences, including IS6110 and the MPT64 gene, have
been widely applied (Kim et al., 2013). Specic sequences of
DNA for diverse mycobacteria have been used as targets for
PCR amplication and differentiation of bacteria of the M.
tuberculosis complex from nontuberculous mycobacteria, as
well as for specic differentiation of M. bovis from other
members of the M. tuberculosis complex (Maas et al., 2013). A
well-validated probe for the Mycobacterium genus that targets
the conserved sequence of the rpoB gene, which encodes the
subunit of RNA polymerase, is now available. This probe facilitates the identication of all Mycobacterium spp. and also
distinguishes Mycobacterium spp. at the species level by restriction enzyme analysis (Lee et al., 2000; Kim et al., 2013).
As related to host reactions to infection, gross lesions observed postmortem in tissues, organs, and carcasses due to M.
tuberculosis complex infection are based on the typical granulomatous appearance of tuberculous lesions (Maas et al.,
2013). In naturally infected cattle, tuberculous lesions are
found most frequently in the dorsocaudal region of the lungs,
often close to the pleural surface (Cassidy, 2006). In countries
where the disease has been subject to longstanding control,
lesions are found with higher frequency in the lymph nodes
associated with the respiratory system (tracheobronchial and
mediastinal) than in the lung parenchyma (Corner, 1994).
However, in disseminated cases, multiple small granulomas
may be found in numerous organs.
As cell-mediated immune responses are the rst and
strongest host response to mycobacterial infections, this category of tests is useful for early detection of MAP infection
(Robbe-Austerman et al., 2007). Among others, these include
interferon-gamma assay and the tuberculin skin test. The
interferon-gamma assay is a test based on production and release of IFN-g by sensitized bovine lymphocytes in response to
in-vitro stimulation with a series of mycobacterial antigens. As
cellular immunity is developed soon after infection, this test is
considered the most sensitive during early infection (Collins,
1996; Stabel, 2001). Whole blood or peripheral blood
mononuclear cells are incubated in the presence or absence of
mycobacterial antigens (avian or bovine puried protein derivative (PPD) or other specic antigens of Mycobacterium spp)
that induce previously sensitized T cells to produce IFN-g
(Bekmurzayeva et al., 2013; Maas et al., 2013). Some studies
have questioned the specicity of the IFN-g assay, indicating
that the test is subject to cross-reactivity with other mycobacteria (Huda et al., 2003). Although results from some
studies suggest that the specicity values are moderate to low
(Kalis et al., 2003; de la Rua-Domenech et al., 2006), some
eld trials have determined specicities as high as 94100%
(Palmer and Waters, 2006).
A widely spread diagnostic test based on the CMI response
is the intradermal tuberculin skin test, which measures a DTH
to mycobacterial antigens. The swelling formed 3 days after
injection of a mycobacterial PPD is measured to determine
the increase of skin thickness (Collins, 2006; Kalis et al., 2003;
382
Disease Control
Eradication of TB from cattle has been successful in several
countries including Austria, Belgium, France, Canada, and
most of the United States (de la Rua-Domenech, 2006). Traditionally, control efforts have included the removal of
tuberculin reactors and suspect cattle (test-and-slaughter),
execution of test-and-segregation methods, disinfection of
383
384
References
Allen, A.R., Minozzi, G.E., Glass, J., et al., 2010. Bovine tuberculosis: The genetic
basis of host susceptibility. Proceedings of the Royal Society B 277, 27372745.
Ameni, G., Aseffa, A., Engers, H., et al., 2007. High prevalence and increased
severity of pathology of bovine tuberculosis in Holsteins compared to zebu
breeds under eld cattle husbandry in central Ethiopia. Clinical and Vaccine
Immunology 14, 13561361.
Bekmurzayeva, A., Sypabekova, M., Kanayeva, D., 2013. Tuberculosis diagnosis
using immunodominant, secreted antigens of Mycobacterium tuberculosis.
Tuberculosis 93, 381388.
Biet, F., Boschiroli, M.L., Thorel, M.F., Guilloteau, L.A., 2005. Zoonotic aspects of
Mycobacterium bovis and Mycobacterium avium-intracellulare complex (MAC).
Veterinary Research 36, 411436.
Bohm, M., Hutchings, M.R., White, P.C.L., 2009. Contact networks in a wildlifelivestock host community: Identifying high-risk individuals in the transmission of
bovine TB among badgers and cattle. PLoS One 4 (4), e5016.
Bruning-Fann, C.S., Schmitt, S.M., Fitzgerald, S.D., et al., 1998. Mycobacterium bovis in coyotes from Michigan. Journal of Wildlife Diseases 34,
632636.
Bruning-Fann, C.S., Schmitt, S.M., Fitzgerald, S.D., et al., 2001. Bovine tuberculosis
in free ranging carnivores from Michigan. Journal of Wildlife Diseases 37,
5864.
Cassidy, J.P., 2006. The pathogenesis and pathology of bovine tuberculosis with
insights from studies of tuberculosis in humans and laboratory animal models.
Veterinary Microbiology 112, 151161.
Chiodini, R.J., Davis, W.C., 1993. The cellular immunology of bovine
paratuberculosis: Immunity may be regulated by CD4 helper and CD8
immunoregulatory T lymphocytes which down-regulate gamma/delta T-cell
cytotoxicity. Microbial Pathogenesis 14, 355367.
Churbanov, A., Milligan, B., 2012. Accurate diagnostics for bovine tuberculosis
based on high throughput sequencing. PLoS One 7 (11), e50147.
Cocito, C., Gilot, P., Coene, M., et al., 1994. Paratuberculosis. Clinical Microbiology
Reviews 7, 328345.
Cole, S.T., Brosch, R., Parkhill, J., et al., 1998. Deciphering the biology of
Mycobacterium tuberculosis from the complete genome sequence. Nature 393,
537544.
Collins, C.H., Grange, J.M., 1983. A review, the bovine tubercle bacillus. Journal of
Applied Bacteriology 55, 1329.
Collins, J.D., 2006. Tuberculosis in cattle: Strategic planning for the future.
Veterinary Microbiology 112, 369381.
Collins, M.T., 1996. Diagnosis of paratuberculosis (including pathology). Veterinary
Clinics of North America Food Animal Practice 12, 357371.
Conner, M.M., Ebinger, M.R., Blanchong, J.A., Cross, P.C., 2008. Infectious disease
in cervids of North America. Annals of the New York Academy of Sciences 1134,
146172.
Corner, L.A.L., 1994. Post mortem diagnosis of Mycobacterium bovis infection in
cattle. Veterinary Microbiology 40, 5363.
Corner, L.A.L., 2006. The role of wild animal populations in the epidemiology of
tuberculosis in domestic animals: How to assess the risk. Veterinary
Microbiology 112, 303312.
Cousins, D.V., Dawson, D.J., 1999. Tuberculosis due to Mycobacterium bovis in the
Australian population: Cases recorded during 19701994. International Journal
of Tuberculosis and Lung Disease 3, 715721.
Coussens, P.M., Verman, N., Coussens, M.A., Elftman, M.D., McNulty, A.M., 2004.
Cytokine gene expression in peripheral blood mononuclear cells and tissues of
cattle infected with Mycobacterium avium subsp. paratuberculosis: Evidence for
an inherent proinammatory gene expression pattern. Infection and Immunity 72,
14091422.
van Dijk, J., 2013. Towards risk-based test protocols: Estimating the contribution of
intensive testing to the UK bovine tuberculosis problem. PLoS One 8 (5), e63961.
Divers, J.D., Peek, S., 2008. Rebhuns, Diseases of Dairy Cattle, second ed.
St. Louis, MO: Saunders Elsevier.
Donald, P.R., Marais, B.J., Barry III, C.E., 2010. Age and the epidemiology and
pathogenesis of tuberculosis. Lancet 375, 18521854.
Eglund, S., 2002. Molecular biology techniques as a tool for detection and
characterization of Mycobacterium avium subsp. paratuberculosis. Doctoral
dissertation, Department of Veterinary Microbiology, SLU. Acta Universitatis
agriculturae Sueciae. Veterinaria, vol. 123. ISSN 1401-6257, ISBN 91-576-6366-1.
Finlay, E.K., Berry, D.P., Wickham, B., Gormley, E.P., Bradley, D.G., 2012. A
genome wide association scan of bovine tuberculosis susceptibility in HolsteinFriesian dairy cattle. PLoS One 7 (2), e30545.
Ford, C., Yusim, K., Ioerger, T., et al., 2012. Mycobacterium tuberculosis
Heterogeneity revealed through whole genome sequencing. Review. Tuberculosis
92, 194201.
Frieden, T.R., Sterling, T.R., Munsiff, S.S., Watt, C.J., Dye, C., 2003. Tuberculosis.
Review. Lancet 362, 887899.
Garnier, T., Eiglmeier, K., Camus, J.C., et al., 2003. The complete genome sequence
of Mycobacterium bovis. Proceedings of National Academy of Sciences USA
100, 78777882.
Gil, O., Diaz, I., Vilaplana, C., et al., 2010. Granuloma encapsulation is a key factor
for containing tuberculosis infection in minipigs. PLoS One 5 (4), e10030.
Gilbert, M., Mitchell, A., Bourn, D., et al., 2005. Cattle movements and bovine
tuberculosis in Great Britain. Nature 435, 491496.
Good, M., Duignan, A., 2011. Perspectives on the history of bovine TB and the role
of tuberculin in bovine tb eradication. Review Article. Veterinary Medicine
International 2011, 111.
Gopal, R., Goodchild, A., Hewinson, G., De la Rua-Domenech, R., Clifton-Hadley, R.,
2006. Introduction of bovine tuberculosis to north-east England by bought in
cattle. Veterinary Record 159, 265271.
Granje, J.M., 2001. Mycobacterium bovis infection in human beings. Tuberculosis
81, 7177.
Grifn, J.M., Dolan, L.A., 1995. The role of cattle-to-cattle transmission of
Mycobacterium bovis in the epidemiology of tuberculosis in cattle in the
Republic of Ireland: A review. Irish Veterinary Journal 48, 228234.
Grifn, J.M., Martin, S.W., Thorburn, M.A., Eves, J.A., Hammond, R.F., 1996. A
case-control study on the association of selected risk factors with the occurrence
of bovine tuberculosis in the Republic of Ireland. Preventive Veterinary Medicine
27, 7587.
Harris, N.B., Barleta, R.G., 2001. Mycobacterium avium subsp. paratuberculosis in
veterinary medicine. Clinical Microbiology Reviews 14, 489512.
Huda, A., Jungersen, G., Chistoffersen, A.B., Lin, P., 2003. Diagnosis of bovine
paratuberculosis by interferon gamma (IFN-gamma) test. Acta Veterinaria
Scandinavica 44, 281.
Humblet, M.F., Boschiroli, M.L., Saegerman, C., 2009. Classication of worldwide
bovine tuberculosis risk factors in cattle: A stratied approach. Veterinary
Research 40, 50.
385
Hunter, R.L., 2011. Pathology of post primary tuberculosis of the lung: An illustrated
critical review. Tuberculosis 91, 497509.
Kalis, C.H., Collins, M.T., Hesselink, J.W., Barkema, H.W., 2003. Specicity of two
tests for the early diagnosis of bovine paratuberculosis based on cell-mediated
immunity: The Johnin skin test and the gamma interferon assay. Veterinary
Microbiology 97, 7386.
Kaneene, J.B., Bruning-Fann, C.S., Granger, L.M., Miller, R., Porter-Spalding, A.,
2002. Environmental and farm management factors associated with tuberculosis
on cattle farms in northeastern Michigan. Journal of American Veterinary Medical
Association 221, 837842.
Kim, Y., Choi, Y., Jeon, B.Y., et al., 2013. A simple and efcient multiplex pcr assay
for the identication of Mycobacterium genus and Mycobacterium tuberculosis
complex to the species level. Yonsei Medical Journal 54, 12201226.
Lamrabet, O., Drancourt, M., 2012. Genetic engineering of Mycobacterium
tuberculosis: A review. Tuberculosis 92, 365376.
Lawn, S.D., Acheampong, J.W., 1999. Pulmonary tuberculosis in adults: Factors
associated with mortality at a Ghanaian teaching hospital. West African Journal
of Medicine 18, 270274.
Lawn, S.D., Zumla, A.I., 2011. Tuberculosis. Lancet 378, 5772.
Lee, H., Park, H.J., Cho, S.N., Bai, G.H., Kim, S.J., 2000. Species identication of
mycobacteria by PCR-restriction fragment length polymorphism of the rpoB gene.
Journal of Clinical Microbiology 38, 29662971.
Lees, V.W., Copeland, S., Rousseau, P., 2003. Bovine tuberculosis in elk (Cervus
elaphus manitobensis) near Riding Mountain National Park, Manitoba, from 1992
to 2002. Canadian Veterinary Journal 44, 830831.
Lesslie, I.W., 1968. Cross infections with mycobacteria between animals and man.
Bulletin of the International Union Against Tuberculosis 41, 285288.
Lyashchenko, K.P., Greenwald, R., Esfandiari, J., et al., 2006. Tuberculosis in
elephants: Antibody responses to dened antigens of Mycobacterium
tuberculosis, potential for early diagnosis, and monitoring of treatment. Clinical
and Vaccine Immunology 13, 722732.
Maas, M., Michel, A.L., Rutten, V.P.M.G., 2013. Facts and dilemmas in diagnosis of
tuberculosis in wildlife. Review. Comparitive Immunology, Microbiology and
Infectious Diseases 36, 269285.
Manning, E.J., 2001. Mycobacterium avium subspecies paratuberculosis: A review of
current knowledge. Journal of Zoo and Wildlife Medicine 32, 293304.
Menin, A., Fleith, R., Reck, C., et al., 2013. Asymptomatic cattle naturally infected
with Mycobacterium bovis present exacerbated tissue pathology and bacterial
dissemination. PLoS One 8 (1), e53884.
Menzies, F.D., Neill, S.D., 2000. Cattle-to-cattle transmission of bovine tuberculosis.
Veterinary Journal 160, 92106.
Miller, M., Olea-Popelka, F., 2013. One Health in the shrinking world: Experiences
with tuberculosis at the humanlivestockwildlife interface. Comparitive
Immunology, Microbiology and Infectious Diseases 36, 263268.
Miller, R.S., Sweeney, S.J., 2013. Mycobacterium bovis (bovine tuberculosis)
infection in North American wildlife: Current status and opportunities for
mitigation of risks of further infection in wildlife populations. Epidemiology &
Infection 141, 13571370.
Monaghan, M.L., Doherty, M.L., Collins, J.D., Kazda, J.F., Quinn, P.J., 1994. The
tuberculin test. Veterinary Microbiology 40, 111124.
Morris, C.A., 2007. A review of genetic resistance to disease in Bos Taurus cattle.
Veterinary Journal 174, 481491.
Mller, B., Drr, S., Alonso, S., et al., 2013. Zoonotic Mycobacterium bovis-induced
tuberculosis in humans. Emerging Infectious Diseases 19, 899908.
Munyeme, M., Muma, J.B., Samui, K.L., et al., 2009. Prevalence of bovine
tuberculosis and animal level risk factors for indigenous cattle under different
grazing strategies in the livestock/wildlife interface areas of Zambia. Tropical
Animal Health and Production 41, 345352.
Naranjo, V., Gortazar, C., Vicente, J., de la Fuente, J., 2008. Evidence of the role of
European wild boar as a reservoir of Mycobacterium tuberculosis complex.
Veterinary Microbiology 127, 19.
National Research Council (NRC), 2003. Committee on Diagnosis and Control of
Johne's Disease. Washington, DC: National Academies Press.
Neill, S.D., Pollock, J.M., Bryson, D.B., Hanna, J., 1994. Pathogenesis of
Mycobacterium bovis infection in cattle. Veterinary Microbiology 40,
4152.
Nol, P., Palmer, M.V., Waters, F.E., et al., 2008. Efcacy of oral and parenteral
Mycobacterium bovis bacilli Calmette-Guerin vaccination against experimental
bovine tuberculosis in white-tailed deer (Odocoileus virginianus): A feasibility
study. Journal of Wildlife Diseases 44, 247259.
O'Brien, D.J., Schmitt, S.M., Fitzgerald, S.D., Berry, D.E., Hickling, G.J., 2006.
Managing the wildlife reservoir of Mycobacterium bovis: The Michigan, USA,
experience. Veterinary Microbiology 112, 313323.
386
Okafor, C.C., Grooms, D.L., Bruning-Fann, C.S., Averill, J.J., Kaneene, J.B., 2011.
Descriptive epidemiology of bovine tuberculosis in Michigan (19752010):
Lessons learned. Veterinary Medicine International. ID: 874924.
Paige, C., Bishai, W.R., 2010. Penitentiary or penthouse condo: The tuberculous
granuloma from the microbe's point of view. Cell Microbiology 12, 301309.
Palmer, M.V., 2007. Tuberculosis: A reemerging disease at the interface of domestic
animals and wildlife. Current Topics in Microbiology and Immunology 315,
195215.
Palmer, M.V., Thacker, T.C., Waters, W.R., 2007. Vaccination of white-tailed deer
(Odocoileus virginianus) with Mycobacterium bovis bacillus Calmette Guern.
Vaccine 25, 25892597.
Palmer, M.V., Waters, W.R., 2006. Advances in bovine tuberculosis diagnosis and
pathogenesis: What policy makers need to know. Veterinary Microbiology 112,
181190.
Palmer, M.V., Waters, W.R., Whipple, D.L., 2004a. Investigation of the transmission
of Mycobacterium bovis from deer to cattle through indirect contact. American
Journal of Veterinary Research 65, 14831489.
Palmer, M.V., Waters, W.R., Whipple, D.L., 2004b. Shared feed as a means of deerto-deer transmission of Mycobacterium bovis. Journal of Wildlife Diseases 40,
8791.
Palmer, M.V., Whipple, D.L., 2006. Survival of Mycobacterium bovis on feedstuffs
commonly used as supplemental feed for white-tailed deer (Odocoileus
virginianus). Journal of Wildlife Diseases 42, 853858.
Palomino, J.C., 2007. Tuberculosis 2007. From Basic Science to Patient Care. In:
Palomino, J.C., Leao, S.C., Ritacco, V. (Eds.), rst ed, pp. 93105. Available at:
www.TuberculosisTextbook.com.
Phillips, C.J., Foster, C.R., Morris, P.A., Teverson, R., 2002. Genetic and
management factors that inuence the susceptibility of cattle to Mycobacterium
bovis infection. Animal Health Research Reviews 3, 313.
Pollock, J.M., McNair, J., Welsh, M.D., et al., 2001. Immune responses in bovine
tuberculosis. Tuberculosis 81, 103107.
Pollock, J.M., Neill, S.D., 2002. Mycobacterium bovis infection and tuberculosis in
cattle. Veterinary Journal 163, 115127.
Pollock, J.M., Rodgers, J.D., Welsh, M.D., McNair, J., 2006. Pathogenesis of bovine
tuberculosis: The role of experimental models of infection. Veterinary
Microbiology 112, 141150.
Rehren, G., Walters, S., Fontan, P., Smith, I., Zarraga, A., 2007. Differential gene
expression between Mycobacterium bovis and Mycobacterium tuberculosis.
Tuberculosis 87, 347359.
Renwick, A.R., White, P.C.L., Bengis, R.G., 2007. Bovine tuberculosis in southern
African wildlife: A multi-species host-pathogen system. Epidemiology & Infection
135, 529540.
Robbe-Austerman, S., Bravo, D.M., Harris, B., 2013. Comparison of the MGIT 960,
BACTEC 460 TB and solid media for isolation of Mycobacterium bovis in United
States veterinary specimens. BMC Veterinary Research 9, 7479.
Robbe-Austerman, S., Stabel, J.R., Morrical, D.G., 2007. Skin test and gamma
interferon enzyme-linked immunosorbent assay results in sheep exposed to dead
Mycobacterium avium subspecies paratuberculosis organisms. Journal of
Veterinary Diagnostic Investigation 19, 8890.
Robert, J., Boulahbal, F., Trystram, D., et al., 1999. A national survey of human
Mycobacterium bovis infection in France. International Journal of Tuberculosis
and Lung Disease 3, 711714.
Robinson, P.A., Corner, L.A., Courcier, E.A., et al., 2012. BCG vaccination against
tuberculosis in European badgers (Meles meles): A review. Comparative
Immunology, Microbiology & Infectious Diseases 35, 277287.
de la Rua Domenech, R., 2006. Human Mycobacterium bovis infection in the United
Kingdom: Incidence, risks, control measures and review of the zoonotic aspects
of bovine tuberculosis. Tuberculosis 86, 77109.
de la Rua-Domenech, R., Goodchild, A.T., Vordermeier, H.M., et al., 2006. Ante
mortem diagnosis of tuberculosis in cattle: A review of the tuberculin tests,
gamma interferon assay and other ancillary diagnostic techniques. Research in
Veterinary Science 81, 190210.
Scantlebury, M., Hutchings, M.R., Allcroft, D.J., Harris, S., 2004. Risk of disease
from wildlife reservoirs: Badgers, cattle, and bovine tuberculosis. Journal of Dairy
Science 87, 330339.
Schiller, I., Oesch, B., Vordermeier, H.M., et al., 2010. Bovine tuberculosis: A review
of current and emerging diagnostic techniques in view of their relevance for
disease control and eradication. Transboundary and Emerging Diseases 57,
205220.
Shah, N.S., Wright, A., Bai, G.H., et al., 2007. Worldwide emergence of extensively
drug-resistant tuberculosis. Emerging Infectious Diseases 3, 380387.
Skuce, R.A., Allen, A.R., McDowell, S.W.J., 2012. Herd-level risk factors for bovine
tuberculosis: A literature review. Veterinary Medicine International. ID: 621210.
St. Amand, A.L., Frank, D.N., De Groote, M.A., Pace, N.R., 2005. Use of specic
rRNA oligonucleotide probes for microscopic detection of Mycobacterium avium
complex organisms. Journal of Clinical Microbiology 43, 15051514.
Stabel, J.R., 2001. An evaluation of a modied interferon-gamma assay for the
detection of paratuberculosis in dairy herds. Veterinary Immunology and
Immunopathology 79, 6981.
Sun, L., Song, Y., Riaz, H., et al., 2012. Polymorphisms in toll-like receptor 1 and 9
genes and their association with tuberculosis susceptibility in Chinese Holstein
cattle. Veterinary Immunology and Immunopathology 147, 195201.
The Center for Food Security and Public Health, 2009. Bovine Tuberculosis. Ames,
IA: Iowa State University. Available at: http://www.cfsph.iastate.edu/Factsheets/
pdfs/bovine_tuberculosis.pdf (accessed 06.01.13).
Thoen, C.O., Barletta, R., 2006. Pathogenesis of Mycobacterium bovis. In: Thoen, C.
O., Steele, J.H., Gilsdorf, M.J. (Eds.), Mycobacterium bovis Infection in Animals
and Humans. Ames, IA: Blackwell Publishing, pp. 1833 (Chapter 4).
Thoen, C., LoBue, P., de Kantor, I., 2006. The importance of Mycobacterium bovis
as a zoonosis. Veterinary Microbiology 112, 339345.
Tiwari, A., VanLeeuwen, J.A., McKenna, S.L., Keefe, G.P., Barkema, H.W., 2006.
Johne's disease in Canada Part I: Clinical symptoms, pathophysiology,
diagnosis, and prevalence in dairy herds. Canadian Veterinary Journal 47,
874882.
Torres-Gonzalez, P., Soberanis-Ramos, O., Martinez-Gamboa, A., et al., 2013.
Prevalence of latent and active tuberculosis among dairy farm workers exposed
to cattle infected by Mycobacterium bovis. PLoS Neglected Tropical Diseases 7
(4), e2177.
Van Campen, H., Rhyan, J., 2010. The role of wildlife in diseases of cattle
review article. Veterinary Clinics of North America: Food Animal Practice 26,
147161.
Volkman, H.E., Clay, H., Beery, D., et al., 2004. Tuberculous granuloma formation is
enhanced by a Mycobacterium virulence determinant. PLoS Biology 2 (11), e367.
Welsh, M.D., Cunningham, R.T., Corbett, D.M., et al., 2005. Inuence of
pathological progression on the balance between cellular and humoral immune
responses in bovine tuberculosis. Immunology 114, 101111.
Wobeser, G., 2009. Bovine tuberculosis in Canadian wildlife: An updated history.
Canadian Veterinary Journal 50, 11691176.
World Health Organization (WHO), 2004. Anti-Tuberculosis Drug Resistance in the
World: Report 4. WHO/HTM/TB/2004.343. Geneva: World Health Organization.
Glossary
Allostasis The ability of an animal to cope with physical
and mental stress.
Animal welfare The current mental and physical states of
an animal.
Distress A state of being when an animal can no longer
cope with a stressor in order to maintain homeostasis that
takes biological resources away from other biological
functions.
Exsanguination An adjunctive method of euthanasia to
ensure death in an unconscious animal. An incision is made
on the throat and all blood vessels and sensory and motor
nerves are transected.
Denitions
The term animal welfare has been used by many in society
and the media with various intentions of meaning. Much of
the disagreement concerning the denition of the term lies in
the mixing of the scientic and ethical questions of what
animal welfare is. Even though the basis of the concept does
have moral implications, this article will focus on the science
of animal welfare. As more science on the welfare of animals is
acquired, the denition of the term evolves but there are
underlining concepts that remain consistent. The Bramble
Committee (1965) was one of the rst inuential writings on
animal welfare. It not only had a signicant effect on how the
world views animal welfare but also had a direct effect on
legislative action taken regarding welfare in Europe. The Ofce
International des Epizooties (OIE), commonly known as
World Organization for Animal Health, denes an animals
welfare to be good if the animal: is healthy, comfortable, well
nourished, safe, able to express innate behavior and. Not
suffering from unpleasant states such as pain, fear of distress.
(OIE, 2010). The Farm Animal Welfare Council (FAWC, 1993)
identies ve areas that address the animals physical and
mental well-being when considering welfare. These areas are
commonly referred to as the Five Freedoms (Table 1).
A more recent concept of animal welfare is based on
allostasis, or the ability to cope with stress (McEwen and
Wingeld, 2003; Korte et al., 2007). This concept argues that
the Five Freedoms are an unrealistic model for an animals
well-being because achieving all ve would essentially be a
state of utopia. Most animals would naturally experience
hunger, which stimulates their hunting/foraging behaviors.
Thus, achieving one thing would be in direct conict with
another.
In scientic terms, animal welfare refers to the actual and
current state of the animal (Keeling et al., 2011). The scientic
community seems to agree that welfare is a characteristic of
doi:10.1016/B978-0-444-52512-3.00204-7
387
388
Table 1
Freedom
Freedom
Freedom
Freedom
Freedom
Free access to freshwater and a diet to maintain full health and vigor
Providing a suitable environment, including shelter and a comfortable resting area
Prevention or rapid diagnosis and treatment
Providing sufcient space, proper facilities, and company of the animal's own kind
Ensuring conditions that avoid mental suffering
Source: Adapted from Webster, A.J.F., 2001. Farm animal welfare: The ve freedoms and the free market. Veterinary Journal 161, 229237.
Global Perspective
Attention to animal welfare varies considerably around the
world. Generally, the EU has the strongest laws and attention
to farm animal welfare among nations. However, individual
member countries in the EU have stronger animal welfare rules
than the EU as a whole. Some European countries that are not
a member of the EU such as Switzerland have strong farm
animal welfare laws. As a general rule in Western Europe, the
more Northern countries have stricter animal welfare laws
than more Southern European countries.
The United States and Canada have some farm animal
welfare laws and regulations. Most laws are related to humane
slaughter. Transportation of farm animals in the United States
must not exceed 28 h. Handling of animals in stockyards are
covered by the US Packers and Stockyard Act.
Within the United States, several states have laws to prevent
certain production practices. For example, Florida, Arizona,
and California have banned gestation crates for pregnant sows.
Some state initiatives have also banned cages for laying hens
and crates for veal calves.
Asia, Africa, and Latin America have few animal welfare
laws or regulations. They may impose international standards
(e.g., for the EU) if they export to countries that request for a
higher animal welfare standard.
Retail companies that sell animal products include grocery
stores, restaurants, and food service companies. Some retailers have animal welfare standards that impact production
practices, whereas some have specic requirements for production standards. A search of each retail companys website
often yields their animal welfare standards. The retailers often
drive change more quickly than through legislation. Activist
organizations have learned that pressure on retailers can lead
to changes more quickly than through legislation.
One critical question has arisen in recent years about global
standards for animal welfare. Most standards are minimum
requirements. Some people feel that an animal welfare
standard must accomplish a high level of animal welfare.
Standards vary around the world based on many factors, including target level (minimum through high); scientic interpretation; geography and unique production methods;
Farm Animals
One of the most common issues and concerns with standard
agriculture practices is the pain and distress it causes the animal. These practices are performed to improve the overall wellbeing of the animal, but may have both human and animal
implications. Scientists are continually researching improved
and more humane methods for standard agricultural procedures. The standard practices of the agriculture industry and
the regulations and requirements that must be followed for
their use in production and research are discussed immediately
below by species, and some recommendations are provided.
As stated in the Guide and the Care and Use of Agricultural
Animals in Research and Teaching, all basic biological needs
should always be met such as food, water, shelter, and even
comfort.
Cattle
Castration
Castration has multiple purposes in several male species, primarily to reduce aggression and therefore limit harm to
handlers and other animals, satisfy food quality regulations in
order to ensure a high-quality eating experience for consumers,
and to manage reproductive and genetic control. Several
methods of castration in cattle are acceptable in the Ag Guide,
for example, surgical or bloodless castration, rubber rings, and
tubing bands. When deciding on a method the animal's age
and weight should be accounted for, and performed before 2
or 3 months of age or below 230 kg (Farm Animal Welfare
Council, 1981) when the procedure is least stressful. At
weights greater than 230 kg, local and topical anesthetics
should be used to minimize pain.
Castration increases the cortisol response (Robertson et al.,
1994), substance-P concentrations (Coetzee et al., 2008),
haptoglobin concentrations (Ballou et al., 2013), and abnormal behaviors (Robertson et al., 1994; Currah et al., 2009),
whereas it suppresses leukocyte concentrations (Ballou et al.,
2013) in calves. The specic castration method used (surgical
or bloodless) can cause increased pain. The bloodless castration methods are associated with both acute and chronic
pain that can last up to 42 days (Molony et al., 1995; Ther
et al., 2007), and should only be used when surgical castration
is not appropriate for research protocols or when
postoperative complications are expected. All ages of castration cause acute pain, but cortisol concentrations were
greatest in calves surgically castrated at older ages (Robertson
et al., 1994).
Pain relief in the form of a local anesthetic and nonsteroid
antiinammatory drug (NSAID) increased appetite and reduced the cortisol response (Sutherland et al., 2013), and
prevented leukocytosis, neutrophilia, and leukocyte suppression (Ballou et al., 2013) in surgically castrated calves.
Administering local anesthesia before castration may reduce
acute pain; however, it does not eliminate it (Ther et al.,
2007).
389
Dehorning
Dehorning in cattle is performed to reduce injury to handlers
and animals, and reduce bruising of carcasses and damage to
hides. Injury to other animals caused by horns is especially
high during transportation. The United States currently does
not have any regulations for disbudding and dehorning, but
the AVMA (2013b) recommends disbudding as the preferred
dehorning method in calves with the use of local anesthetics
and NSAIDs at the earliest age practicable. Polled breeds
eliminate the need for dehorning and disbudding, and should
be used when possible.
Disbudding occurs with a heated disbudding iron or
chemical paste when the horn buds are 510 mm long, approximately 8 weeks of age (Stafford and Mellor, 2005). Amputation dehorning causes a greater cortisol response than
cautery or chemical disbudding with cautery having the lowest
response and the preferred technique (Stafford and Mellor,
2011). There are no differences in cortisol response between
the four different amputation dehorning methods: scoop,
guillotine shears, saw, or embryotomy wire (Sylvester et al.,
1998a), suggesting that all amputation methods of dehorning
are stressful in calves.
The cortisol response using a scoop method of dehorning
was elevated for 34 h postdehorning (Sylvester et al., 1998b)
or as long as 7 h (McMeekan et al., 1998a, 1998b). Local anesthetics reduce the peak cortisol response to scoop dehorning
but as soon as the drug wears off, concentrations increase as if
no local anesthetic had been applied. More than just local
anesthetic is needed for long-term pain from dehorning. Local
anesthetic maintains cortisol concentrations 5 h after dehorning, but then it remains elevated for up to 10 h after dehorning (Sutherland et al., 2002a; McMeekan et al., 1998b).
Local anesthetic plus cauterizing the wound (Sylvester et al.,
1998b; Sutherland et al., 2002b), administering a second
treatment of local anesthetics during the period of pain
(McMeekan et al., 1998a), or administering both the local
anesthetics and a NSAID (McMeekan et al., 1998b) will reduce
cortisol concentrations to levels comparable to controls.
However, the type of drugs used may not have the appropriate
mechanism of action to alleviate the pain caused from dehorning. The NSAID, ketoprofen, worked with local anesthetic,
but phenylbutazone did not reduce the cortisol response
(Sutherland et al., 2002a).
Abnormal or pain behaviors also increase after dehorning.
Head shaking and tail and ear icking increased after dehorning, but administration of a local anesthetic reduced those
behaviors, however, for only 2 h after dehorning (Sylvester
Identication
Several methods of identication are used in cattle: ear and tail
tags, ear notches, back tags, tattoos, electronic identication,
branding, and paint marks. Most of these forms of identication are not permanent and the type of identication should
be appropriate for the farm and research protocols. However,
permanent methods of identication should be used in order
to trace the origin of individual production animals in order to
protect the agriculture industry and public health (AVMA,
2013c). States in the United States have brand registries and
regulations related to branding, but only Montana, Nevada,
Oregon, and Idaho require hot-iron branding applied to cattle
imported from Canada and Mexico (AVMA, 2011).
The only two methods of permanent identication are hotiron and freeze branding. Hot-iron branding burns the skin to
leave a scar, whereas freeze branding kills pigment-producing
cells found in the hair follicles so that the hair is depigmented
when it grows back. Cattle that are hot-iron branded have a
greater cortisol response (Schwartzkopf-Genswein et al.,
1997a), high epinephrine concentrations (Lay Jr. et al., 1992a),
show more pain behaviors of tail-icks, kicks, falls, and vocalizations (Schwartzkopf-Genswein et al., 1997b, 1998), but
no differences in sensitivity to touch or in stress-induced analgesia are found between hot-iron and freeze branding
(Schwartzkopf-Genswein et al., 1997a). Hot-iron branding
causes greater distances and velocities of head movements and
forces on the headgate and chute (Schwartzkopf-Genswein
et al., 1998). Hot-iron branding also causes more tissue
damage than freeze branding, with freeze branding showing
more inammation through infrared thermography early after
branding and hot-iron having a prolonged inammatory response (Schwartzkopf-Genswein and Stookey, 1997). Dairy
calves, however, showed a different response with no differences in cortisol, epinephrine, and norepinephrine concentrations between hot-iron and freeze branding, but hot-iron
branded cows exhibited a greater escape avoidance reaction
and had increased heart rate (Lay Jr. et al., 1992b).
The physiological, behavioral, and inammatory responses
of cattle indicate that hot-iron branding causes more pain or
discomt than freeze branding, and therefore freeze branding
is the preferable branding technique regardless of breed.
However, other alternatives should be used for branding if
possible. No research has studied administered pain relief
during branding, but to minimize pain and discomfort this
should be considered.
390
Euthanasia
Humane methods to alleviate or eliminate pain and distress
that immediately results in unconsciousness should be carried
out during euthanasia. When animals are sick, injured, or
suffering for any reason that continued life is not a humane
option or is worse than death, then the owner or veterinarian
should euthanize the animal. This process is for the sake of the
animals welfare and quality of life. Acceptable methods of
euthanasia consistently result in a humane death by (1) direct
depression of neurons that are required for life, (2) hypoxia, or
(3) physical disruption of brain activity. The AVMA Guidelines
on Euthanasia (AVMA, 2013a) lists several methods of euthanasia appropriate for ruminants.
Several criteria have been listed by the AVMA for evaluating
humane euthanasia methods: (1) ability to induce loss of
consciousness and death with a minimum of pain and distress;
(2) time required to induce loss of consciousness; (3) reliability;
(4) safety of the personnel; (5) irreversibility; (6) compatibility
with intended animal use and purpose; (7) documented emotional effect on observers or operators; (8) compatibility with
subsequent evaluation, examination, or use of tissue; (9) drug
availability and human abuse potential; (10) compatibility with
species, age, and health status; (11) ability to maintain equipment in proper working order; (12) safety for predators or
scavengers should the animals remains be consumed; (13)
legal requirements; and (14) environmental impacts of the
method or disposition of the animal's remains.
The use of barbiturates is an acceptable method of euthanasia; however, large amounts of drug are required in larger
animals so cost may deter its use. Barbiturates must also be
administered by a person who is registered with the US Drug
Enforcement Agency and under veterinarian supervision.
Residues remain in the tissue and animals euthanized with
barbiturates; therefore any drug that leaves residues cannot be
used for human consumption unless approved by the US
Department of Food and Drug Administration. Physical
methods of euthanasia using gunshot or penetrating captive
bolt (see Figure 1) are most commonly used in cattle. Physical
methods disrupt and destroy the brain tissue. Additional
(a)
(b)
Figure 1 Anatomical landmarks for penetrating captive bolt or gunshot physical methods of euthanasia. The intersection of the dotted lines
indicated with a circle in the front view (a) is the proper point of entry. The side view (b) dotted line shows the trajectory through the brain.
Reproduced from Shearer, J.K., 2013. Humane Euthanasia of Sick, Injured and/or Debilitated Livestock. Ames, IA: Iowa State University. Available
at: http://vetmed.iastate.edu/HumaneEuthanasia (accessed 21.08.13).
391
Swine
Housing
Pigs are social animals and should be housed in groups in
production systems. Isolation has shown to increase cortisol
production and shift leukocyte percentages (Ruis et al., 2001)
in pigs. It is common to see group-housed growing pigs in
production, typically in groups of 230 pigs per pen, but
groups of hundreds and thousands are becoming more common (FASS, 2010). Mixing unfamiliar pigs does increase social
stress, which affects the physiology and immune system
(Morrow-Tesch et al., 1994). Fighting for dominance in larger
groups typically lasts 48 h (Meese and Ewbank, 1973) after
mixing, then once the hierarchy is established the group remains relatively stable. Hides (structures for animals to put
their head in) are one alternative to allow submissive pigs to
protect their heads and ears in order to escape aggressive attacks in order to improve their own well-being during mixing
392
Table 2
Score gait
Description
Behavioral criteria
1. Sound
2. Imperfect gait
3. Mildly lame
4. Moderately lame
5. Severely lame
Flat back
Steady head carriage
Hind hooves track up
Joints ex freely
Symmetrical gait
All legs bear weight equally
Flat or mildly arched back
Steady head carriage
Hind hooves do not track up perfectly
Joints slightly stiff
Slightly asymmetric gait
All legs bear weight equally
Arched back
Steady head carriage
Hind hooves do not track up
Joints show signs of stiffness
Asymmetric gait
Slight limb
Obvious arched back
Head bobs slightly
Hind hooves do not track up
Joints are stiff and strides are hesitant
Asymmetric gait
Reluctant to bear weight on hurt limb but still uses it
in locomotion
Extremely arched back
Obvious head bob
Poor tracking up with short strides
Obvious joint stiffness with no exion, hesitant and
deliberate strides
Asymmetric gait
Inability to bear weight on one or more limbs
Source: Adapted from Flower, F.C., Weary, D.M., 2006. Effect of hoof pathologies on subjective assessments of dairy cow gait. Journal of Dairy Science 89, 139146.
Castration
Pigs are castrated at an early age to reduce boar taint, a foul
smelling odor and avor in meat caused from androstenone
and skatole, reduce aggression toward other pigs and handlers,
and to control for unwanted pregnancies at market age. Castration causes acute pain-induced distress that can reduce
nursing and increase vocalizations and pain-like behaviors
making it an animal well-being concern (McGlone et al.,
1993). Painful production procedures without the use of
Table 3
393
Euthanasia method
Carbon dioxide
Gunshot
Penetrating captive bolt
Nonpenetrating captive bolt
Electrocution from head to heart
Electrocution in head only
Anesthetic overdose
Blunt trauma
Nursery pig
Growernisher pig
Mature pig
Up to 5.5 kg
Up to 32 kg
Up to market weight
Yes
No
No
Yes
Only for pigs 44.5 kg
Only for pigs 44.5 kg
Yes
Yes
Yes
Yes
Yes
Yes with secondary step
Yes
Yes with secondary step
Yes
No
Source: Adapted from National Pork Board, 2008. On-farm Euthanasia of Swine: Recommendations for Producers. Des Moines, IA: National Pork Board.
Euthanasia
There are six acceptable methods of euthanasia for pigs of
different ages and sizes in On-Farm Euthanasia of Swine
Recommendations for the producer developed by the
National Pork Board and American Association of Swine
Veterinarians. When a pig is ill or injured a decision based on
the best interest of the well-being of the animal should be
made for treatment or euthanasia. Euthanasia may be best if
the pig has not improved after 2 days of intensive care, it is
severely injured or nonambulatory with the inability to
Sheep/Goats
Herd management
Welfare strategies concerning sheep and goats are focused on
the typical topics: housing, nutrition, health, and mental wellbeing. Personnel giving daily care to animals should be familiar with sheep and goat behavior, signs of illness as well as
potential health treatments so that they can prevent injury and
disease. Sheep and goats should be fed to maintain a body
condition score (BCS) of at least a 1.5 on a 15 point scale
(FASS, 2010). Sheep are particularly sensitive to copper (Cu)
toxicity, and therefore, copper should be considered when
formulating diets with special consideration to the Cu concentration in available forages. Care should be taken to prevent Johnes disease (paratuberculosis), which can be
transmitted from infected ewes on supplementing with raw
colostrum from an infected ewe.
Shearing can be stressful as it can not only induce fear by
restraint and handling but also from the heat and noise of the
shears. In addition, sheep may acquire lacerations during the
shearing process; thus, it is suggested that shearing should only
be done by trained professionals. Time of shearing should be
taken into account and sheep should have access to shelter
from severe weather and environmental conditions (freezing
temperatures, cold rain, extreme wind, or sun without shade)
after shearing if needed. Shearing ewes before lambing can
increase birth weights of lambs (Kenyon et al., 2006a,b).
Newborn lambs may nd it easier to nurse without obstruction when ewes are sheared. If management or weather
prevents the shearing of ewes, a common practice of removing
wool from the dock and udder (crutching) can be done.
Mulesing is a procedure developed to reduce the incidence
of y strike on particularly wrinkled skin breeds of sheep such
as the Merino breed. This procedure involves removing excess
skin to prevent ies from laying eggs in soiled folds of skin.
However, the procedure is considered painful and is highly
criticized. Thus, mulesing is no longer practiced in most
countries.
394
Behavior
Sheep and goats are very herd oriented. When handling, performing routine herd maintenance and when transporting,
animals should be kept in groups to prevent injury to animals
and humans by sheep and goats attempting to escape or regroup with the herd. Sheep and goats are trainable to load and
can be handled in restraint devices such as a squeeze chute
table (Grandin, 1989), head stanchions (Sheldon et al., 2006),
manual methods (Battaglia, 1998), and the Panepinto sling
(FASS, 2010).
Euthanasia
As in cattle, barbiturates, gunshot, and captive bolt are approved methods of euthanasia followed by exsanguinations,
or administration of potassium chloride or magnesium sulfate
to ensure death. Electrocution may also be used as a method
of euthanasia but restraint and proper placement of the electrodes make electrocution an unlikely option for research and
eld use (AVMA, 2013a).
Poultry
Housing
There are several housing systems available for poultry: conventional and furnished cages, aviaries, littered oors, and free
range. Regardless of the housing system it should allow for the
cleaning of equipment and inspection of the birds without
handling them, although the birds should be easily accessible
(FASS, 2010). No system is stress free. Hens in oor housing
have social hierarchies and cannibalistic pecking is a serious
welfare concern. In caged hens this seems to be more prominent in extreme crowding when feeding competition is a
problem, and in noncaged systems because of the larger group
sizes. If group size is too large, hens display escape and fear
behaviors (Craig and Adams, 1984).
Systems with similar characteristics have similar welfare
problems (Lay Jr. et al., 2011). Conventional cages do not
meet behavioral needs of nesting, perching, and dust bathing,
Forced molting
Natural molting replaces the plumage after sexual maturity in
poultry. During this time egg production is paused and can be
out of sync with the ock, so commercial production operations force molt in order to synchronize molting, rejuvenate
the ock, and extend production by 2 or 3 laying cycles (FASS,
2010). Forced molting is done by reducing day length and
withdrawing feed and water from laying hens.
Forced molting increases eosinophils, total white blood
cells, monocytes, and packed cell volume (Brake et al., 1982).
It also decreases liver, ovary, oviduct, and body weights (Brake
and Thaxton, 1979). However, greater amounts of weight loss
is associated with more eggs, egg weight, specic gravity, and
shell weights (Baker et al., 1983), and nonmolted hens perform poorly in egg quality and production (Zimmermann and
Andrews, 1987; Lee, 1982). The practice of forced molting not
only benets the industry by increasing egg production and
quality but also reduces the number of male chicks and hens
euthanized annually and rejuvenates feathers improving
thermoregulation in hens (FASS, 2010).
Beak trimming
Beak trimming is performed in poultry production to reduce
cannibalism, aggressive behaviors, and feather pecking (for
review see: Cunningham, 1997). This is an economic advantage for the producer, but a welfare concern for the animal. The
sensory receptors are cut from the tip of the beak, and sensory
395
396
Blind spot
A
60
45
Handler position
to stop movement
B
Handler position
to start movement
90
Point of
balance
Figure 2 Flight zone showing how to effectively move an animal. Adapted from Figure 1 in FASS, 2010. Chapter 5: Animal handling and
transport. In: Guide for the Care and Use of Agricultural Animals in Research and Teaching, third ed., p. 46. Champaign, IL: Federation of Animal
Science Societies. Available at: http://www.fass.org/page.asp?pageID=216 (accessed 15.01.14).
(a)
(b)
(c)
(d)
Figure 3 Livestock handling and sorting equipment: (a) rattle paddle, (b) ag, (c) electric prod, and (d) sort board/panel. Products (a) and (b) are
provided by Koehn Marketing, Inc. and products (c) and (d) are distributed by QC Supply.
Table 4
Minimum space allowances during transportation for
different livestock species
397
Table 5
Recommended minimum space requirements for grouphoused small animals (ILAR, 2011)
Species
Weight (kg)
Space (m2)
Animal
Weight (g)
Height (cm)
Cattle
273
545
5
23
113
27
55
113227
0.80
1.40
0.06
0.14
0.40
0.20
0.30
1.75
1.40
Mice
o10
Up to 15
Up to 25
425
38.7
51.6
77.4
Z96.7
330
109.6
148.35
187.05
258
387
Z451.5
800
64.5
83.8
103.2
Z122.5
387
Z651.5
12.7
12.7
12.7
12.7
12.7
17.8
17.8
17.8
17.8
17.8
17.8
17.8
15.2
15.2
15.2
15.2
17.8
17.8
Swine
Sheep
Horses
Foals
Source: Adapted from FASS, 2010. Guide for the Care and Use of Agricultural Animals
in Research and Teaching, third rev. ed. Champaign, IL: Federation of Animal Science
Societies and National Pork Board, 2008. Transport Quality Assurance (TQA)
Handbook. Des Moines, IA: National Pork Board.
Humane Slaughter
Animals must be killed (also called slaughtering or harvesting)
and the carcass processed before human consumption. Animals have been killed for human food since animals were rst
domesticated more than 10 000 years ago. The method of
slaughter in the European and American custom is meant to be
humane. EU requires that food animals be killed in a way
that avoids unnecessary suffering. The US legislation that
governs animal harvest is the Humane Methods of Slaughter
Act of 1958; referred to as the Humane Slaughter Act or HSA).
The HSA requires that animals are rendered rapidly insensible
before being shackled or cut.
Another method of slaughter is ritual slaughter for Jewish
and Muslim faiths. In ritual slaughter, the animal is not rendered insensible before being shackled or cut. Ritual slaughter
is considered not humane by some people, but is required by
the customs of people of certain religions, and therefore is
acceptable.
Transport and handling before stun and exsanguination is
also the subject of animal welfare concern. Extensive guidelines are provided by Temple Grandin, the AMI, and others.
Guinea pigs
o100
Up to 200
Up to 300
Up to 400
Up to 500
4500
o 60
Up to 80
Up to 100
4100
Up to 350
4350
Table 6
Recommended minimum space requirements for grouphoused larger animals (ILAR, 2011)
Animal
Weight (kg)
Height (cm)
Rabbits
o2
Up to 400
Up to 5.4
45.4
r4
44
o15
Up to 300
430
0.14
0.28
0.37
Z0.46
0.28
Z0.37
0.74
1.2
Z2.4
0.07
0.023
40.5
40.5
40.5
40.5
60.8
60.8
Sufcient to stand
with feet on oor
1.5
3
10
15
20
25
30
0.2
0.28
0.4
0.56
0.74
0.93
1.4
Z2.32
76.2
76.2
76.2
81.3
91.4
116.8
116.8
152.4
10
1.4
Z2.32
152.4
213.4
Cats
Dogs
Pigeons
Quail
Monkeys
Group 1
Up to
Group 2
Up to
Group 3
Up to
Group 4
Up to
Group 5
Up to
Group 6
Up to
Group 7
Up to
Group 8
430
Chimpanzees
Juveniles Up to
Adults
410
Sufcient to stand
with feet on oor
Laboratory Animals
Laboratory animals used for research and teaching should be
housed with adequate space (Tables 5 and 6) and resources
that meet their physiological and behavioral needs (ILAR,
2011). Social animals should be housed in pairs or groups that
allow for social interaction unless the research protocol does
not allow for social contact. Environmental enrichment should
398
Wildlife
Wildlife mammalian research involves the collection of
mammals in the eld in order for scientists to understand
community and population dynamics, genetics, anatomy and
physiology, ecology and diseases (ASM, 1987). Kill traps
should have low probability of capturing nontarget animals
and kill the animal quickly. Live traps should keep the animal
alive and uninjured. Live trapping may be painful or distressful to the animal especially when trying to escape, so
padded traps may be more humane (Bekoff, 1995). Pitfalls can
be used for both live and dead captures, but should have
enough food to sustain the animal until the next trap check or
enough liquid to drown the animal quickly. Humane methods
should be used during euthanasia. Gases (carbon dioxide and
ether), thoracic compression or cervical dislocation, and
shooting if it causes instantaneous death are approved methods that should be used when appropriate for the animal.
Taking samples of tissue should be in a way to minimize
pain. If it is a short procedure anesthetics may not be used in
order to release the animal quickly, but longer more painful
procedures should end in euthanasia of the animal. Marking
the animal for reidentication should be done with minimal
pain and should not restrict the natural movements of the
animal, and should be suitable for the length of the study.
When using amphibians and reptiles in research, care must
be given to the unique husbandry practices. Thermoregulation
is difcult to satisfy because heat uptake and loss is from the
environment, and light intensity must match the temperature
of the environment. Shallow water containers or daily spraying
and hiding places are appropriate for their habitats (Pough,
1992).
Horse Shows
Horses exhibited in a public display, in competition, except
events where speed is the prime factor, such as rodeo events,
parades, and organized trail rides are regulated by APHIS
under the Horse Protection Act (HPA) of 1970. The HPA is
focused on the Tennessee Walking Horse industry to prevent
the practice of soring, which is stimulating a horse to step
higher by intentionally rendering a horse unsound by physical
or chemical means. Even though the HPA focuses on soring, it
could be applied, or easily amended to include other aspects
of the equine industry. It has been proposed to amend the
HPA to include the transport of horses for the purpose of
slaughter illegal. Larger horse show organizations have implemented their own animal welfare statues as proactive
measures in support of the human treatment of horses.
Regulations include the testing for controlled substances,
altering tail function to minimize tail swishing, appropriate
footing, and checkpoints for endurance horses. There are also
many tack and equipment rules and regulations among show
associations. In 2012, the American Quarter Horse Association
received its rst report from its newly formed Animal Welfare
399
Commission with regard to identify issues that negatively affect the welfare of horses as well as recommendations to dene
and prevent inhumane treatment of horses.
References
Appleby, M.C., Smith, S.F., Hughes, B.O., 1993. Nesting, dust bathing and perching
by laying hens in cages: Effects of design on behavior and welfare. British
Poultry Science 34, 835847.
ASIA (American Sheep Industry Association), 2002. Sheep Production Handbook.
Fort Collins, CO: ADS/Nightwing Publishing.
ASM (American Society of Mammalogists), 1987. Acceptable eld methods in
mammaology: Preliminary guidelines approved by the American Society of
Mammologists. Journal of Mammalogy 68 (Suppl.), 118.
AVMA, 2005. Pregnant sow housing. www.avma.org/issues/policy/animal_welfare/
pregnant_sow_housing.asp (accessed 14.08.13).
AVMA, 2010. Brochure: Welfare implications of beak trimming. Available at:
https://www.avma.org/KB/Policies/Pages/Beak-Trimming.aspx (accessed
09.08.13)
AVMA, 2011. Brochure: Welfare Implications of hot-iron branding and its
alternatives. Available at: https://www.avma.org/KB/Resources/Backgrounders/
Documents/hot-iron_branding_bgnd.pdf (accessed 06.08.13)
AVMA, 2013a. Guidelines for the euthanasia of animals: 2013 edition. Available at:
https://www.avma.org/KB/Policies/Pages/Euthanasia-Guidelines.aspx (accessed
06.08.13)
AVMA, 2013b. Policy: Castration and dehorning of cattle. Available at: https://www.
avma.org/KB/Policies/Pages/Castration-and-Dehorning-of-Cattle.aspx (accessed
05.08.13)
AVMA, 2013c. Policy: Livestock identication. Available at: https://www.avma.org/
KB/Policies/Pages/AVMA-Position-on-Livestock-Identication.aspx (accessed
06.08.13)
AVMA, 2013d. Policy: Tail docking of cattle. Available at: https://www.avma.org/KB/
Policies/Pages/Tail-Docking-of-Cattle.aspx (accessed 07.08.13)
AVMA, 2013e. Policies: Beak trimming. Available at: https://www.avma.org/KB/
Policies/Pages/Beak-Trimming.aspx (accessed 09.08.13)
AZA, 2013. Association of zoos and aquariums accreditation standards and policies.
Available at: http://www.aza.org/uploadedFiles/Accreditation/AZA-AccreditationStandards.pdf (accessed 05.08.13)
Baker, M., Brake, J., McDaniel, G.R., 1983. The relationship between body weight
loss during an induced molt and postmolt egg production, egg weight, and shell
quality in caged layers. Poultry Science 62, 409413.
Ballou, M.A., Sutherland, M.A., Brooks, T.A., et al., 2013. Administration of
anesthetic and analgesic prevent the suppression of many leukocyte responses
following surgical castration and physical dehorning. Veterinary Immunology and
Immunopathology 151, 285293.
400
McGlone, J.J., 2001. Farm animal welfare in the context of other society issues:
Toward sustainable systems. Livestock Production Science 72, 7581.
McGlone, J.J., 2013a. Review: Updated scientic evidence on the welfare of
gestation sows kept in different housing systems. Professional Animal Scientist
29, 189198.
McGlone, J.J., 2013b. The future of pork production in the world: Towards
sustainable, welfare-positive systems. Animals 3 (2), 401415.
McGlone, J.J., von Borell, E.H., Deen, J., et al., 2004. Compilation of the scientic
literature comparing housing systems for gestating sows and gilts using
measures of physiology, behavior, performance and health. Professional Animal
Scientist 20, 105117.
McGlone, J.J., Curtis, S.E., 1985. Behavior and performance of weanling pigs in
pens equipped with hide areas. Journal of Animal Science 60, 2024.
McGlone, J.J., Nicholson, R.I., Hellman, J.M., Herzog, D.N., 1993. The development
of pain in young pigs associated with castration and attempts to prevent
castration induced behavioral changes. Journal of Animal Science 71,
14411446.
McMeekan, C.M., Mellor, D.J., Stafford, K.J., et al., 1998a. Effects of local
anaesthesia of 4 to 8 h' duration on the acute cortisol response to scoop
dehorning in calves. Australian Veterinary Journal 76, 281285.
McMeekan, C.M., Stafford, K.J., Mellor, D.J., et al., 1998b. Effects of regional
analgesia and or a non-steroidal anti-inammatory analgesic on the acute
cortisol response to dehorning in calves. Research in Veterinary Science 64,
147150.
Meese, G.B., Ewbank, R., 1973. The establishment and nature of the dominance
hierarchy in the domesticated pig. Animal Behaviour 21, 326334.
Moberg, G.P., 2000. Biological response to stress: Implications for animal welfare.
In: Moberg, G.P., Mench, J.A. (Eds.), The Biology of Animal Stress Basic
Principles and Implications for Animal Welfare. New York: CABI Publishing,
pp. 121.
Molony, V., Kent, J.E., 1997. Assessment of acute pain in farm animals using
behavioral and physiological measurements. Journal of Animal Science 75,
266272.
Molony, V., Kent, J.E., Robertson, I.S., 1995. Assessment of acute and chronic pain
after different methods of castration of calves. Applied Animal Behaviour Science
46, 3348.
Morrow-Tesch, J.L., McGlone, J.J., Salak-Johnson, J.L., 1994. Heat and social
stress effects on pig immune measures. Journal of Animal Science 72,
25992609.
National Pork Board, 2008. Transport Quality Assurance (TQA) Handbook. Des
Moines, Iowa: National Pork Board.
NRC, 1994. Nutrient Requirements of Poultry. Washington, DC: National Academies
Press.
NRC, 1996. Nutrient Requirements of Beef Cattle, seventh rev. ed. Washington, DC:
National Academies Press.
NRC, 1998. Nutrient Requirements of Pigs, tenth rev. ed. Washington, DC: National
Academies Press.
NRC, 2001. Nutrient Requirements of Dairy Cattle, sixth rev. ed. Washington, DC:
National Academies Press.
NRC, 2007a. Nutrient Requirements of Small Ruminants: Sheep, goats, cervids, and
New World camelids. Washington, DC: National Academies Press.
NRC, 2007b. Nutrient Requirements of Horses, sixth rev. ed. Washington, DC:
National Academies Press.
O'Callaghan, K., 2002. Lameness and associated pain in cattle Challenging
traditional perceptions. In Practice 24, 212219.
OIE, 2010. Terrestrial Animal Health Code. Available at: http://www.oie.int/en/
international-standard-setting/terrestrial-code/access-online/ (accessed 08.08.13).
Petrie, N.J., Mellor, D.J., Stafford, K.J., Bruce, R.A., Ward, R.N., 1996. Cortisol
responses of claves to two methods of tail docking used with or without local
anaesthetic. New Zealand Veterinary Journal 44, 48.
Phillips, P.A., Fraswer, D., Thompson, B.K., 1991. Preference by sows for a partially
enclosed farrowing crate. Applied Animal Behaviour Science 32, 3543.
Pough, F.H., 1992. Setting guidelines for the care of reptiles, amphibians and shes.
In: Schaeffer, D.O., Kleinow, K.M., Krulisch, L. (Eds.), The Care and Use of
Amphibians, Reptiles and Fish in Research., pp. 714.
Rhodes, T.R, Appleby, M.C., Chinn, K., et al., 2005. A comprehensive review of
housing for pregnant sows. Journal of the American Veterinary Medical
Association 227 (10), 15801590.
Robertson, I.A., Kent, J.E., Malony, V., 1994. Effect of different methods of castration
on behavior and plasma cortisol in calves of three ages. Research in Veterinary
Science 56, 817.
Ross, C.V., 1989. Sheep Production and Management. Englewood Cliffs, NJ:
Prentince-Hall.
401
Ruis, M.A.W., te Brake, J.H.A., Engel, B., et al., 2001. Adapation to social isolation
acute and long-term stress responses of growing gilts with different coping
characteristics. Physiology & Behavior 73, 541551.
Schreiner, D.A., Ruegg, P.L., 2002a. Responses to tail docking in calves and heifers.
Journal of Dairy Science 85, 32873296.
Schreiner, D.A., Ruegg, P.L., 2002b. Effects of tail docking on milk quality and cow
cleanliness. Journal of Dairy Science 85, 25032511.
Schwartzkopf-Genswein, K.S., Stookey, J.M., 1997. The use of infrared thermography
to assess inammation associated with hot-iron and freeze branding in cattle.
Canadian Journal of Animal Science 77, 577583.
Schwartzkopf-Genswein, K.S., Stookey, J.M., Crowe, T.G., Genswein, B.M.A., 1998.
Comparison of image analysis, exertion force and behavior measurements for use
in the assessment of beff cattle responses to hot-iron and freeze branding.
Journal of Animal Science 76, 972979.
Schwartzkopf-Genswein, K.S., Stookey, J.M., de Passille, A.M., Rushen, J., 1997a.
Comparison of hot-iron and freeze branding on cortisol levels and pain
sensitivity in beef cattle. Canadian Journal of Animal Science 77, 369374.
Schwartzkopf-Genswein, K.S., Stookey, J.M., Welford, R., 1997b. Behavior of cattle
during hot-iron and freeze branding and the effects on subsequent handling ease.
Journal of Animal Science 75, 20642072.
Sheldon, C.C., Sonsthagen, T., Topel, J.A., 2006. Animal Restraint for Veterinary
Professionals. St. Louis, MO: Mosby.
Smith, B., Wickersham, T., Miller, K., 1983. Beginning Shepherd's Manual. Ames,
IA: Iowa State University Press.
Sprecher, D.J., Hostetler, D.E., Kaneene, J.B., 1997. A lameness scoring system that
uses posture and gait to predict dairy cattle reproductive performance.
Theriogenology 47, 11791187.
Stafford, K.J., Mellor, D.J., 2005. Dehorning and disbudding distress and its
alleviation in calves. Veterinary Journal 169, 337349.
Stafford, K.J., Mellor, D.J., 2011. Addressing the pain associated with
disbudding and dehorning in cattle. Applied Animal Behaviour Science 135,
226231.
Stull, C.L., Payne, M.A., Berry, S.L., Hullinger, P.J., 2002. Evaluation of the
scientic justication for tail docking in dairy cattle. Journal of the American
Veterinary Medical Association 220, 12981303.
Sutherland, M.A., Ballou, M.A., Davis, B.L., Brooks, T.A., 2013. Effect of castration
and dehorning singularly and combined on the behavior and physiology of
Holstein calves. Journal of Animal Science 91, 935942.
Sutherland, M.A., Davis, B.L., Brooks, T.A., Coetzee, J.F., 2012. The physiological
and behavioral response of pigs castrated with and without anesthesia and
analgesia. Journal of Animal Science 90, 22112221.
Sutherland, M.A., Davis, B.L., Brooks, T.A., McGlone, J.J., 2010. Physiology and
behavior of pigs before and after castration: Effects of two topical anesthetics.
Animal 4, 20712079.
Sutherland, M.A., Mellor, D.J., Stafford, K.J., et al., 2002a. Cortisol responses to
dehorning of calves given a 5-h local anaestetic regimen plus phenylbutazone,
ketoprofen, or adrenocorticotropic hormone prior to dehorning. Research in
Veterinary Science 73, 115123.
Sutherland, M.A., Mellor, D.J., Stafford, K.J., et al., 2002b. Effect of local anesthetic
combined with wound cauterization on the cortisol response to dehorning in
calves. Australian Veterinary Journal 80, 165168.
Sutherland, M.A., Mellor, D.J., Stafford, K.J., et al., 1999. Acute cortisol responses
of lambs to ring castration and docking after the injection of lignocaine into the
scrotal neck or testes at the time of ring application. Australian Veterinary
Journal 77, 738741.
Sylvester, S.P., Mellor, D.J., Stafford, K.J., Bruce, R.A., Ward, R.N., 1998b. Acute
cortisol responses of calves to scoop dehorning using local anesthesia and/or
cautery of the wound. Australian Veterinary Journal 76, 118122.
Sylvester, S.P., Stafford, K.J., Mellor, D.J., Bruce, R.A., Ward, R.N., 2004. Behavioral
responses of calves to amputation dehorning with and without local anesthesia.
Australian Veterinary Journal 82, 697700.
Sylvester, S.P., Stafford, K.J., Mellor, D.J., Bruice, R.A., Ward, R.N., 1998a. Acute
cortisol responses of calves to four methods of dehorning by amputation.
Australian Veterinary Journal 76, 123126.
Tactacan, G.B., Guenter, W., Lewis, N.J., Rodriguez-Lecompte, J.C., House, J.D.,
2009. Performance and welfare of laying hens in conventional and enriched
cages. Poultry Science 88, 698707.
Ther, S., Mellema, S., Doherr, M.G., et al., 2007. Effect of local anesthesia on
short- and long-term pain induced by two bloodless castration methods in
calves. Veterinary Journal 173, 333342.
Thomas, D.L., Waldron, D.F., Morrical, G.D., et al., 2003. Length of docked tail and
the incidence of rectal prolapse in lambs. Journal of Animal Science 81,
27252732.
402
Tom, E.M., Rushen, J., Duncan, I.J.H., de Passille, A.M., 2002. Behavioral, health
and cortisol responses of young calves to tail docking using a rubber ring or
docking iron. Canadian Journal of Animal Science 82, 19.
US Code: 49 USC Sec. 80502, 2012. Transportation of animals. Available at: http://
uscode.house.gov (accessed 09.08.13)
US Code: 21 USC 601, 2012. Humane Methods of Livestock Slaughter Act.
Available at: http://uscode.house.gov (accessed 09.08.13)
Van Den Brand, H., Parmentier, H.K., Kemp, B., 2004. Effects of housing system
(outdoor vs. cages) and age of laying hens on egg characteristics. British Poultry
Science 45, 745752.
Webster, A.B., 2004. Welfare implications of avian osteoporosis. Poultry Science 83,
184192.
Whay, H.R., Waterman, A.E., Webster, A.J.F., 1997. Associations between
locomotion, claw lesions and nociceptive threshold in dairy heifers during the
peri-partum period. Veterinary Journal 154, 155161.
Whay, H.R., Waterman, A.E., Webster, A.J.F., O'Brien, J.K., 1998. The inuence of
lesion type on the duration of hyperalgesia associated with hindlimb lameness in
dairy cattle. Veterinary Journal 156, 2329.
Wood, G.N., Molony, B., Fleetwood-Walker, S.M., Hodgson, J.C., Mellor, D.J.,
1991. Effects of local anesthesia and intravenous naloxone on the changes in
behavior and plasma concentrations of cortisol produced by castration and tail
docking with tight rubber rings in young lambs. Research in Veterinary Science
51, 193199.
Zamaratskaia, G., Rydhmer, L., Andersson, H.K., et al., 2008. Long-term effect of
vaccination against gonadotropin-releasing hormone, using Improvac, on
hormonal prole and behavior of male pigs. Animal Reproduction 108, 3747.
Zimmermann, N.G., Andrews, D.K., 1987. Comparison of several induced molting
methods on subsequent performance of single comb White Leghorn hens.
Poultry Science 66, 408417.
Relevant Websites
http://www.fass.org/docs/agguide3rd/Ag_Guide_3rd_ed.pdf
Ag Guide.
http://www.agcouncil.com/
American Greyhound Council.
http://www.horsecouncil.org/WelfareCode.php
American Horse Council.
http://www.apha.com/programs/showing/animal-welfare
American Paint Horse Association.
http://www.aqha.com/Resources/Handbook/Policy-Statement.aspx
American Quarter Horse Association Welfare Policy.
http://awic.nal.usda.gov/
Animal Welfare Information Center.
http://www.aza.org/uploadedFiles/Accreditation/AZA-Accreditation-Standards.pdf
Association of Zoos and Aquariums Accreditation Standards and Policies.
https://www.avma.org/KB/Policies/Pages/Euthanasia-Guidelines.aspx?
utm_source=prettyurl&utm_medium=web&utm_campaign=redirect&utm_
keyword=issue-animal_welfare-euthanasia-pdf
AVMA Guidelines for the Euthanasia of Animals.
https://www.gov.uk/government/policies/protecting-animal-welfare
Defra/UK Policies for Animal Welfare.
http://www.fws.gov/endangered/laws-policies/
Endangerd Species Act.
http://www.fao.org/ag/againfo/themes/en/animal_health.html
FAO Animal Health.
http://www.fass.org/page.asp?pageID=216&autotry=true&ULnotkn=true
FASS Guidelines (Ag Guide).
http://www.fei.org/
Federation Equestrian International.
http://www.mammalogy.org/uploads/Sikes%20et%20al%202011.pdf
http://www.depts.ttu.edu/animalwelfare/Research/Transport/28hourslaw.php
28-hour Law.
http://www.aphis.usda.gov/animal_welfare/hp/hp_act_regs.shtml
Horse Protection Act.
http://khrc.ky.gov/Pages/default.aspx
Kentucky Racing Commission.
http://www.aphis.usda.gov/animal_welfare/policy.php USDA/APHIS Animal Care
Policy Manual.
http://www.prorodeo.com/pdfs/AnimalWelfare.pdf
PRCA/Rodeo.
http://arcicom.businesscatalyst.com/
Racing Commissioners International.
http://www.daff.gov.au/__data/assets/pdf_le/0006/1935591/review-aaws.pdf
The Australian Animal Welfare Strategy: Australian Veterinary Association:
Patient.
http://www.animallaw.info/statutes/stusfd7usca1901.htm
The Humane Methods of Slaughter Act.
http://www.collegerodeo.com/rulebook.asp
The NIRA.
http://www.prorodeo.com/
The PRCA.
http://awic.nal.usda.gov/farm-animals/livestock-species
USDA Farm Animal Welfare Information Center.
http://awic.nal.usda.gov/government-and-professional-resources/state-and-local-laws
USDA State and Local Laws.
http://www.usef.org/_IFrames/RuleBook/rules.aspx
US Equestrian Federation.
http://www.daff.gov.au/animal-plant-health/welfare/
model_code_of_practice_for_the_welfare_of_animals
Welfare Codes in AU.
http://ec.europa.eu/food/animal/welfare/index_en.htm
http://ec.europa.eu/food/animal/welfare/slaughter/slaughter_directive_en.htm
http://www.aasv.org/aasv/documents/SwineEuthanasia.pdf
www.animalhandling.org
http://www.animallaw.info/statutes/stusfd7usca1901.htm
http://www.depts.ttu.edu/animalwelfare/Research/Transport/index.php#7
www.grandin.com
Asian Aquaculture
F Corsin, IDH, The Sustainable Trade Initiative, Hanoi, Vietnam
K Yamamoto, University of Stirling, Stirling, UK
r 2014 Elsevier Inc. All rights reserved.
Glossary
Aquaculture The farming of aquatic organisms, including
sh, mollusks, crustaceans, and aquatic plants, with some
sort of intervention in the rearing process to enhance
production, such as regular stocking, feeding, protection
from predators, etc. Farming also implies individual or
corporate ownership of the stock being cultivated.
Domesticated In a broader sense, animals selected from
the wild adapt to a special habitat created for them by
humans, bringing a wild species under human
management. In a genetic context, process in which changes
in gene frequencies and performance arise from a new set of
selection pressures exerted on a population.
Feed conversion ratio (FCR) Ratio between the dry
weight of feed fed and the weight of yield gain. It is the
measure of the efciency of conversion of feed to sh (e.g.,
FCR 2.8 means that 2.8 kg of feed is needed to produce
1 kg of sh live weight).
Food and Agriculture Organization (FAO) An agency of
the United Nations that leads international efforts to raise
doi:10.1016/B978-0-444-52512-3.00133-9
403
404
Asian Aquaculture
100
Poultry meat
80
Cattle meat
60
40
20
0
1960
1970
1980
1990
2000
2010
Figure 1 Global production of cattle meat, poultry, and food sh from aquaculture between 1961 and 2011. Reproduced from FAO, 2013a.
Aquaculture and Capture Production 19502011. Rome: Statistics and Information Service of the Fisheries and Aquaculture Department; FAO,
2013b. Cultured Aquatic Species Information Programme: Pangasius hypophthalmus (Sauvage, 1878). Available at: http://www.fao.org/shery/
culturedspecies/Pangasius_hypophthalmus/en (accessed 08.04.14); and FAO, 2013c. FAOSTATS. Available at: http://faostat.fao.org/site/291/default.
aspx (accessed 08.04.14).
Capture fisheries
1970
1990
100
90
80
70
60
50
40
30
20
10
0
1950
1960
1980
2000
2010
Figure 2 World capture sheries and aquaculture food sh production during 19502011. Reproduced from FAO, 2013a. Aquaculture and
Capture Production 19502011. Rome: Statistics and Information Service of the Fisheries and Aquaculture Department; FAO, 2013b. Cultured
Aquatic Species Information Programme: Pangasius hypophthalmus (Sauvage, 1878). Available at: http://www.fao.org/shery/culturedspecies/
Pangasius_hypophthalmus/en (accessed 08.04.14); and FAO, 2013c. FAOSTATS. Available at: http://faostat.fao.org/site/291/default.aspx (accessed
08.04.14).
Asian Aquaculture
Table 1
Annual average rate of growth for food production
between 1961 and 2011
Cattle
Poultry
27.69
8.95
1.52
62.54
101.74
62.70
1.64%
Aquaculture
4.98%
405
7.72%
Source: Reproduced from FAO, 2013a. Aquaculture and Capture Production 1950
2011. Rome: Statistics and Information Service of the Fisheries and Aquaculture
Department; FAO, 2013b. Cultured Aquatic Species Information Programme: Pangasius
hypophthalmus (Sauvage, 1878). Available at: http://www.fao.org/shery/
culturedspecies/Pangasius_hypophthalmus/en (accessed 08.04.14); and FAO, 2013c.
FAOSTATS. Available at: http://faostat.fao.org/site/291/default.aspx (accessed
08.04.14).
China
Rest of Asia
Rest of the World (Africa, Europe, Americas, Middle East, and Oceania)
million metric tons
140
120
100
80
60
40
20
2009
2007
2005
2003
2001
1999
1997
1995
1993
1991
1989
1987
1985
1983
1981
1979
1977
1975
1973
1971
1969
1967
1965
1963
1961
Figure 3 Apparent sh consumption (million metric tons). Reproduced from FAO Food Balance Sheet. Available at: http://faostat3.fao.org/faostatgateway/go/to/download/FB/*/E (accessed 08.04.14).
406
Asian Aquaculture
02 kg year1
25 kg year1
510 kg year1
1020 kg year1
2030 kg year1
3060 kg year1
> 60 kg year1
Figure 4 Fish as food: per capita supply (average 200709). Reproduced from FAO, 2012. The State of World Fisheries and Aquaculture. Rome: FAO.
Table 2
Number of aquaculture species and number of those
aquaculture species that have been domesticated
Phylum
Aquacultured
Finsh
Mollusks
Crustaceans
Seaweed
227
77
35
420
91
30
19
6
40
39
54
30
359
136
37
Total
Domesticated
Domestication (%)
Source: Reproduced from Benzie, J.A.H., Nguyen, T.T.T., Hulata, G., et al., 2012.
Promoting responsible use and conservation of aquatic biodiversity for sustainable
aquaculture development. In: Subasinghe, R.P., Arthur, J.R., Bartley, D.M., et al. (Eds.),
Farming the Waters for People and Food. Proceedings of the Global Conference on
Aquaculture 2010, Phuket, Thailand, 2225 September 2010, pp. 337383. Rome:
FAO and Bangkok: NACA.
Table 3
Protein content of major animal foods and feed conversion efciencies for their production
Commodity
Milk
Carp
Eggs
Chicken
Pork
Beef
0.7
0.7
3.5
40
1.5
2.3
18
30
3.8
4.2
13
30
2.3
4.2
20
25
5.9
10.7
14
13
12.7
31.7
15
5
Source: Reproduced from Hall, S.J., Delaporte, A., Phillips, M.J., 2011. Blue Frontiers: Managing the Environmental Costs of Aquaculture. Penang, Malaysia: The WorldFish Center.
Asian Aquaculture
Continents
Production in 2011
(million metric tons)
Africa
Americas
Asia
Europe
Oceania
1.5
3.0
76.3
2.7
0.2
1.8
3.5
91.2
3.2
0.2
Source: Reproduced from FAO, 2013a. Aquaculture and Capture Production 1950
2011. Rome: Statistics and Information Service of the Fisheries and Aquaculture
Department; FAO, 2013b. Cultured Aquatic Species Information Programme: Pangasius
hypophthalmus (Sauvage, 1878). Available at: http://www.fao.org/shery/
culturedspecies/Pangasius_hypophthalmus/en (accessed 08.04.14); and FAO, 2013c.
FAOSTATS. Available at: http://faostat.fao.org/site/291/default.aspx (accessed
08.04.14).
Table 5
407
Table 6
Continents
2010
Asia
Latin America and the Caribbean
Africa
Europe
Oceania
North America
World
16 078 000
248 000
150 000
85 000
6 000
4 000
16 570 000
97.0
1.5
0.9
0.5
0.04
0.02
Source: Reproduced from FAO, 2012. The State of World Fisheries and Aquaculture.
Rome: FAO.
Ranking
Country
Continents
Production
(million metric tons)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
China
Indonesia
India
Vietnam
Philippines
Bangladesh
Republic of Korea
Norway
Thailand
Egypt
Chile
Japan
Myanmar
Brazil
Malaysia
Democratic People's Republic of Korea
USA
Taiwan Province of China
Ecuador
Spain
Asia
Asia
Asia
Asia
Asia
Asia
Asia
Europe
Asia
Africa
Americas
Asia
Asia
Americas
Asia
Asia
Americas
Asia
Americas
Europe
50.2
7.9
4.6
3.1
2.6
1.5
1.5
1.1
1.0
1.0
1.0
0.9
0.8
0.6
0.5
0.5
0.4
0.3
0.3
0.3
59.9
9.5
5.5
3.6
3.1
1.8
1.8
1.4
1.2
1.2
1.2
1.1
1.0
0.8
0.6
0.6
0.5
0.4
0.4
0.3
Source: Reproduced from FAO, 2013a. Aquaculture and Capture Production 19502011. Rome: Statistics and Information Service of the Fisheries and Aquaculture Department; FAO,
2013b. Cultured Aquatic Species Information Programme: Pangasius hypophthalmus (Sauvage, 1878). Available at: http://www.fao.org/shery/culturedspecies/
Pangasius_hypophthalmus/en (accessed 08.04.14); and FAO, 2013c. FAOSTATS. Available at: http://faostat.fao.org/site/291/default.aspx (accessed 08.04.14).
408
Asian Aquaculture
Table 7
Ranking
Species
Categories
Production
(million metric tons)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
Silver carp
Japanese kelp
Eucheuma seaweeds
Grass carp
Cupped oysters
Japanese carpet shell
Common carp
Aquatic plants
Bighead carp
Catla
Whiteleg shrimp
Crucian carp
Elkhorn sea moss
Nile tilapia
Wakame
Warty gracilaria
Roho labeo
Pangas catshes
Scallops
Freshwater shes
Fish
Seaweed
Seaweed
Fish
Mollusks
Mollusks
Fish
Seaweed
Fish
Fish
Crustaceans
Fish
Seaweed
Fish
Seaweed
Seaweed
Fish
Fish
Mollusks
Fish
5.3
5.3
4.6
4.5
3.8
3.6
3.4
2.9
2.7
2.4
2.4
2.3
2.1
2.0
1.8
1.5
1.4
1.4
1.3
1.3
7.0
6.9
6.0
6.0
4.9
4.8
4.5
3.8
3.5
3.2
3.1
3.0
2.7
2.6
2.3
2.0
1.9
1.9
1.7
1.7
Source: Reproduced from FAO, 2012. The State of World Fisheries and Aquaculture. Rome: FAO.
Table 8
Ranking
Species
Categories
Value
(billion USD)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
Whiteleg shrimp
Silver carp
Grass carp
Catla
Common carp
Chinese mitten crab
Bighead carp
Giant tiger prawn
Japanese carpet shell
Nile tilapia
Mandarin sh
Crucian carp
Red swamp crawsh
Roho labeo
Pangas catshes nei
Cupped oysters nei
Freshwater shes nei
Scallops nei
Japanese eel
Milksh
Crustaceans
Fish
Fish
Fish
Fish
Crustaceans
Fish
Crustaceans
Mollusks
Fish
Fish
Fish
Crustaceans
Fish
Fish
Mollusks
Fish
Mollusks
Fish
Fish
9.9
7.7
5.8
4.7
4.6
4.5
3.5
3.4
3.3
3.1
2.6
2.5
2.3
2.2
2.2
2.2
1.9
1.9
1.6
1.6
9.2
7.1
5.4
4.4
4.3
4.2
3.2
3.2
3.0
2.9
2.4
2.3
2.2
2.1
2.1
2.1
1.7
1.7
1.5
1.4
Source: Reproduced from FAO, 2012. The State of World Fisheries and Aquaculture. Rome: FAO.
Asian Aquaculture
4 MT
6%
Brackish water
35 MT
46%
37 MT
48%
Fresh water
Marine
US$26
24%
US$13
12%
Brackish water
Fresh water
Marine
US$69
64%
409
410
Asian Aquaculture
Yield
biomass
Environment
Fish health
Earnings:
Socio-economics
investment
Food
safety
Table 9
Species
Total
Asia
ASC certied
Pangasius
Tilapi
Salmon
Total
36
27
2
65
36
20
0
56
BAP certied
Salmon
Shrimp
Tilapia
Pangasius
Mussels
Catsh
Jade Perch
Total
131
111
49
10
8
2
1
312
0
103
43
10
0
0
1
157
Aquaculture Certication
Future Forecast and Some Final Remarks
When talking about sustainable development, it is almost
impossible to neglect mentioning certication, which for
many is synonymous with sustainability. At the earlier time,
it is likely that most of the aquaculture production would
have been used for local consumption; hence, aquaculture
Asian Aquaculture
Table 10
Africa
Asia
Europe
Latin
America
and the
Caribbean
Northern
America
Oceania
World
Supplydemand
gap 2030 (million
metric tons)
11.7
156.5
18.6
16.2
18.7
186.3
23.4
18.3
7.0
29.8
4.8
2.1
6.2
12.9
6.6
1.5
210.7
1.8
261.2
0.3
50.6
Source: Reproduced from FAO Statistics and Information Service of the Fisheries and
Aquaculture Department, 2013. Aquaculture and Capture Production 19502011.
Rome: Food and Agriculture Organization of the United Nations.
conduct this future forecast were (1) aquaculture follows recent trends and capture sheries remain stationary and (2)
consumers consumption preference and sh prices unchanged
to calculate per capita sh demand using International Monetary Fund (IMF) GDP projection and multiply it by the UN
population projection.
The results indicated that there will be 51 million metric
tons of sh shortage in the world with most severe insufciency in Asia, amounting to almost 30 million metric tons
(Table 10).
This production increase needs to be driven by expansion
of sustainable aquaculture, which can be achieved only
through efcient farming systems that operate in harmony
with environment while providing social benets. Asia is both
the top producer and top consumer of aquaculture products,
which is likely to change for decades to come. For the livelihood and safety of Asian people it is essential that the sustainability challenges of the sector are addressed in a timely
manner. This requires a concerted effort that brings together
both the public and the private sectors. The experiences from
pangasius aquaculture in Vietnam have shown that public
private cooperation can achieve an unprecedented shift toward
increased sustainability, with a current production of ASCcertied pangasius of more than 20%, which was achieved
within approximately 2 years thanks to a partnership between
the Vietnamese government, producers, buyers, and nonprot
organizations (authors' personal observation). PublicPrivate
Partnerships are increasingly becoming key instruments to
achieve similar sustainability shifts and, with a growing competition for resources, are likely to become essential for the
aquaculture of the future.
411
References
Benzie, J.A.H., Nguyen, T.T.T., Hulata, G., et al., 2012. Promoting responsible use
and conservation of aquatic biodiversity for sustainable aquaculture development.
In: Subasinghe, R.P., Arthur, J.R., Bartley, D.M., et al. (Eds.), Farming the
Waters for People and Food. Proceedings of the Global Conference on
Aquaculture 2010, Phuket, Thailand, 2225 September 2010, pp. 337383.
Rome: FAO and Bangkok: NACA.
Cunningham, E.P., Syrstad, O., 1987. Crossbreeding Bos indicus and Bos taurus for
Milk Production in the Tropics. Rome: FAO.
FAO, 1995. Code of Conduct for Responsible Fisheries. Rome: FAO, p. 41.
FAO, 2011. Technical Guidelines on Aquaculture Certication. Rome: FAO.
FAO, 2012. The State of World Fisheries and Aquaculture. Rome: FAO.
FAO, 2013a. Aquaculture and Capture Production 19502011. Rome: Statistics and
Information Service of the Fisheries and Aquaculture Department.
FAO, 2013b. Cultured Aquatic Species Information Programme: Pangasius
hypophthalmus (Sauvage, 1878). Available at: http://www.fao.org/shery/
culturedspecies/Pangasius_hypophthalmus/en (accessed 08.04.14).
FAO, 2013c. FAOSTATS. Available at: http://faostat.fao.org/site/291/default.aspx
(accessed 08.04.14).
FAO/APFIC/NACA, 2012. Regional challenges and actions to support sustainable
intensication. Conclusions and recommendations of the FAO/APFIC/NACA
Regional Consultation on Sustainable intensication of aquaculture in the AsiaPacic 911 October 2012. Bangkok: FAO/APFIC/NACA.
FAO/WHO, 2011. Report of the joint FAO/WHO Expert Consultation on the Risks
and Benets of Fish Consumption, FAO Fisheries and Aquaculture Report
No.978. Rome: FAO.
Hall, S.J., Delaporte, A., Phillips, M.J., Beveridge, M., OKeefe, M., 2011. Blue
Frontiers: Managing the Environmental Costs of Aquaculture. Penang, Malaysia:
The WorldFish Center.
Hamilton, L.C., Haedrich, R.L., Duncan, C.M., 2004. Above and below the water:
Social/ecological transformation in Northwest Newfoundland. Population and
Environment 25 (3), 195215.
Marshall, M., 2013. Fish farming overtakes beef. New Scientist 218 (2922), 4.
Tacon, A., Hasan, M., Metian, M., 2011. Demand and supply of feed ingredients for
farmed sh and crustaceans: Trends and prospects. FAO Fisheries and
Aquaculture Technical Paper No. 564. Rome: FAO, p. 87.
WHO, 2006. Report of a joint FAO/OIE/WHO expert consultation on antimicrobial
use in aquaculture and antimicrobial resistance, 1316 June 2006. Seoul,
Republic of Korea: FAO/OIE/WHO.
Wikipedia, 2013. Available at: http://en.wikipedia.org/wiki/Seafood (accessed
08.04.14).
Xuan, L.X., Hien, L.L., 2010. Supply and use of catsh (Pangasianodon
hypophthalmus) seed in the Mekong Delta of Vietnam. Aquaculture Asia XV (1),
2633.
Relevant Websites
http://www.fao.org//glossary/
FAO.
http://www.fao.org/shery/culturedspecies/Pangasius_hypophthalmus/en
FAO.
ENCYCLOPEDIA OF
AGRICULTURE AND
FOOD SYSTEMS
VOLUME 2
ENCYCLOPEDIA OF
AGRICULTURE AND
FOOD SYSTEMS
EDITOR-IN-CHIEF
Academic Press
Academic Press is an imprint of Elsevier
32 Jamestown Road, London NW1 7BY, UK
225 Wyman Street, Waltham, MA 02451, USA
525 B Street, Suite 1800, San Diego, CA 92101-4495, USA
Copyright r 2014 Elsevier Inc. unless otherwise stated. All rights reserved
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic,
mechanical, photocopying, recording or otherwise without the prior written permission of the publisher
Permissions may be sought directly from Elseviers Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865
843830; fax (+44) (0) 1865 853333; email: permissions@elsevier.com. Alternatively you can submit your request online by visiting the
Elsevier web site at http://elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material
Notice
No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability,
negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein,
Because of rapid advances in the medical sciences, in particular, independent verication of diagnoses and drug dosages should be made
British Library Cataloguing in Publication Data
A catalogue record for this book is available from the British Library
Library of Congress Cataloging-in-Publication Data
A catalog record for this book is available from the Library of Congress
ISBN (print): 978-0-444-52512-3
EDITORIAL BOARD
Editor-in-Chief
Neal K Van Alfen
University of California, Davis, CA, USA
Associate Editors
Brent Clothier
Plant & Food Research
Palmerston North
New Zealand
John P Nichols
Texas A& M University
College Station, TX
USA
Daryl Lund
University of Wisconsin
Madison, WI
USA
Harris A Lewin
University of California
Davis, CA
USA
Mary Delany
University of California
Davis, CA
USA
R James Cook
Washington State University
Pullman, WA
USA
Roger RB Leakey
James Cook University
Queensland
Australia
Jeremy J Burdon
Commonwealth Scientic and Industrial
Research Organisation
Black Mountain, Canberra
Australia
Ronald L Phillips
University of Minnesota
St Paul, MN
USA
CONTRIBUTORS TO VOLUME 2
MC Ahearn
US Department of Agriculture Economic Research
Service, Washington, DC, USA
QX Fang
Qingdao Agricultural University, Qingdao, Shandong,
China
LR Ahuja
Agricultural Systems Research Unit, USDA-ARS, Fort
Collins, CO, USA
DR Farias
Federal University of Pelotas, Pelotas, RS, Brazil
KL Anderson
North Carolina State University, Raleigh, NC, USA
WJ Armbruster
Farm Foundation, Darien, IL, USA
B Auvermann
Texas A& M AgriLife Research and Extension Center,
Amarillo, TX, USA
RO Azizoglu
North Carolina State University, Raleigh, NC, USA
D Barile
University of California, Davis, CA, USA
GL Bennett
USDA, ARS, US Meat Animal Research Center, Clay
Center, NE, USA
T Breeze
University of Reading, Reading, UK
J Burke
University College Dublin, Dublin, Ireland
MV Chaudhari
National Dairy Research Institute, Karnal, Haryana,
India
J Chen
Texas A& M University, College Station, TX, USA
A Costa de Oliveira
Federal University of Pelotas, Pelotas, RS, Brazil
D Dallas
University of California, Davis, CA, USA
R Darbyshire
University of Melbourne, Carlton, VIC, Australia
C Feltrin
University of California, Davis, CA, USA
K Garbach
Loyola University Chicago, Chicago, IL, USA
KA Garrett
Kansas State University, Manhattan, KS, USA, and
Plant Biosecurity Cooperative Research Centre,
Canberra, Australia
B Gemmill-Herren
Food and Agricultural Organization of the United
Nations, Rome, Italy
P Gepts
University of California, Davis, CA, USA
I Goodwin
Horticultural Production Sciences, Tatura, VIC,
Australia
KG Grunert
Aarhus University, Aarhus, Denmark
ID Gupta
National Dairy Research Institute, Karnal, Haryana,
India
J Gupta
National Dairy Research Institute, Karnal, Haryana,
India
KE Hammond-Kosack
Rothamsted Research, Harpenden, UK
JL Hateld
USDA-ARS National Laboratory for Agriculture and the
Environment, Ames, IA, USA
FAJ DeClerck
Bioversity International, Maccarese, Rome, Italy
JF Hernandez Nopsa
Kansas State University, Manhattan, KS, USA, and
Plant Biosecurity Cooperative Research Centre,
Canberra, Australia
SO Duke
USDA, ARS, Oxford, MS, USA
AD Herring
Texas A& M University, College Station, TX, USA
TR Famula
University of California, Davis, CA
JB Holland
North Carolina State University, Raleigh, NC, USA
vii
viii
Contributors to Volume 2
P Huang
Texas A& M University, College Station, TX, USA
M Newell-McGloughlin
University of California, Davis, CA, USA
A Islam
Indian Council of Agricultural Research, New Delhi,
India
M van Noordwijk
Jalan Cifor, Bogor, Indonesia
DS Karp
University of California-Berkeley, Berkeley, CA, USA
SE Place
Oklahoma State University, Stillwater, OK, USA
T Kim
Seocho-gu, Seoul, Korea
EJ Pollak
USDA, ARS, US Meat Animal Research Center, Clay
Center, NE, USA
S Kjemtrup
Monsanto Company, Research Triangle Park, NC, USA
SG Potts
University of Reading, Reading, UK
LA Kuehn
USDA, ARS, US Meat Animal Research Center, Clay
Center, NE, USA
JE Preece
University of California, Davis, CA, USA
M Lange
UC Davis Health System, Sacramento, CA, USA, and
University of California, Davis, CA, USA
PE Read
University of Nebraska-Lincoln, Lincoln, NE, USA
JW Richardson
Texas A& M University, College Station, TX, USA
P Lavelle
Institute of Ecology and Environmental Sciences, Paris,
France
MC Roberts
North Carolina State University, Raleigh, NC, USA
A Le Parc
University of California, Davis, CA, USA
PJ Ross
University of California, Davis, CA, USA
H Lee
University of California, Davis, CA, USA
SA Saseendran
Agricultural Systems Research Unit, USDA-ARS, Fort
Collins, CO, USA, and Colorado State University, Fort
Collins, CO, USA
L Ma
Agricultural Systems Research Unit, USDA-ARS, Fort
Collins, CO, USA
RW Malone
National laboratory for Agriculture and the
Environment, USDA-ARS, Ames, IA, USA
N Marini
Federal University of Pelotas, Pelotas, RS, Brazil
BA McCarl
Texas A& M University, College Station, TX, USA
JC Milder
Rainforest Alliance, New York, NY, USA
BD Miller
Minnesota Department of Agriculture, St. Paul, MN,
USA
M Montenegro
University of California-Berkeley, Berkeley, CA, USA
F Moreira
Universidade Federal de Lavras (UFLA), Minas Gerais,
Brazil
JMLN de Moura Bell
University of California, Davis, CA, USA
G Schnitkey
University of Illinois, USA
B Sharratt
USDA Agricultural Research Service, Pullman, WA,
USA
B Sherrick
University of Illinois, USA
L Shiva
Texas A& M University, College Station, TX, USA
WM Snelling
USDA, ARS, US Meat Animal Research Center, Clay
Center, NE, USA
A Spain
The University of Western Australia, Perth, Australia
TL Talarico
Medicago USA, Durham, NC, USA
S Thomas-Sharma
Kansas State University, Manhattan, KS, USA
HCM van Trijp
Wageningen University, Wageningen, The Netherlands
Contributors to Volume 2
V Ursin
Monsanto Company, Mystic, CT, USA
CL Walthall
USDA-ARS Ofce of National Programs,
GWCC-BLTSVL, Beltsville, MD, USA
L Webb
Commonwealth Scientic and Industrial Research
Organisation (CSIRO), Aspendale, VIC, Australia
BA Welt
University of Florida, Gainesville, FL, USA
ix
Cross-References
Index
Contributors
xi
SUBJECT CLASSIFICATION
Agriculture and People
Agribusiness Organization and Management
Agricultural Cooperatives
Agricultural Ethics and Social Justice
Agricultural Finance
Agricultural Labor: Demand for Labor
Agricultural Labor: Gender Issues
Agricultural Labor: Labor Market Operation
Agricultural Labor: Supply of Labor
Agricultural Law
Agricultural Policy: A Global View
Analyses of Total Phenolics, Total Flavonoids, and
Total Antioxidant Activities in Foods and Dietary
Supplements
Changing Structure and Organization of US
Agriculture
Climate Change, Society, and Agriculture: An
Economic and Policy Perspective
Computer Modeling: Policy Analysis and Simulation
Consumer-Oriented New Product Development
Crop Insurance
Determining Functional Properties and Sources of
Recently Identied Bioactive Food Components:
Oligosaccharides, Glycolipids, Glycoproteins, and
Peptides
Farm Management
Food Chain: Farm to Market
Food Labeling
Food Law
Food Marketing
Food Security, Market Processes, and the Role of
Government Policy
Food Security: Development Strategies
Food Security: Food Defense and Biosecurity
From Foraging to Agriculture
Global Food Supply Chains
Government Agricultural Policy, United States
Human Nutrition: Malnutrition and Diet
Industrialized Farming and Its Relationship to
Community Well-Being
Intellectual Property in Agriculture
International and Regional Institutions and
Instruments for Agricultural Policy, Research, and
Development
International Trade
Investments in and the Economic Returns to
Agricultural and Food R&D Worldwide
Markets and Prices
Mathematical Models to Elaborate Plans for Adaptation
of Rural Communities to Climate Change
xiii
xiv
Subject Classication
Agriculture Products
Advances in Pesticide Risk Reduction
Agricultural Mechanization
Agroforestry: Complex Multistrata Agriculture
Agroforestry: Fertilizer Trees
Agroforestry: Fodder Trees
Agroforestry: Participatory Domestication of Trees
Agroforestry: Practices and Systems
Asian Aquaculture
Beef Cattle
Climate Change: Animal Systems
Climate Change: Cropping System Changes and
Adaptations
Climate Change: Horticulture
Climate Change: New Breeding Pressures and Goals
Critical Tracking Events Approach to Food
Traceability
Dairy Animals
Edaphic Soil Science, Introduction to
Fermentation: Food Products
Fermented Beverages
Food Engineering
Food Microbiology
Food Packaging
Food Safety: Emerging Pathogens
Food Safety: Food Analysis Technologies/Techniques
Food Safety: Shelf Life Extension Technologies
Food Security: Postharvest Losses
Food Security: Yield Gap
Food Toxicology
Forage Crops
Global Agriculture: Industrial Feedstocks for Energy
and Materials
Green Revolution: Past, Present, and Future
Medicinal Crops
Organic Agricultural Production: Plants
Organic Livestock Production
Precision Agriculture: Irrigation
Animal Health
Animal Health: Ectoparasites
Animal Health: Foot-and-Mouth Disease
Animal Health: Global Antibiotic Issues
Animal Health: Mycotoxins
Animal Health: Tuberculosis
Animal Welfare: Stress, Global Issues, and
Perspectives
Biosecurity and Equine Infectious Diseases
Detection and Causes of Bovine Mastitis with
Emphasis on Staphylococcus aureus
Emerging Zoonoses in Domesticated Livestock of
Southeast Asia
Invasive Aquatic Animals
Marek's Disease and Differential Diagnosis with
Other Tumor Viral Diseases of Poultry
Poultry and Avian Diseases
Quarantine and Biosecurity
Swine Diseases and Disorders
Vaccines and Vaccination Practices: Key to
Sustainable Animal Production
Zoonotic Helminths of Livestock
Plant Health
Climate Change and Plant Disease
Emerging Plant Diseases
Integrated Pest Management in Tree Fruit Crops
Invasive Species: Plants
Mineral Nutrition and Suppression of Plant Disease
Pathogen-Tested Planting Material
Plant Abiotic Stress: Salt
Plant Abiotic Stress: Temperature Extremes
Plant Abiotic Stress: Water
Plant Biotic Stress: Weeds
Plant Disease and Resistance
Plant Health Management: Biological Control of
Insect Pests
Subject Classication
xv
Biotechnology: Pharming
Biotechnology: Plant Protection
Biotechnology: Regulatory Issues
Breeding: Animals
Breeding: Plants, Modern
Cloning Animals by Somatic Cell Nuclear
Transplantation
Cloning: Plants Micropropagation/Tissue Culture
Domestication of Animals
Domestication of Plants
Genebanks: Past, Present, and Optimistic Future
Genomics of Food Animals
Genomics: Plant Genetic Improvement
Heterosis in Plants
Plant Cloning: Macropropagation
Plant Virus Control by Post-Transcriptional Gene
Silencing
Regulatory Challenges to Commercializing the
Products of Ag Biotech
Stem Cells
Transgenic Methodologies Plants
PREFACE
Food is absolutely necessary for human existence, yet for most
in wealthy nations it is largely taken for granted because of its
abundance. Sufcient food is a concern, however, for about 1
billion of the earth's inhabitants today who often go to bed
hungry. Food security in a broad sense is becoming a worry of
the future for those who understand the limitations of our
earth's ecosystems. Malthusian prophecies have so far been
wrong, but there is growing concern that we are rapidly
reaching the point where feeding the world's growing and
richer population will be at the cost to our environment that is
unacceptable. In the next few decades we face the challenge of
growing more food, with less water, with less fertilizer on less
land because of the growth of urban areas on prime agriculture land. We also face the largely unknown consequences
that global warming will have on agricultural production.
During the last century agricultural scientists were able to bring
cutting-edge science into traditional agricultural practices and
increase food production sufciently to prevent global food
shortages. The hope that new scientic discoveries will provide
the means to keep ahead of world food demand is complicated by a growing public discomfort with biotechnology
being applied to food production.
The concept of services being provided by the ecosystems of
the earth is a fairly recent attempt to understand and place
value on functions of natural lands that have historically been
assumed to have few limits. In the past, if more food was
needed, new lands were converted from forests or steppe lands
into farm land and new water systems developed to provide
the water needed for agriculture. When human populations
were low our activities were largely buffered by the abundance
of forest and steppe, but too late, we are beginning to
understand that these provisioning services of our ecosystems
are being overused and are no longer buffered by the abundance of wild lands and waters. We are rapidly losing our
planet's biodiversity, irreplaceable ground water is being unsustainably consumed, and major river systems are being
overused and polluted. Our oceans, the last place on the planet that still support our hunter and gathering traditions may
not be able to sustain these activities into the future. And, food
production and processing activities contribute to the greenhouse gas emissions that are rapidly warming our planet.
Agriculture is the single greatest user of the earth's land and
water resources. In the concept of ecosystem services, provisioning or providing food for all organisms is one of the
services provided by ecosystems. Human population growth
has and will continue to overtax the ecosystems we inhabit.
The ultimate outcome of this major diversion of nature's resources into provisioning the human species is unknown, but
it is critically important for us to understand what we must do
to sustain our planet.
The breakthrough discovery about 10 000 years ago that
plants and animals could be bred to provide a more abundant
and secure food source was the foundation upon which
all other human activities were able to ourish. Activities other
than nding food now became possible and our diverse
The issue raised by Dr. Borlaug is probably the most important challenge we face. Human behavior and the food
choices of consumers will determine the outcome of the race
between food supply and population. Population control has
been advocated for decades, and in some cases has become
part of national policy, but the world's population continues
to grow. Science breakthroughs cannot solve our food security
and environmental quality challenges if consumers reject food
that is not traditionally produced. Likewise, if meat products
and other inefciently produced food continue to be in high
demand by consumers, there will be increased pressure on our
food production systems. As supplies become short, prices rise.
While this may be good for farmers, high food prices and food
shortages will probably undermine our efforts to preserve the
xvii
xviii
Preface
fortunate to be joined by a very distinguished group of colleagues who, I hope, are still friends. They spent much more
time and effort in bringing this project to completion than any
of us anticipated. I want to thank our authors who while
overly committed and overworked, fullled their commitments to contribute to this work. I have been impressed with
the quality of their contributions. The editorial staff of Elsevier
have had the professionalism and patience to work with scientists who do not work under the same time and budget
constraints that the staff work. I want to particularly thank
Kristi Gomez, Donna de Weerd-Wilson, and Simon Holt who,
each in succession, oversaw this effort, and I especially thank
the project managers, who worked directly with me, and the
associate editors, Kate Miklaszewka-Gorczyca, Will BowdenGreen, and Sam Mahfoudh.
Neal K Van Alfen
Professor, Department of Plant Pathology Dean Emeritus,
College of Agricultural and Environmental Sciences,
University of California Davis, CA, USA
CONTENTS TO VOLUME 2
Editorial Board
Contributors to Volume 2
Guide to using the Encyclopedia
v
vii
xi
Subject Classification
xiii
Preface
xvii
B
Beef Cattle
AD Herring
21
41
61
69
94
Biotechnology: Pharming
S Kjemtrup, TL Talarico, and V Ursin
117
134
153
Breeding: Animals
GL Bennett, EJ Pollak, LA Kuehn, and WM Snelling
173
187
C
Changing Structure and Organization of US Agriculture
WJ Armbruster and MC Ahearn
201
220
232
244
xix
xx
Contents to Volume 2
256
266
284
294
307
317
337
359
375
387
Crop Insurance
G Schnitkey and B Sherrick
399
Crop Pollination
SG Potts, T Breeze, and B Gemmill-Herren
408
D
Dairy Animals
J Gupta, ID Gupta, and MV Chaudhari
419
435
Determining Functional Properties and Sources of Recently Identified Bioactive Food Components:
Oligosaccharides, Glycolipids, Glycoproteins, and Peptides
M Lange, H Lee, D Dallas, A Le Parc, JMLN de Moura Bell, and D Barile
441
Domestication of Animals
TR Famula
462
Domestication of Plants
P Gepts
474
487
B
Beef Cattle
AD Herring, Texas A&M University, College Station, TX, USA
r 2014 Elsevier Inc. All rights reserved.
This article is a summary of Beef Cattle Production Systems by Andy Herring
CAB International 2014, and reproduced with permission from CAB
International, Wallingford.
Glossary
Beef The meat from cattle carcasses.
Bos indicus Distinct subspecies of cattle that are
descendants of domestication in South Central Asia (India);
these cattle generally have a hump over the shoulder and are
known for extreme tropical adaptation.
Bos taurus Distinct subspecies of cattle that are
descendants of domestication in the Near/Middle East and
comprise the historical breeds of Europe; these cattle are
nonhumped.
Bull An intact (uncastrated) male bovine.
Calf A young bovine, generally less than 12 months of age.
doi:10.1016/B978-0-444-52512-3.00130-3
Beef Cattle
Table 1
Name
Description
Seedstock
Seedstock herds are mainly purebred herds with animals registered in breed society herd books that produce
animals for breeding purposes. They can be classied as elite and multiplier operations. Elite operations produce
the highest valued breeding animals in the breed and sell animals to other seedstock operators; multiplier
operations sell primarily bulls to commercial cow-calf operations
Cow-calf operations are driven by cow reproductive performance and overall productivity evaluated through calf
production to weaning. Commercial cow-calf operations may sell calves close to weaning or may also/instead
sell animals from grower and nishing phases. Different combinations of traits will receive emphasis relative to
what age/stage of development animals are sold
These operations purchase or obtain young animals for growth. This can be grazing based on rangeland, forage
crops, row crop residues, or may be feedlot based. Cattle are grown for some time, but not to completion of
market size, weight, or fatness. These may utilize calves destined for beef, or replacement heifers or males for
breeding purposes
These operations produce cattle that go directly to slaughter. These can be grazing entirely, grain-assisted with
grazing, conned feeding of green crops (such as cut-and-carry), or conned feeding of high-grain/concentrate
diets. These operations can obtain cattle from cowcalf operations or from grower operations
A commercial herd as component of a seedstock operation adds exibility for progeny testing, production of
recipient females for embryo transfer; it is common that some seedstock operations also have a commercial
herd rather than a primarily commercial herd developing a seedstock portion
Finisher
Table 2
Estimated global production, emissions, and emission intensity from cattle milk and meat production
System
Milk
Meat
Milk
Meat
Milk
Meat
508.6
26.8
34.6
1331.1
486.2
2338.4
2.6
18.2
67.6
Dairy
Beef
Source: Reproduced from Gerber, P.J., Steinfeld, H., Henderson, B., et al., 2013. Tackling Climate Change Through Livestock A Global Assessment of Emissions and Mitigation
Opportunities. Rome: Food and Agriculture Organization of the United Nations (FAO).
the genus Bos are known as the true cattle and include yak,
banteng, gaur, kouprey, and domesticated cattle. Yak, banteng,
and gaur have domesticated populations as well as wild
populations. The autosomes of cattle (Bos spp.) are acrocentric
and the X chromosome is submetacentric; however, in Bos
taurus the Y chromosome is submetacentric, whereas in Bos
indicus it is acrocentric.
Domesticated cattle (B. taurus and B. indicus) were developed
from the ancient wild ox (aurochs, aurochsen plural, and
Bos primigenius) that existed from the European (present-day
Britain) Atlantic coasts to the Asian Pacic coasts. Several cave
paintings in Western Europe show artists interpretations of the
appearance of these animals. They had long horns, were lean,
apparently light muscled in hindquarters, and had mediumlength hair with large skeletal size, perhaps 2 m (6 ft) tall at the
shoulder (Porter, 1991). Bos indicus and B. taurus are believed to
have arisen from two distinct domestication events, and the
common ancestors of these two groups may have separated
100 000 years ago or more (well before domestication).
Breeds
There are approximately 1000 different breeds of cattle globally. Most breeds have been developed purposely or have
evolved from local cattle types. In the past 100 years, several
Beef Cattle
Poll
Nose or
muzzle
Crest of
neck
Hump location
in Zebu
M
M
Tail head
Hook or
F
hip bone
F
M
Shoulder
Dewlap
Rear flank
M
F
F
Brisket
Tail switch
M
Forearm
Sheath and
naval area
Knee
Hock
Dewclaw
Hoof
Figure 1 Identication of some general beef cattle body areas and locations to evaluate fat (F) and muscle (M).
Table 3
Name
Description
Class Mammalia
Subclass Theria
Infraclass Eutheria
Order Cetartiodactyla
Suborder Ruminatia
Infraorder Pecora
Family Bovidae
Subfamily Bovinae
Tribe Bovini
Genus Bos
Species Bos indicus or Bos taurus, or hybrids
Beef Cattle
Table 4
General classications and descriptions of some fundamental biological types of domesticated cattle that relate to production and
adaptation aspects
Term
Subspecies
Bos taurus
Bos indicus
Purpose
Beef
Dairy
Draft
Dual purpose
All purpose
Geography
British
Caucasian
Chinese yellow cattle
Continental European
Criollo
Gray Steppe
Podolian
Sanga
Western African humpless
Japan/Korea
Breeds from British Islands off European continent developed for meat production
Short-horned ancient-type of B. taurus cattle from Mediterranean, the Middle East, Eastern and Southeastern
Europe, and Northern Africa
Indigenous domestic cattle of China, not a reference to coat color. Common yellow cattle are typically nonhumped;
yellow cattle further south have some evidence of a hump
Breeds from Western and Central Europe used for meat production, but many had ancestors also used for draft;
several are dual purpose meat and milk
Tropically adapted B. taurus cattle of North and South America whose ancestors originally came from the Iberian
peninsula of Spain and Portugal
Long-horned, light haired, and dark-pigmented B. taurus cattle of Eastern Europe considered an ancient type
Breeds of Central Europe, primarily Italy, which were derived from eastern steppe cattle origin and include Apulian,
Chianina, Maremmana, Marchigiana, Piedmontese, and Romagnola
Cattle native to Africa that possess a neck hump, originally in Eastern and Southern African continent, some have
classied Sanga as B. taurus because these breed possess a submetacentric Y chromosome
Nonhumped breeds that are indigenous and survive in the tsetse y region of West Africa and include Baoul,
N'Dama, Kuri, and Lobi
Wagyu/Hanwoo East Asian breeds known for extremely high levels of intramuscular fat deposition ability
of genes/alleles (such as when an allele is dominant over another or when the genotypes at different spots of the genome
interact to inuence the phenotypic expression). These potential nonadditive genetic interactions typically inuence
many traits through the phenomenon of heterosis (hybrid
vigor). This phenomenon occurs when the crosses of parental
stocks perform more favorably than expected, which is based
simply on the amount of parental stock in the crossbred animals. Table 7 provides general guidelines of heterosis expectations relative to heritability for types of traits in beef cattle.
Consideration of both of these genetic inuences is quite
important for beef cattle production systems but can have
varying relative importance in specic production components. In the vast majority of situations, some type of
crossbreeding system where crossbred cows are utilized allows
improved productivity when production of market beef animals is the goal (Figure 3).
Nutrition
Beef cattle as ruminants have the ability to convert forage into
meat production that cannot directly occur in nonruminant
species. Consequently, cattle and other grazing livestock can
commonly utilize lands that are not functional for other
agricultural uses, such as farming. Depending on the geographical region, the ability to match the nutritional
Beef Cattle
Table 5
Examples of some breeds (excluding recent composites) with regard to biological groupings
British beef
Angus/Red Angus
Belted Galloway
British White
Devon
Dexter
Galloway
Hereford
Highland
Shorthorn
South Devon
Sussex
Welsh Black
Sanga
Africander (Afrikaner)
Ankole
Barotese
Bapedi
Dinka
Zebua
American Brahman
Boran
Fulani
Gir
Hariana
Indu-Brazil
Kankrej (Guzer)
Ongole (Nelore)
Red Sindi
Sahiwal
Criollob
Blanco Orejinegro
Carac
Chaqueo
Chusco
Mexican Corriente
Romosinuano
San Martinero
Texas Longhorn
European dairy
Ayrshire
Guernsey
Holstein-Friesian
Jersey
Pinzgauer
Salers
Simmental
Tarentaise
Caucasian
Anatolian Black
Baladi
Brown Atlas
Bua
Greek Shorthorn
Kurdi
Mashona
Nguni
Nkone
Tuli
Tswana
Marchigiana
Piedmontese
Romagnola
Milking Shorthorn
Norwegian Red
Swedish Red and White
Swiss Brown
Turkish Gray
Ukranian Gray
Nanyang
Qinchuan
Tibetan
Yanbian
consume is provided to them as in a feedlot. In some situations there may be conditions that warrant intensive feeding
of cattle for a particular stage of production or environmental
situation (such as drought, etc.). Tables 10 and 11 provide
some examples of diets to feed growing cattle. Adequate daily
supply of clean water is crucial; cattle are expected to consume
approximately 1 l of water per every 12 kg of live weight (1 gal
per 100 lb) daily under nonextreme conditions.
The diets, mentioned in Table 10, which are appropriate
for growing cattle can also be used for mature cows or
feedlot fattening (nishing) of growing or older cattle. The
rate of weight gain associated with any diet fed to cattle
depends on their current weight (and stage of production)
and the rate of intake of the diet. Usually, with intensive
feeding of cattle there is a balance desired between increased
production potential and increased costs. This same concept
holds true for grazing situations but may not be obvious to
managers if they do not know the forage cost or consumption. Any ration that is formulated to meet nutritional
requirements must be fed at the recommended rate for it to
be effective as it was designed.
Proper feeding of cattle is essentially proper feeding of the
rumen microbes. Thus, it is obvious that rapid transitions
from drastically different diets could cause digestive problems when the rumen microbial population has its nutrient
Manure Production
It is appropriate that the last topic discussed under nutritional concepts is manure production. The amount and
nutritional composition of manure vary directly as a function
of the diet according to digestibility and specic feedstuffs
consumed. Manure is the waste produced from digestion and
Beef Cattle
Table 6
Trait
Estimate
Reproductive traits
Age at rst calving
Age at puberty
Calf survival
Calving interval
Calving date
Calving rate
Calving to rst insemination
Days to calving
Dystocia
First service conception rate
Heifer pregnancy rate
Pregnancy rate
Ovulation rate
Twinning rate
Scrotal circumference
0.100.25
0.200.40
0.10
0.10
0.100.20
0.10
o0.10
o0.10
0.30
0.050.20
0.150.20
0.050.10
0.100.40
0.10
0.300.50
0.40
0.30
0.35
0.80
0.80
0.35
0.30
0.45
0.45
0.42
0.28
0.39
0.41
0.48
0.45
0.28
0.51
0.52
0.51
0.54
0.51
0.45
Reproduction
Reproduction in beef cattle herds is the primary limitation for
beef production systems, and the amount of beef that can be
produced is a direct function of animal numbers. Some reproductive considerations specic to beef cattle are addressed
here regarding female, male, and herd concepts.
Female Considerations
The estrous cycle in cattle is dened as the time between two
consecutive estrus periods (time between heat periods) of a
female. In cattle the estrous cycle is 21 days long on average.
The length of the heat or estrus period itself is approximately
1218 h, and ovulation typically occurs 2430 h after the
onset of estrus (beginning of heat period), so this typically
corresponds to approximately 12 h after heat (and is the basis
of the old recommendation that if a cow is in heat in the
morning, breed it in the evening that day, and if it is in heat in
the evening, breed it the following morning, otherwise known
as the ampm rule).
Heifers must reach puberty at an early enough age where
herd fertility is not impeded, and this is critical when there
are dened breeding and calving seasons. In many environments and with most B. taurus breeds and their crosses, age of
puberty is not a limiting factor of reproductive success, provided that adequate nutrition is available. Puberty in heifers
can be dened in different ways, such as time of rst ovulation, time of rst estrus, or time of rst pregnancy carried to
full term; here it means the time when a heifer can rst become pregnant and produce a calf. Breeds that are known for
high levels of milk production are known to have earlier age
of puberty than breeds with lower milk production potential.
Within the same level of milk production, breeds that are
larger in size may reach puberty later than those of smaller
mature size, but this relationship is less precise than with
milk production.
Heifers of most B. taurus breeds reach puberty at 1013
months of age when nutrition is not limiting; however, in
many dual-purpose breeds this can be as low as 6 months or
even earlier. In those cases puberty may be so early that some
of the bull calves may breed some of their heifer mates before
they are weaned, which presents other reproductive management challenges. This is the exception rather than the rule in
most situations. In many environments, a target calving age of
approximately 24 months is realistic with B. taurus breeds and
most B. indicusB. taurus crosses. With limited feed resources, a
more realistic age of rst calving is approximately 36 months
Beef Cattle
Table 7
Summary of heritability and heterosis levels for beef cattle production traits
Type of trait
Heritability
Heterosis
Low
Moderate
High
High
Moderate
Low
MP
F1
Heterosis
Mean of
breed A
MP value
(expected mean of
group that is A and
B without heterosis)
Mean of
breed B
Figure 3 When crossing two breeds (A and B), the mid-parent(MP) value is halfway between the purebred means. The amount of deviation of
the crossbred population mean from the MP value is the amount of heterosis. F1 Refers to the rst cross progeny resulting from mating
purebred parents of different breeds such as A sires with B dams, and, B sires with A dams.
Table 8
General guidelines for total digestible nutrients (TDN) and
crude protein (CP) requirements for cattle
Table 9
Production cycle/calendar of the cow herd thought of in
3-month increments relative to energy and protein requirements
Class of cattle
TDN (%)
CP (%)
Stage
Crude protein
(%)
Growing animals
Lactating mature cows
Dry mature cows
6065
5560
5055
1213
10
78
Early lactation
Mid-lactationearly
pregnancy
Late lactation
mid-gestation
Late gestation
Highest
Intermediate
Highest
Intermediate
Lowest
Lowest
Intermediate
Intermediate
Articial Insemination
Articial insemination (AI) is a reproductive tool that can
greatly aid in breeding programs and is widely available for beef
cattle producers. Semen is commonly collected on highly prized
bulls and available for purchase. In general, bulls are kept at
facilities specialized in semen collection and processing. The
semen is collected by means of an articial vagina when the bull
mounts a xed dummy structure or another animal. After
collection, the semen is evaluated for its quality (abnormalities,
motility, etc.), has some type of extender solution added to it,
and is placed into plastic straws that are labeled with the facility
code, breed, and individual ID of the bull. The straws are then
Beef Cattle
Digestibility
Crude protein
30
70
26
65
22
60
18
55
14
50
10
45
Digestibility (%)
75
40
Warm
season
grasses
Cool
season
grasses
Warm
season
legumes
Cool
season
legumes
Figure 4 General guidelines for energy (digestibility as TDN) and CP content of different classes of forage for meeting cattle nutritional requirements.
All forage species are highly variable within and across time and location. Annuals may be slightly higher in digestibility than perennials.
Table 10
Example 1
Sudan hay
Wheat
Maize
Soybean meal
Dicalcium phosphate
Limestone
Salt
Proportion (%)
55.7
20.0
18.0
5.0
0.5
0.5
0.3
Example 4
Grass hay
Wheat
Grain sorghum
Soybean meal
Dicalcium phosphate
Limestone
Salt
Proportion (%)
54.7
20.0
19.0
5.5
0.5
0.5
0.3
Example 2
Grass hay
Grain sorghum
Soybean meal
Dicalcium phosphate
Limestone
Salt
Proportion (%)
52.2
40.0
7.0
0.5
0.5
0.3
Example 5
Sudan hay
Maize
Soybean meal
Dicalcium phosphate
Limestone
Salt
Proportion (%)
57.2
35.0
7.0
0.5
0.5
0.3
Example 3
Alfalfa hay
Maize
Dicalcium phosphate
Salt
Proportion (%)
67.7
31.5
0.5
0.3
Example 6
Alfalfa hay
Grain sorgum
Dicalcium phosphate
Salt
Proportion (%)
59.2
40.0
0.5
0.3
Note: It is recommended that hays be ground and grains be rolled or ground. Components of these examples may be used as supplements for cattle grazing forage if relative
nutritional values of forage are known.
Source: Adapted from Lusby, K.S., Gill, D., 1982. Formulating Complete Rations. Fact Sheet 3013. Stillwater, OK, USA: Oklahoma State University (OSU) Cooperative Extension
Service.
Male Considerations
Several research trials have been conducted that show semen
quality and scrotal circumference increase dramatically for 46
months following puberty. As a result, it should not be assumed that a bull is fully fertile because it has reached puberty.
Beef Cattle
Table 11
Ration 1
Ration 2
Item
Kg day
Dry hay
12%
protein
Grain corn
Supplement
5.5
Premix
1
Ration 3
Item
Kg day
5.2
2.8
0.5
Dry hay
15%
protein
Mixed grain
Supplement
3.5
0
0.03
Premix
0.06
Would require
approximately 1100 kg
of hay and 560 kg of
grain corn per calf
1
Would require
approximately 1040 kg
of hay and 700 kg of
mixed grain per calf
Ration 4
Item
Kg day
Dry hay
15%
protein
Corn silage
Corn
screenings
Supplement
Premix
2.5
1
8.5
2.5
0.5
0.03
Ration 5
Item
Kg day 1
0.5
0.5
7.5
7.5
Corn silage
High moisture corn
(HMC) and cob meal
Corn gluten feed
Premix
10.0
2.5
Item
Kg day
Dry hay
15%
protein
Corn silage
Haylage
Corn
Supplement
Premix
1.4
0.2
0.03
1
2.4
0.09
Would require
approximately 500 kg of
hay, 1700 kg of corn
silage and 500 kg of
corn screenings per calf
2806
3426
3098
1
Note: Diets such as these should result in average daily gain of 0.9 kg day over 200 days for cattle growing from 227 to 408 kg of weight with an expected daily dry matter intake of
2.5% of body weight; all are expected to provide approximately 8.68.7 feed to gain ratio.
Source: Reproduced from Martin, D., 2006. Typical beef feedlot and background diets. Fact Sheet Agdex# 425/60. Ontario Ministry of Agriculture and Food. Available at: http://www.
omafra.gov.on.ca/english/livestock/beef/facts/06-017.htm (accessed 03.09.13) as for Ontario, Canada.
Figure 5 Nellore bulls in Brazil fed corn plant-based diet. The picture on the right shows the ration in the feed bunk (trough) that consisted
mainly of maize (corn) plants (stalk and leaves and cobs with grain) that had been ground.
43.3
5.0
58.6
93.5
14.0
37.9
17.4
35.0
5.0
56.7
93.6
14.1
38.2
17.7
90.0
65.0
79
63.7
93.6
15.0
32.9
13.0
60.0
5.0
35.0
0
65.0
90.0
73.3
1012
67.9
93.8
15.4
31.2
11.0
68.3
5.0
26.7
0
73.3
90.0
81.7
1315
76.3
95.7
15.5
31.5
8.5
76.7
5.0
18.3
0
81.7
90.0
90.0
1619
83.2
95.2
15.3
31.3
7.7
85.0
5.0
10.0
0
90.0
On the rapid adaptation protocol, only the 40%, 65%, and 90% concentrate diets were fed. All diets were used in the gradual adaptation protocol (shown above).
The barley grain was dry-rolled as a single lot to a processing index of 84.6%: [(volume weight after processing/volume weight before processing) 100%].
c
Supplement contained urea as a N source, as well as Ca, 10.9%; Na, 1.4%; Zn, 1150 ppm; Mn, 530 ppm; Cu, 290 ppm; I, 13.0 ppm; Se, 5.7 ppm; Co, 4.7 ppm; vitamin A, 96 000 IU kg 1; vitamin D, 9500 IU kg 1; vitamin E, 630 IU kg 1;
and monensin sodium, 684 ppm.
d
Values determined from analysis. All values except DM, %, are expressed on a DM basis.
e
All cattle were on 40% diet, but beginning on day 1 half were switched to 65% diet and half were switched to 48.3% diet. On day 4 the rapid adaptation heifers were switched to 90% diet, but the gradual adaptation heifers were switched to
the 56.7% diet, etc.
Abbreviation: DM, dry matter.
Source: Reproduced from Bevans, D.W., Beauchemin, K.A., Schwartzkopf-Genswein, K.S., McKinnon, J.J., McAllister, T.A., 2005. Effect of rapid or gradual grain adaptation on subacute acidosis and feed intake by feedlot cattle. Journal of Animal Science
83, 11161132.
90.0
56.7
40.0
40.0
Rapid adaptation
Gradual adaptation
65.0
48.3
61.6
94.0
15.6
32.6
14.2
51.7
5.0
38.3
5.0
56.7
Treatmente
41.7
10.0
48.3
45.0
15.0
40.0
Example of feedlot rations with varying amounts of grain and associated nutritional analyses from a study evaluating feed transition time
Ingredients (% of DM)
Barley silage
Grass hay
Concentrate
Barley grainb
Supplementc
Chemical composition (%)d
DM
Organic matter
Crude protein
Neutral detergent ber
Acid detergent ber
Item
Table 12
10
Beef Cattle
Beef Cattle
Table 13
11
Quantity
Weight
(kg day 1)
Volume
(m3 day 1)
Total solids
(kg day 1)
Organic matter
Volatile solids
(kg day 1)
COD
(kg day 1)
C:N ratio
Plant nutrients
N (kg day 1)
P (kg day 1)
K (kg day 1)
Examplesb
Grazing cow
Grazing 200 to
340 kg calf
340 to 454 kg
Yearling on
high-forage
diet
340 to 454 kg
Yearling on
high-energy
diet
550 kg Cow
grazing
pasture
400 kg Steer
grazing
400 kg Feedlot
steer
28.57
26.39
26.80
23.22
34.6
23.6
20.5
0.028 3
0.026 319
0.026 885
0.023 206
0.034 3
0.023 7
0.020 4
3.31
3.42
3.07
2.68
4.0
2.7
2.4
2.81
2.91
2.74
2.47
3.406
2.413
2.174
2.72
2.72
2.77
2.54
3.296
2.441
2.242
0.18
0.07
0.14
0.12
0.04
0.10
0.12
0.04
0.08
10
12
0.15
0.05
0.12
0.14
0.05
0.09
11
10
0.14
0.05
0.11
0.14
0.04
0.10
Values from Hamilton (2004). Weight is total mass of urine and feces excreted; volatile solids refer to mass percentage of total solids that will ignite when heated to 550 1C;
Chemical oxygen demand (COD) is related to amount of oxygen required to digest manure; carbon to nitrogen ratio (C:N) is related to stability.
b
The calculation for daily manure production in the examples comes from taking the appropriate rate for the size class in accordance with the animal's weight (for instance
daily manure solids from a 550 kg cow takes the rate of 3.31 kg day 1/454 kg of weight and multiplies this value by the ratio of the animal's weight of 550 kg as compared
with the standard rate, or 3.31 kg is expected from a 454 kg cow, but a 550 kg cow is expected to produce 550/454 1.21 times as much, or 4.0 kg, etc.).
Reproductive
success
4
5
6
Body condition score
Early Weaning
In many geographical areas it is common to wean calves at an
average age of approximately 7 months. There is nothing
magical about this calf age for weaning, but many breed societies or associations adjust weaning weight to a standardized
calf age (200 days, 205 days, etc.). Some producers weigh
calves around this age to submit weights to breed societies, but
keep calves on the cows until 9 or 10 months of age. Many
12
Beef Cattle
Table 14
Breed
Angus
Charolais
Horned Hereford
Polled Hereford
Simmental
Limousin
Santa Gertrudis
Brahman
o14
1417
1820
2123
2426
2730
3136
436
34.8
32.6
33.0
34.8
33.4
30.6
34.0
21.9
35.9
35.4
32.2
34.2
36.5
31.7
35.3
27.4
36.6
34.5
34.1
34.9
32.0
35.5
29.4
36.9
34.9
36.2
34.9
33.9
36.7
31.4
36.7
34.6
33.4
34.8
36.0
36.5
31.7
36.3
36.2
33.8
35.0
36.4
33.5
36.6
37.1
35.2
35.6
38.3
34.7
38.2
38.1
34.0
36.4
37.2
35.5
40.5
36.7
Source: Reproduced from Sprott, L.R., Thrift, T.A., Carpenter, B.B., 1998. Breeding Soundness of Bulls. Pub # L-5051. College Station, TX: Texas A&M AgriLife Extension Service.
Table 15
Reproductive tract
Semen evaluation
Calving interval
Note: Although only semen evaluation traits are given a score, the failure in any category can result in failure of the overall breeding soundness exam. Libido or serving capacity is not
evaluated as a component of breeding soundness exams under the Society of Theriogenology (USA) but is included under the Australian Association of Cattle Veterinarians
(McGowan et al., 1995) evaluation. The Western Canadian Association of Bovine Practitioners (Barth, 2000) has a spot on the form for libido assessment but states the producer of the
bull should evaluate this.
Health
commercial producers wean calves when they are approximately 68-month old on average. Some producers may let
cows wean the calves on their own; under extensive conditions
a cow will usually stop nursing its calf when it is getting closer
to having another calf, but not always. Other commercial
producers may wean calves early at approximately 6090 days
of age. Weaning at this young age has widely reported reproductive advantages for the cows. There is a direct neural
Beef Cattle
Table 16
13
Sign
Abnormal indications
Rectal temperature
38.5 1C (101.5 F)
30
6070
Demeanora
Feces
Movementa
Hair appearance
What is normal behavior as well as other traits can vary drastically across individuals and circumstances (such as with a newborn calf), and abnormal is a marked deviation
from what is typical. History of observation provides useful information. Documentation of these signs that are suspected to be abnormal will aid veterinarians in diagnoses.
a
Table 17
Summary statistics for hair coat characteristics and sweating rate for Braford cows in Mato Grosso do Sul (Brazil)
Trait
Mean
SD
CV (%)
Minimum
Maximum
3.73
993
10.41
30.98
18
319.97
1.72
504
3.91
8.13
13
83.02
46.1
50.8
37.6
26.2
72.2
25.9
1.00
319
4.13
11.00
1
89.20
13.00
4852
26.50
69.00
63
591.48
Note: Based on 1607 observations across heifers and cows through 5-year-olds in a single commercial herd. Females were generated from 33 sires and varied in breed composition
from 25% Hereford75% Nelore to 75% Hereford25% Nelore.
Source: Reproduced from Bertipaglia, E.C.A., da Silva, R.G., Cardoso, V., Fries, L.A., 2007. Hair coat characteristics and sweating rate of Braford cows in Brazil. Livestock Science
112, 99108.
Adaptation
Cattle as a species are quite remarkable in that they can exist
in very extreme climatic conditions. However, this does not
mean that all types of cattle can equally exist in all conditions.
Cattle can adapt to harsh cold climates as well as tropical
environments. Two terms that should be discussed here are
14
Beef Cattle
Table 18
Recommendations about space and rest for cattle hauled long distances and small calves
Cattle size
500 kg
8
12
24
24
8
6
12
6
Floor space for young calves of different sizes
Up to 55 kg
55110 kg
0.30.4 sq m
0.40.7 sq m
110250 kg
0.70.8 sq m
Source: Values taken and adapted from European Commission (2002). The welfare of animals during transport (details for horses, pigs, sheep and cattle). Report of the Scientic
Committee on Animal Health and Animal Welfare. Brussels: European Commission.
Table 19
Recommended loading densities of cattle to be
transported by truck
Mean live weight
(kg, lb)
250,
300,
350,
400,
450,
500,
550,
600,
650,
0.77,
0.86,
0.98,
1.05,
1.13,
1.23,
1.34,
1.47,
1.63,
38
34
30
28
26
24
22
20
18
551
662
772
882
992
1103
1213
1323
1433
8.3
9.3
10.5
11.3
12.2
13.2
14.4
15.8
17.5
Source: Taken from Australian standards and guidelines for the welfare of animals-land
transport of livestock.
Beef Cattle
15
Table 20
General compositional aspects of market weight beef,
pork, and lamb
Round
Short
loin
Flank
Sirloin
Trait
Beef
Pork
Lamb
454544
95104
45
36
60
6
70
812
50
272318
6873
23
Lean
Fat
Bone
Short
plate
Chuck
Fo
re
55
28
17
Source: Reproduced from FAO, 2012. Meat cutting and utilization of meat cuts. Rome,
Italy: Food and Agriculture Organisation of the United Nations. Available at: http://www.
fao.org/docrep/004/t0279e/t0279e05.htm (accessed 22.10.13).
Brisket
Rib
sh
an
Genetics
Within B. taurus, biological type of British-based versus Continental European-based differences exist with regard to tenderness, marbling, and muscle deposition that correspond to
differences in growth rate, weight at the time of slaughter, and
fatness at slaughter. British types seem to have slight advantages in tenderness when other composition factors are held
constant, but increase in tenderness in several cases when
differences in other factors, such as fat thickness, time on feed,
etc., are not equal. Continental European cattle tend to be
taller, have heavier and more muscular carcasses at a constant
fat thickness, and require a longer time on high-energy diets to
reach a constant fat endpoint. The two main differences (related to genetics) between B. taurus and B. indicus cattle relate
to tenderness associated and degree of marbling, where B.
taurus (particularly British type) has advantages in both traits.
Certain genetic types, such as Japanese Black (Wagyu) and
Korean Hanwoo, have extremely high marbling potential,
particularly when fed for long times; other genetic types, such
as double-muscled breeds like Belgian Blue, Piedmontese, etc.,
have very little marbling.
Physiological Age
Age is associated with palatability, which is usually assessed by
skeletal ossication and dentition but may also be indicated
by lean muscle color. Increased age is associated with reduced
Nutrition
Higher planes of nutrition will speed up growth rate as well as
fat deposition. Type of diet, such as grass-fed versus concentrate-fed diet, and even type of forage and grain can impact
color, avor, and fatty acid prole. Differences in marbling are
thought to be driven primarily in differences in external fat
thickness. Differences in tenderness appear to be a function of
differences in age.
Environmental Stresses
How animals handle stress can affect energy metabolism. This
may be due to illness as severity of bovine respiratory disease
has been shown to reduce carcass marbling; impacts on tenderness do not seem to be obviously impacted but have not
been intensely studied. Energy used to conserve and dissipate
body heat can affect efciency of gain and carcass composition
when conditions are drastically different from the thermoneutral zone. Long-term stress is thought to increase risk of
producing dark cutting beef (color of the lean muscle is much
16
Beef Cattle
Table 21
Expected percentages of live weight and weights for various by-products from cattle of different biological type (550 kg live weight
basis at external fat of 1012 mm)
Percentage (%) of live weight
English
Holstein
Z50% Indicus
English
Holstein
Z50% Indicus
Green hide
Trimmed hide
Fleshed hide
Cured hide
8.2
7.7
6.7
5.9
6.5
6.0
5.7
5.0
9.2
8.7
7.4
6.3
45.1
42.4
36.9
32.5
35.8
33.0
31.4
27.5
50.6
47.9
40.7
34.7
Liver
Heart
Tunic tissue
Green tripe
Scalded tripe
Oxtail
Weasand meat
Pancreas
Sweetbread
Kidney
1.45
0.48
0.026
2.04
1.24
0.26
0.030
0.084
0.091
0.223
1.96
0.50
0.02
2.15
1.13
0.21
0.034
0.093
0.104
0.255
1.26
0.39
0.024
2.00
1.04
0.28
0.032
0.086
0.062
0.215
8.0
2.6
0.1
11.2
6.8
1.4
0.2
0.5
0.5
1.2
10.8
2.8
0.1
11.8
6.2
1.2
0.2
0.5
0.6
1.4
6.9
2.1
0.1
11.0
5.7
1.5
0.2
0.5
0.3
1.2
Whole head
Cheek meat
Head meat
Oxlips
Salivary glands
Skull
2.35
0.45
0.20
0.097
0.098
1.51
2.56
0.47
0.20
0.110
0.063
1.77
2.13
0.35
0.15
0.089
0.083
1.47
12.9
2.5
1.1
0.5
0.5
8.3
14.1
2.6
1.1
0.6
0.3
9.7
11.7
1.9
0.8
0.5
0.5
8.1
Whole tongue
Trimmed tongue
Tongue trim
Tongue meat
Gullet
Tongue bone
Tongue root muscle
0.78
0.39
0.21
0.026
0.096
0.018
0.042
0.75
0.36
0.19
0.051
0.105
0.018
0.029
0.71
0.35
0.23
0.012
0.078
0.015
0.027
4.3
2.1
1.2
0.14
0.5
0.10
0.23
4.1
2.0
1.0
0.28
0.6
0.10
0.16
3.9
1.9
1.3
0.07
0.4
0.08
0.15
Blood
Hooves
Lungs
Small intestine
Spleen
Ear and lip trim
Large intestine
Trachea
Rufe fat
Final rail trim
Heart bone
Bile
2.48
1.76
0.85
2.29
0.20
0.24
4.31
0.12
0.95
0.95
0.006
0.066
2.93
1.78
1.1
2.71
0.24
0.23
5.15
0.28
1.3
0.24
0.005
0.096
2.62
1.79
0.92
1.99
0.20
0.24
4.09
0.13
0.85
0.52
0.007
0.075
13.6
9.7
4.7
12.6
1.1
1.3
23.7
0.7
5.2
5.2
0.03
0.4
16.1
9.8
6.1
14.9
1.3
1.3
28.3
1.5
7.2
1.3
0.03
0.5
14.4
9.8
5.1
10.9
1.1
1.3
22.5
0.7
4.7
2.9
0.04
0.4
Source: Percentages taken from Terry, C.A., Knapp, R.H., Edwards, J.W., et al., 1990. Yields of by-products from different cattle types. Journal of Animal Science 68,
42004205.
darker than typical and is not the color that consumers are
accustomed to).
Cattle By-Products
Parts of the animal's body that do not remain with the carcass
are collectively referred to as offal, and most of these items can
be useful by-products, some edible, others not. Hooves may be
used for dog treats and horns may be used as containers (such
as for gun powder, historically) or for decorations. Some items
that are made in part with inedible cattle by-products include
cosmetics, explosives, and numerous leather products. Edible
by-products include the heart, liver, pancreas, kidneys, stomach, tail, head, and several other components. Since recent
bovine spongiform encephalopathy (BSE, or mad cow disease)
Beef Cattle
Table 22
Table 24
Raw by-product
Principle use
Brains
Heart
Kidneys
Liver
Spleen (melt)
Sweetbreads (pancreas)
Tongue
Oxtails
Cheek and trimmings
Beef extract
Blood
Fats from cattle and calves
Variety meat
Variety meat
Variety meat
Variety meat
Variety meat
Variety meat
Variety meat
Soup stock
Sausage ingredient
Soups and bouillon
Sausage component
Shortening, candies, and chewing
gum
Stomach
Suckling calves
Beef (reticulum and rumen)
Intestines, small
Intestines, large (beef and pork)
Esophagus (weasand)
Bones
Source: Aberle, E.D., Forrest, J.C., Gerrard, D.E., Mills, E.W., 2001. Principles of Meat
Science, fourth ed. Dubuque, IA: Kendall/Hunt Publishing Company.
Table 23
veal calf
Variety meat
Protein (g)
Fat (g)
Calories
Brain
Heart
Kidney
Liver
Lung
Pancreas
Spleen
Thymus
Tongue
10.5
26.3
26.3
21.5
18.8
29.1
23.9
18.4
26.2
7.4
4.5
5.9
7.6
2.6
14.6
2.6
2.9
8.3
111
153
165
160
104
256
125
105
187
Source: Adapted from Romans, J.R., Costello, W.J., Carlson, C.W., Greaser, M.L.,
Jones, K.W., 2001. The Meat We Eat, fourteenth ed. Danville, IL: Interstate
Publishers, Inc.
17
18
Beef Cattle
Table 25
Blood
Cell culture laboratories: Bovine serum albumin provides a wide variety of macromolecular proteins, low molecular weight nutrients, carrier proteins for
water-insoluble components, and other compounds necessary for in vitro growth of cells, such as hormones and attachment factors. Serum adds
buffering capacity to the medium and binds or neutralizes toxic components in the growth milieu.
Home and industrial uses: Plywood adhesives, fertilizer, foam re extinguisher, and chemical xer for dyes
Fatty acids (derived from tallows)
General uses: Plastics, tires, candles, crayons, cosmetics, lubricants, soaps, fabric softeners, asphalt emulsiers, synthetic rubber, linoleum (metallic
stearate), PVC (calcium stearate), jet engine lubricants, carrier for pesticides and herbicides, wetting agents, dispersing agents, defoamers,
solubilizers, and viscosity modiers
Many specic examples (oleic acid, stearic acid, etc.) are used for specic purposes or products
Tallow (fats and oils derived from meat, bone, hooves, and horns)
Various industrial tallows used as lubricants and greases: Top White Tallow, All-Beef Packer Tallow, Extra Fancy Tallow, Fancy Tallow, Bleachable Fancy
Tallow, Prime Tallow, Special Tallow, No. 2 Tallow, A Tallow, Choice White Grease, and Yellow Grease
Collagen (derived from connective tissues and beef hides)
Numerous uses: Hemostats, vascular sealants, tissue sealants, orthopedic implant coatings, vascular implant coatings, articial skin, bone graft
substitutes, corneal shields, injectable collagen for plastic surgery, injectable collagen for incontinence treatment, meat casings, food additives,
articial dura maters, dental implants, wound dressings, antiadhesion barriers, platelet analyzer reagents, research reagents, antibiotic wound
dressing, and lacrimal plugs
Glycerin products (derived from tallows)
Glycerin derivatives: A wide range of pharmaceuticals, including cough syrups and lozenges, tranquilizers, eyewashes, contraceptive jellies and creams,
ear drops, poison ivy solutions, solvent for digitalis and intramuscular injection, sclerosing solutions for treatment of varicose veins and hemorrhoids,
suppositories, and gel capsules
Glycerol: Solvent, sweetener, dynamite, cosmetics, liquid soaps, candy, liqueurs, inks, lubricants, antifreeze mixtures, and culture nutrients for
antibiotics
Gelatin (derived from collagen)
Nonfood uses include cosmetics, industrial uses, photographic paper, and photograph development as an aid in binding for glues, adhesives, and
emulsion and as a binder in pills and suppositories
Source: Reproduced from Klinkenborg, V., 2001. Cow Parts. Discover Magazine (online). Available at: http://discovermagazine.com/2001/aug/featcow (accessed 14.01.12).
Table 26
Rank
Total cattle
Country
1
2
3
4
5
6
7
8
9
10
India
Brazil
China
USA
EU-27
Argentina
Colombia
Australia
Mexico
Russia
World
Calf crop
Numbera
323.7
197.6
104.3
90.8
86.2
49.6
30.9
28.5
20.1
19.7
1019.3
Country
India
Brazil
China
USA
EU-27
Argentina
Australia
Russia
Mexico
Colombia
World
Imports
Numbera
63.4
49.7
41.0
34.3
29.3
13.8
10.0
6.9
6.8
5.1
280.8
Exports
Country
Numberb
Country
Numberb
USA
Venezuela
Russia
China
Egypt
Canada
Japan
Mexico
Ukraine
Belarus
2256
616
138
115
95
56
14
10
3
2
Mexico
Canada
EU-27
Australia
Brazil
Colombia
USA
Uruguay
New Zealand
China
1539
825
769
620
512
299
191
75
42
28
World
3112
World
4878
Numbers for total cattle and calf crop are reported in millions.
Numbers for imports and exports are reported in thousands.
Source: Taken from USDA Foreign Agricultural Service Production, Supply and Distribution (PSD) online database. Available at: http://www.fas.usda.gov/psdonline/psdHome.aspx
(23.04.13).
b
Beef Cattle
Table 27
Rank
1
2
3
4
5
6
7
8
9
10
19
Top 10 rankings for beef production and trade amounts by country for year 2012
Total production
Domestic consumption
Imports
Exports
Country
Amount
Country
Amount
Country
Amount
Country
Amount
USA
Brazil
EU-27
China
India
Argentina
Australia
Mexico
Pakistan
Russia
World
11 855
9 307
7 765
5 540
3 460
2 620
2 152
1 820
1 400
1 380
57 170
USA
Brazil
EU-27
China
Argentina
Russia
India
Mexico
Pakistan
Japan
World
11 744
7 845
7 806
5 597
2 458
2 395
2 049
1 835
1 367
1 255
55 513
Russia
USA
Japan
South Korea
EU-27
Canada
Egypt
Hong Kong
Venezuela
Mexico
World
1023
1007
737
370
348
301
250
241
220
215
6683
Brazil
India
Australia
USA
New Zealand
Uruguay
Canada
EU-27
Paraguay
Mexico
World
1524
1411
1407
1114
517
355
335
307
251
200
8324
Note: Values are reported in millions of kg and are on carcass weight equivalent basis.
Source: Taken from the USDA Foreign Agricultural Service Production, Supply and Distribution (PSD) online database. Available at: http://www.fas.usda.gov/psdonline/psdHome.aspx
(accessed 23.04.13).
Summary
Beef cattle are very useful in a wide range of production environments globally to supply a wide array of products. The
weight and amount of muscle in beef cattle are important in
many cultures. In some cases, it is the older animals that are
utilized for beef after they have been utilized for draft purposes; however, it has been the assumption throughout this
article that production of cattle for beef carcass markets is a
primary goal. This article has not discussed many specic
considerations involved in beef cattle production but has attempted to point out unique aspects of beef cattle production
that might be different in other livestock species. General
See also: Air: Conned Animal Facilities and Air Quality Issues.
Animal Health: Ectoparasites. Animal Health: Global Antibiotic
Issues. Animal Welfare: Stress, Global Issues, and Perspectives.
Breeding: Animals. Climate Change: Animal Systems. Critical
Tracking Events Approach to Food Traceability. Domestication of
Animals. Food Chain: Farm to Market. Forage Crops. Genomics of
Food Animals. International Trade. Production Economics. Vaccines
and Vaccination Practices: Key to Sustainable Animal Production.
Zoonotic Helminths of Livestock
References
Barth, A.D., 2000. Bull Breeding Soundness Evaluation, second ed. Alberta: Western
Canadian Association of Bovine Practioners Lacombe.
BIF, 2010. Utilization. In: Cundiff, L.V., Van Vleck, L.D., Hohenboken, W.D. (Eds.),
Guidelines for Uniform Beef Improvement Programs, ninth ed. Raleigh, NC, USA:
Beef Improvement Federation, pp. 183. (Chapter6). Available at: www.
beemprovement.org (accessed 30.07.12)
Gerber, P.J., Steinfeld, H., Henderson, B., et al., 2013. Tackling Climate
Change Through Livestock A Global Assessment of Emissions and
Mitigation Opportunities. Rome: Food and Agriculture Organization of the United
Nations (FAO).
Hamilton, D., 2004. Chapter 37: Waste Management in Beef Cattle Manual, fourth
ed., E-913. Stillwater, OK, USA: Oklahoma Cooperative Extension Service,
Oklahoma State University System.
McGowan, M., Galloway, D., Taylor, E., Entwistle, K., Johnston, P., 1995. The
Veterinary Examination of Bulls. Indooroopilly, QLD: Australian Association of
Cattle Veterinarians.
Porter, V., 1991. Cattle: A Handbook to the Breeds of the World. New York, NY:
Facts on File, Inc.
Romans, J.R., Costello, W.J., Carlson, C.W., Greaser, M.L., Jones, K.W., 2001. The
Meat We Eat, fourteenth ed. Danville, IL: Interstate Publishers, Inc.
20
Beef Cattle
Relevant Websites
http://www.agribenchmark.org/home.html
Agri Benchmark.
https://www.cia.gov/library/publications/the-world-factbook/
CIA World Factbook.
http://www.codexalimentarius.org/
Codex Alimentarius Commission.
http://epp.eurostat.ec.europa.eu/portal/page/portal/eurostat/home/
Eurostat Searchable Databases.
http://www.nbin.umn.edu/
FINBIN.
http://www.fao.org
Food and Agriculture Organization of the United Nations.
http://www.growsafe.com/
GrowSafe Systems, Ltd.
http://www.ilri.org/
International Livestock Research Institute (ILRI).
http://www.merckmanuals.com/vet/index.html
Merck Veterinary Manual.
http://www.ansi.okstate.edu/breeds/
Oklahoma State University Breeds of Livestock.
http://www.onehealthinitiative.com/
One Health Initiative.
http://www.sexingtechnologies.com/
Sexing Technologies, Inc.
http://transova.com/
Trans Ova Genetics.
http://www.fas.usda.gov/
United States Department of Agriculture Foreign Agricultural Service.
http://extension.usu.edu/behave/
Utah State University Extension Service.
http://www.oie.int/
World Organisation for Animal Health (OIE).
Glossary
Agroecology The application of ecological concepts and
principles to the design and management of sustainable
agroecosystems.
Agroecosystems Agricultural ecosystems including
biophysical and human components and their interactions.
Biodiversity The variation of life in all forms from genes,
to species, to communities, to whole ecosystems.
Ecosystem service providers Organisms, guilds, and
ecological communities that are biological mediators of
ecosystem services, providing services through their
functions and interactions.
Ecosystem services Functions of ecosystems including
agroecosystems that are useful to humans or support
human well-being: (1) provisioning services include the
production of food, fuel, ber, and other harvestable goods;
(2) regulating services include climate regulation, ood
control, disease control, waste decomposition, and water
quality regulation; (3) supporting services include the
foundational processes necessary for production of other
services, including soil formation, nutrient cycling, and
photosynthesis (primary production); and (4) cultural
Introduction
Historically, agricultural systems have been managed, above
all, for the production of food and ber; however, agricultural
landscapes can provide a wide range of goods and services to
society. Ecosystem services are those functions of ecosystems
including agroecosystems that are useful to humans
or support human well-being (Daily, 1997; Kremen, 2005).
The ecosystem services concept is remarkably longstanding.
Mooney and Ehrlich (1997) noted that in approximately 400
BC, Plato observed how forests provided important services to
Attica and forest loss resulted in drying springs and soil erosion. Plato's work highlights that people have been aware
of these critical services long before the dawn of industrial
agriculture (Rapidel et al., 2011).
In the past two decades, work at the interface of ecology
and economics to characterize, value, and manage ecosystem
services has supported a paradigm shift in how society thinks
about ecosystems and human relationships to them. As both
major providers and major beneciaries of ecosystem services,
agricultural landscapes and the people within them are at the
center of this shift. Growing calls for agriculture landscapes to
be managed as multifunctional systems create new mandates,
as well as opportunities, to maintain and enhance ecosystem
services as part of productive agroecosystems.
Work on multifunctional ecosystems draws on the Millennium Ecosystem Assessment (2005) and other recent evaluations of ecosystem services (e.g., The Economics of Ecosystems
and Biodiversity and The Common International Classication
of Ecosystem Services). The Millennium Ecosystem Assessment
provides a globally recognized classication that emphasizes
relationships between ecosystem services and human wellbeing and describes four types of services (The authors draw
on the classication of ecosystems services used in Millennium
Ecosystem Assessment throughout the article (MEA, 2005),
recognizing that more recent classications have minimized
or eliminated supporting services in favor of specic, operational descriptions designed for environmental accounting
(Haines-Young and Potschin, 2012) and economic valuation
(TEEB, 2010)). Provisioning services include the production
of food, fuel, ber, and other harvestable goods. Regulating
services include climate regulation, ood control, disease
control, waste decomposition, and water quality regulation.
Supporting services include the foundational processes necessary for production of other services, including soil formation,
nutrient cycling, and photosynthesis (primary production).
Cultural services provide recreational, esthetic, spiritual, and
other nonmaterial benets. Most classications, despite their
variations, consider interdependence between ecosystem services and human well-being as well as variation in ecosystem
doi:10.1016/B978-0-444-52512-3.00013-9
21
22
control through the effects of large root and mycorrhizal networks holding soil in place (Balvanera et al., 2006). It is also
important to note that some ecosystem services are provided in
part by the abiotic (nonliving) components of ecosystems, such
as aquifers and inorganic portions of soils. Biodiversity can be
considered a form of biological insurance that helps to assure
ecosystem performance, including providing ecosystem services, as diversity increases the chances that one or more species
will be able to perform critical functions, even in the event of
disturbance or species loss (e.g., natural disaster and humaninduced land use change) (Naeem and Li, 1997).
Agroecosystems both provide and rely on ecosystem
services to sustain production of food, ber, and other
Global
Regional
Local
Human well-being
Basic materials and conditions necessary
for a good life
Human
activities
Photosynthesis
Biogeochemical cycling
Provisioning
Goods and products obtained from an ecosystem
Food, fuel, fiber
Biochemicals
Genetic resources
Regulating
Benefits obtained from regulation of ecosystem
processes
Carbon sequestration
Pollination, pest control
carbon sequestration climate regulation
water purification
Cultural
Soil formation
Supporting
Ecosystem services
Biodiversity
Figure 1 Typology of ecosystem services. This ecosystem service typology, adapted from the Millennium Ecosystem Assessment (MEA, 2005),
considers biodiversity as a foundation for all ecosystem services (represented with a dotted line framing ecosystem services). Ecosystem services
include provisioning, regulating, and cultural services (dark gray boxes, solid outline), as well as supporting services (light gray box, dashed
outline). Ecosystem services support human well-being (charcoal gray box, white text), and, in turn, are inuenced by human activities and landuse management decisions. Both ecosystem services and human well-being can be considered at nested spatial scales from local, to regional, to
global.
23
Ecosystem service descriptions and related on-farm benets and public, off-farm benets
Ecosystem service
Description
On-farm benets
Erosion protection
Pollination
Pest control
Weed control
Carbon sequestration
Genetic resources
On-farm carbon sequestration can be associated with on-farm benets in closely related ecosystem services, such as increased soil organic matter and microclimate regulation
(e.g., shade provided by trees).
24
Services to agriculture
Services from agriculture
Genetic resources
Provisioning services:
Food, fuel, fiber
biochemicals
Hydrologic services
Water flow regulation
Water purification
Pest control
Agroecosystems
Pollination
Carbon sequestration
Soil conservation
Cultural and aesthetic services
Habitat provision
Disservices to agriculture
Pest damage
Pathogen outbreaks
Habitat degradation/loss
Competition for:
Water
Nutrients
Pollination
Soil degradation/loss
Water quality degradation/loss
Other off-site, negative impacts
Feedback
Figure 2 Ecosystem services and disservices to and from agriculture Farming systems can be both producers and beneciaries of ecosystem
services, and in many cases these relationships are deliberately managed by farmers. Such ecosystem services are represented by two gray boxes
in the diagram. Production systems can also suffer from various disservices or contribute to disservices or loss of services. These negative
relationships are usually the unintentional result of management action, represented by the two lower gray boxes and the dashed arrows.
Disservices from agriculture can also lead to agricultural inputs and result in detrimental on-farm impacts, such as when habitat for natural
enemies is removed and pest outbreaks increase, represented by the feedback arrow at the bottom of the diagram. Adapted from Zhang, W.,
Ricketts, T., Kremen C., et al., 2007. Ecosystem services and dis-services to agriculture. Ecological Economics 64, 253260 and Swinton, S., Lupi,
F., Robertson, G., Hamilton, S., 2007. Ecosystem services and agriculture: Cultivating agricultural ecosystems for diverse benets. Ecological
Economics 64, 245252.
25
Pollination
Animal pollinators are essential for approximately 35% of
global crop production, and 6090% of all plant species are
pollinator-dependent (Klein et al., 2007). Bees are recognized
as the taxon providing most pollination services, yet other
taxa including birds, bats, thrips, butteries and moths, ies,
wasps, and beetles also pollinate some of the world's most
important food crops (Nabhan and Buchmann, 1997). Pollination is necessary for sexual reproduction in many crops,
including fruits, vegetables, nuts, and seeds (Klein et al., 2007)
as well as many wild plants known to contribute calories and
micronutrients to human diets (Sundriyal and Sundriyal,
2004). There are also many globally important crops that are
pollinated passively or by wind, including cereals, sugarcane,
and grasses (Klein et al., 2007).
Overall, pollinators play a signicant role in the world's
food systems and agricultural economies. The estimated value
of insect-pollinated crops in the United States ranged from US
$1827 billion in 2003. If calculations include secondary
products, such as beef and milk from cattle fed alfalfa, the
estimated value more than doubles (Mader et al., 2011). Although honey bees (Apis spp.) are the most important commercially managed pollinator, native and wild bee species
also make signicant contributions. Approximately 15% of
the value associated with pollination services comes from
native bees and other animals living in farmlands and adjacent
natural habitat (Mader et al., 2011). Both agricultural management and landscape conguration are important in determining availability and distribution of pollination services.
Some wild (native) pollinators nest within elds, including
ground-nesting bees, or disperse from nearby unmanaged
habitats to pollinate crops (Ricketts et al., 2004). Conserving
wild pollinators in unmanaged or restored natural habitats
adjacent to agricultural elds can improve pollination levels
and stability, which can support increases in agricultural yields
(Klein et al., 2003).
The potential contributions of native pollinators have
received a great deal of recent attention due to global declines
in managed honey bee colonies (National Academies, 2006).
Declines in honey bee abundance, driven by establishment of
parasitic mites (e.g., Varroa destructor), hive pests, and social
factors such as aging beekeeper populations, have resulted in
pollination shortages in some areas (Klein et al., 2007). This
has caused increased prices for honey bee rental and created
concern about pollination shortfalls, such as those seen in
California almonds (National Academies, 2006). These factors
have heightened interest in the role of native pollinators to
help assure availability and stability of crop pollination services. Recommendations for managing pollinator-friendly
landscapes include maintaining areas of natural and seminatural perennial habitat (e.g., grass and woodlands, forests,
26
Pest control
Pest damage is a major limiting factor for global food production. Animal pests destroy 815% of global wheat, rice,
maize, potato, soybean, and cotton production (Oerke, 2005)
and cause more than US$30 billion in damage in the United
States each year (Pimentel et al., 2005). However, despite
dramatic increases in pesticide application, damage levels remained roughly unchanged during the four decades following
the escalation of pesticide use after World War II (Pimentel
et al., 1992; Oerke, 2005). Pesticides have even precipitated
pest outbreaks. For instance, Southeast Asian rice elds were
devastated by the brown planthopper (Nilaparvata lugens) after
excessive pesticide application caused the pest to evolve resistance while its predators continued to suffer high mortality
(Kenmore et al., 1984). In Indonesia, planthopper outbreaks
abated once many pesticides were banned (Naylor and
Ehrlich, 1997). Instead, farmers adopted an integrated pest
management approach in which natural pest predators were
fostered, and pesticides were used only after damage exceeded
critical economic thresholds.
The idea that farmers can harness nature to provide pest
control benets is not new. As early as AD 304, Chinese farmers
created and maintained citrus ant (Oecophylla smaragdina) nests
in their orchards to control pest outbreaks (Huang and Pei,
1987). Centuries later, in 1888, the modern concept of classic
biological control emerged, again in citrus orchards, when
introduced vedalia beetles (Rodolia cardinalis) caused the near
complete collapse of cottony-cushion scale (Icerya purchasi)
pests in California (Caltagirone and Doutt, 1989). Since then it
has become widely recognized that adjusting agricultural
practices to benet pest predators can provide a valuable pest
control strategy with signicant benet to farmers.
Strategies for enhancing pest control services to agriculture
may require understanding predator ecology to ensure that
pest predators have suitable food and habitat resources
throughout their life cycles (Landis et al., 2000). Plants that
provide oral or nectar resources can be used to sustain
predators and parasitoids. Sweet alyssum (Lobularia maritima)
has proven especially effective for bolstering syrphid y
abundances in California (Tillman et al., 2012). Predator
populations can also be enhanced indirectly through agricultural practices that increase nonpest prey, for example, by
applying mulch or intercropping (Riechert and Bishop, 1990;
Bugg et al., 1991). Small patches of native vegetation on
and around farms can provide these species with food resources and overwintering habitat (Landis et al., 2000; Tillman
et al., 2012). Emerging evidence suggests that conservation
activities at a landscape scale can also benet farmers. For
example, conserving natural habitat surrounding farms increases predators and often enhances pest control services
(Thies and Tscharntke, 1999; Bianchi et al., 2006; ChaplinKramer et al., 2011b; Karp et al., 2013). These examples represent but a few of many techniques that have emerged for
controlling crop pests with native predators, many of which
are readily accessible to farmers through government, university, and agency extension programs.
27
breeders, thereby increasing the vulnerability of crops to sudden environmental changes (Esquinas-Alczar, 2005).
28
29
Table 2
Ecosystem services and disservices to agriculture, the scales over which they are typically provided, and organism, guilds, and
communities that provide them
Organisms, guilds, and communities that provide services at the following scales:
Field
Farm
Landscape
Region/globe
Riparian vegetation;
vegetative cover on steep
areas, thin soils;
oodplains
Riparian vegetation;
vegetative cover on steep
areas, thin soils;
oodplains
Flowering weeds
Services to agriculture
Genetic resources
Weed control
Pollination
Disservices to agriculture
Pest damage and pathogen
outbreaks
Predators, parasites
(animals and insects,
including vertebrates,
invertebrates, and
parasitoids)
Predators, competitors
(herbivores, seed
predators, and other
competitors that limit
plants and fungi)
Pollinators: primarily bees
but also bats, thrips,
butteries and moths,
ies, wasps, beetles, and
birds (note: some crops
are wind-pollinated)
Microbes, micro and macro
invertebrates, nitrogenxing plants
Vegetation in watersheds
Flowering plants in
watershed
Source: Adapted from Zhang, W., Ricketts, T., Kremen, C., et al., 2007. Ecosystem services and dis-services to agriculture. Ecological Economics 64, 253260.
Many ecological studies aim to understand which populations, species, functional groups, guilds, food webs, and
habitat types produce key services. One method to do so is
a functional inventory, which includes identifying and describing the focal ecosystem service providers in a landscape
and quantifying their contributions (Kremen and Ostfeld,
2005). A functional inventory is most relevant at the scale
of the focal ecosystem service. Thus, evaluating disease resistance in crops may require a functional inventory at
the genetic level, (Zhu et al., 2000) whereas evaluating
biological control of pests may require an inventory at the
30
Functional Differences
A second method to build understanding of ecosystem service
providers is evaluating functional attribute diversity (Kremen
and Ostfeld, 2005). This method describes differences within
the guild, functional group, or community that provides each
service. A commonly used metric is ecological distance, which
describes differences in morphology, ecology, or behavior of
the organisms (Lalibert and Legendre, 2010; Walker et al.,
1999) that provide ecosystem services. Characteristics that
determine how an organism performs key functions are often
used for measuring ecological distance, such as root depth of
plants (potential determinant of water ow regulation), timing of emergence and senescence (primary production and
nutrient cycling), or pollinator's tongue length (pollination).
Response to Disturbance
Comprehensive evaluation of the abundance of ecosystem
services providers, and broader patterns of ecosystem services
availability, can build a solid foundation for investigating
potential inuence of disturbance. For example, what happens
when species that provide key services are lost? Sometimes
ecosystem services are resilient to disturbance and loss. If remaining species can compensate for the species that are removed or have become extinct, ecosystem services may also be
maintained rather than diminished. This compensation effect
can happen in several ways.
First, compensation can occur through response diversity,
described as the diversity of responses to change shown among
species contributing to the same ecosystem functions and
services disturbance (Elmqvist et al., 2003). Second, it can
occur through functional compensation, which occurs when
efciencies of individual ecosystem service providers shift in
response to changing community composition. Third, compensation may also happen through the portfolio effect. Just as
having a diverse investment portfolio may buffer an investor
against uctuations in individual investments, a diverse biological community is more likely to contain some species that
can persist through disturbances (Tilman et al., 1998).
31
Conservation agriculture
Ecosystem services
Yield
Legend
Ecosystem services
Pest control
Weed control
C sequestration
>50% of
comparisons
Habitat provision
Soil fertility
2550% of
comparisons
Erosion control
Water purification
Yield
>25% of
comparisons
Figure 3 Synergies and trade-offs between ecosystem services and yield in conservation agriculture and system of rice intensication. Bubble
location indicates the specic combination of outcomes for ecosystem services (Y-axis: enhanced, upper quadrants; diminished, lower quadrants)
and yield (X-axis: enhanced, right quadrants; diminished, left quadrants) relative to comparison systems. Bubbles located on the axis indicate no
signicant difference from the comparison system. Bubble size indicates the percent of reviewed comparisons reporting each combination of yield
and AEI outcomes: large bubbles indicate 450% of comparisons; medium bubbles indicate 2550% of comparisons; and small bubbles indicate
o25% of comparisons. The ecosystem services evaluated are represented by colored charts in each bubble and represented as the percentage of
comparisons in which the ecosystem service was measured. Adapted from Garbach, K., Milder, J.C., DeClerck, F., et al., in press. Closing yield
gaps and nature gaps: Multi-functionality in ve systems of agroecological intensication. Proceedings of the National Academy of Sciences-Plus.
Landscape Context
From above, agricultural landscapes often resemble a patchwork of rural villages, natural and seminatural habitat, and
farms cultivating a diverse array of crops. Natural habitat
in this context describes the full range of natural, seminatural,
and weedy vegetation types that tend to be present in
32
Pollination
Although managed honey bees (Apis mellifera) provide most
pollination globally, native insects are often more effective
pollinators and provide complementary pollination benets
(Garibaldi et al., 2013). Further, native insects enhance pollination resilience, especially as honey bee colonies continue
to collapse (Winfree and Kremen, 2009). Retaining a diverse
pollinator community is thus increasingly recognized as an
essential component of any sustainable food system.
Unsurprisingly, native pollinators rely on native habitat.
Many species center their foraging activity around the nest,
often located in patches of habitat embedded in agricultural
landscapes (Lonsdorf et al., 2009; Jha and Kremen, 2013).
Pollinator activity matches pollinator foraging ranges, and
pollination is thus consistently higher at the edges of crop
elds near native habitat than in the interior of large crop
monocultures (Kremen et al., 2004; Ricketts et al., 2004, 2008;
Klein et al., 2012). As large elds of a single crop variety replace more diversied farms, the total length of time during
which crop species are owering becomes shorter. As a result,
pollinators may become increasingly dependent on the wild
plants that ower throughout the year in noncropped areas
(Mandelik et al., 2012). Pollination services are thus not only
higher but also more stable at eld edges than in the interior
(Garibaldi et al., 2011).
Although pollination services may vary from crop to crop,
pollinator to pollinator, and region to region, the positive
inuence of natural habitat on pollinator activity has proven
remarkably consistent across many studies (Ricketts et al.,
2008). This consistency has allowed researchers to create
spatial pollination models that estimate pollination provision
on the farm based on the composition of the surrounding
landscape (Lonsdorf et al., 2009). For instance, the InVEST, the
ecosystem service modeling platform operated by the Natural
Capital Project, allows land managers to predict the pollination consequences of their land-use decisions and manage
land assets accordingly.
Pest Control
Not all crops are animal pollinated, but every crop suffers pest
damage. The shift from diversied, agricultural landscapes
with patches of natural habitat to large monocultures that lack
natural habitat has likely brought with it more severe pest
outbreaks. High vegetation diversity ensures that specialist
pests do not enjoy vast food resources (Matson et al., 1997).
Further, because not all crops and vegetation in natural habitat
is palatable to pests, complex landscapes may inhibit pest
movements and cause more localized outbreaks (Avelino et al.,
2012). However, natural habitat can sometimes provide pests
with resources vital for completing their lifecycles and thus
facilitate outbreaks (Chaplin-Kramer et al., 2011b). For example, because aphids sequester chemicals in wild mustards
(Brassica nigra) as antipredator defenses, the proximity of
natural habitat with high mustard density may function to
increase the density of aphids in nearby crop elds (ChaplinKramer et al., 2011a).
Another critical consideration, however, is the predators
of crop pests. Predators rely on natural habitat for essential
activities, including breeding, roosting, foraging, and hibernating (Landis et al., 2000; Jirinec et al., 2011). Predator
abundance and diversity thus regularly decline as agricultural
landscapes shift from complex mosaics of natural habitat and
cropland to simplied monocultures (Bianchi et al., 2006;
Chaplin-Kramer et al., 2011b). Although diverse predator
communities are not always more effective at providing pest
control because predators sometimes consume each other
(Vance-Chalcraft et al., 2007), most studies report that more
predator diversity translates to more effective pest control
(Bianchi et al., 2006; Letourneau et al., 2009; Chaplin-Kramer
et al., 2011b).
An increasing number of studies have documented increased pest consumption in complex versus simple landscapes
(Thies and Tscharntke, 1999; Gardiner et al., 2009; ChaplinKramer and Kremen, 2013; Karp et al., 2013). Fewer studies,
however, have traced the benet of maintaining natural habitat
all the way to crop yields and prots, but some have reported
positive effects (Thies and Tscharntke, 1999; Karp et al.,
2013). Like pollination, the relevant scale for pest management can vary from predator to predator and from pest to
pest, such that distant areas may determine the abundance
of highly mobile animals (Werling and Gratton, 2010). Simply focusing on local agricultural practices may be ineffective.
Because predator communities often collapse after harvest,
a stream of colonizers from adjacent natural habitat may
be required to replenish the predator community in the
following year.
33
0.25
km
2370 kg Berries saved
0 kg Berries saved
N
Coffee
1.5
km
Pasture
Figure 4 Pest control value of forest patches to coffee plantations in Southern Costa Rica forest provides habitat for the insectivorous birds that
consume the coffee berry borer beetle (Hypothenemus hampei), coffee's most economically damaging insect pest. Maps show the estimated
kilograms of coffee berries saved from infestation by each patch of forest across the Coto Brus Valley. Integrated together, the small, unprotected
forest patches embedded within or adjacent to coffee plantations provided the majority of pest control value to coffee farmers.
34
Government Regulation
Agriculture in most countries is a relatively lightly regulated
enterprise when compared with other land uses, such as
industrial facilities, mines, urban development, and even
Market-Based Instruments
In the context of policy options, the term market-based is
used broadly to refer to strategies that seek to inuence behavior by adjusting the price signals to various market actors,
including farmers, corporations, and consumers. Such instruments are often intended to remedy market failures that can
occur when the providers of ecosystem services do not reap the
full benet of delivering these services, or when they avoid
bearing the full cost when they diminish these services. For
instance, farmers usually receive little or no monetary benet
from protecting wildlife habitat, although this is an important
35
Table 3
Typology of policies, programs, and instruments that may be used to conserve and enhance ecosystem services from agricultural
landscapes
Type of policy, program, or
instrument
Role of farmers
Examples
Subject of regulations
Regulation of agricultural
inputs
Regulation of other
agricultural practices
Other regulations affecting
agricultural lands
Market-based instruments (inuencing price signals or incentive structures)
Taxes and subsidies
High (establish tax and
Payer of taxes or recipient of
subsidy policies)
subsidies
Note: Some of these instruments also serve additional aims or are not always used to manage ecosystem services in agricultural landscapes. The abbreviation PES stands for payment
for ecosystem services.
of ecosystem services. For instance, in Kazakhstan, the government in 2008 began subsidizing farmers to adopt conservation
agriculture technologies including continuous soil cover, direct
seeding, and no-till management that are credited with helping
to increase farmer yields and protability while reducing soil
erosion.
PES are abroad set of market-based instruments that have
proliferated since the mid-1990s to channel new investment in
ecosystem services. Formally, PES has been dened as voluntary transactions between ecosystem service seller(s) (such as
farmers or other land managers) and ecosystem service buyer
(s) (such as water users or conservation organizations) that
provide cash or other payment in exchange for the provision
of specic dened ecosystem services (Engel et al., 2008). In
practice, however, many PES schemes do not conform to this
denition, for instance, because they do not target specic
36
Knowledge Gaps
Although scientic understanding of ecosystem services and
their biological mediators in agricultural landscapes has grown
dramatically in the past couple of decades, several critical
knowledge gaps remain.
First, there is a need to develop mechanistic understanding
of the organisms, guilds, and ecological communities that
provide ecosystem services (Kremen and Ostfeld, 2005; Kremen, 2005). Identifying key ecosystem service providers and
understanding their requirements for performing the biological functions that underpin service delivery are essential for
effective management of agroecosystems that deliver both
sustained crop yield and ecosystem services. However, to date,
these biological requirements are known for only a small
subset of key ecosystem service providers (e.g., area requirements for pollination by native bees; Kremen et al., 2004).
Second, there are relatively few studies that examine quantitative measures of yield and ecosystem services in the same
system (Milder et al., 2012). For instance, although recent
metareviews have included 300 or more comparisons of yield
effects relative to conventional systems (e.g., Seufert et al.,
2012), relatively few studies provide rigorous data on paired
outcomes for yield as well as ecosystem services. A third
knowledge gap is the lack of studies that link management
practices to ecosystem service outcomes at multiple scales.
Measuring the spatial and temporal scales over which ecosystem service providers deliver key services is imperative to
addressing this gap (Kremen and Ostfeld, 2005). Specically,
building understanding of how ecosystem functions are inuenced by the species and communities within an area is
needed to understand how their attributes and services can
aggregate at different scales from cultivated elds to broader
regions, including cultivated and noncultivated areas.
Addressing these knowledge gaps is essential to designing
and managing multifunctional agroecosystems. Continued
work on this front is needed to answer the growing call for
agricultural landscapes that can simultaneously meet production and conservation goals.
References
Africare, Oxfam America, WWF-ICRISAT, 2010. More Rice for People, More Water
for the Planet. Hyderabad, India: WWF-ICRISAT.
37
38
Farley, K.A., Jobbgy, E.G., Jackson, R.B., 2005. Effects of afforestation on water
yield: A global synthesis with implications for policy. Global Change Biology 11,
15651576.
Fisher, B., Edwards, D.P., Giam, X., Wilcove, D.S., 2011. The high costs of
conserving Southeast Asia's lowland rainforests. Frontiers in Ecology and the
Environment 9, 329334.
Foley, J.A., DeFries, R., Asner, G.P., et al., 2005. Global consequences of land use.
Science 309, 570.
Free, J.B., 1993. Insect Pollination of Crops. London, U.K: Academic Press.
Gabriel, D., Sait, S.M., Hodgson, J.A., et al., 2010. Scale matters: The impact of
organic farming on biodiversity at different spatial scales. Ecology Letters 13,
858869.
Garbach, K., Lubell, M., DeClerck, F.A., 2012. Payment for ecosystem services: The
roles of positive incentives and information sharing in stimulating adoption of
silvopastoral conservation practices. Agriculture, Ecosystems and Environment
156, 2736.
Garbach, K., Milder, J.C., DeClerck, F., et al., in press. Closing yield gaps and
nature gaps: Multi-functionality in ve systems of agroecological intensication.
Proceedings of the National Academy of Sciences-Plus.
Gardiner, M.M., Landis, D.A., Gratton, C., et al., 2009. Landscape diversity enhances
biological control of an introduced crop pest in the north-central USA. Ecological
Applications 19, 143154.
Garibaldi, L.A., 2011. Stability of pollination services decreases with isolation from
natural areas despite honey bee visits. Ecology Letters 14, 10621072.
Garibaldi, L.A., 2013. Wild pollinators enhance fruit set of crops regardless of honey
bee abundance. Science 339, 16081611.
Gennet, S., Howard, J., Langholz, J., et al., 2013. Farm practices for food safety: An
emerging threat to oodplain and riparian ecosystems. Frontiers in Ecology and
the Environment 11, 236242.
Gliessman, S., Engles, E.W., Krieger, R., 1998. Agroecology: Ecological Processes in
Sustainable Agriculture. Boca Raton, FL: CRC Press.
Godfray, H.C.J., Beddington, J.R., Crute, I.R., et al., 2010. Food security: The
challenge of feeding 9 billion people. Science 327, 812818.
de Groot, R.S., Wilson, M.A., Boumans, R.M., 2002. A typology for the
classication, description and valuation of ecosystem functions, goods and
services. Ecological Economics 41, 393408.
Haggblade, S., Tembo, G., 2003. Conservation farming in Zambia. Discussion paper
108. Washington, DC: International Food Policy Research Institute (IFPRI).
Haines-Young, R., Potschin, M. (Eds.), 2012. CICES (Common International
Classication System of Ecosystem Services). Consultation on Version 4,
AugustDecember 2012. Nottingham: Centre for Environmental Management,
University of Nottingham.
Harvey, C., Medina, A., Snchez, D., et al., 2006. Patterns of animal diversity in
different forms of tree cover in agricultural landscapes. Ecological Applications
16, 19861999.
Hawtin, G.C., 2000. Genetic diversity and food security. UNESCO Courier, May
2000, pp. 2729. Available at http://www.unesco.org/courier/2000_05/uk/doss23.
htm (accessed 15.01.14).
Hendrix, P.F., Crossley Jr., D.A., Blair, J.M., Coleman, D.C., 1990. Soil biota as
components of sustainable agroecosystems. In: Edwards, C.A., Lal, R., Madden,
P., Miller, R.H., House, G. (Eds.), Sustainable Agricultural Systems. Boca Raton,
FL: CRC Press, pp. 637654.
Heuperman, A.F., Kapoor, A.S., Denecke, H.W. (Eds.), 2002. Biodrainage
Principles, Experiences and Applications. Rome, Italy: Food and Agriculture
Organization of the United Nations.
Hooper, D., Chapin Iii, F., Ewel, J., et al., 2005. Effects of biodiversity on ecosystem
functioning: A consensus of current knowledge. Ecological Monographs 75, 335.
Huang, H.T., Pei, Y., 1987. The ancient cultured citrus ant. BioScience 37, 665671.
Jaipal, S., Malik, R.K., Hobbs, P., Yadav, A., Singh, S., 2005. Conservation
Agriculture-IPM issues. Conservation Agriculture: Status & Prospects. New Delhi,
India: Centre for Advancement of Sustainable Agriculture, National Agriculture
Science Centre.
Jha, S., Kremen, C., 2013. Resource diversity and landscape-level homogeneity
drive native bee foraging. Proceedings of the National Academy of Sciences 110,
555558.
Jirinec, V., Campos, B.R., Johnson, M.D., 2011. Roosting behaviour of a migratory
songbird on Jamaican coffee farms: Landscape composition may affect delivery
of an ecosystem service. Bird Conservation International 21, 353361.
Karp, D.S., Mendenhall, C.D., Sandi, R.F., et al., 2013. Forest bolsters bird
abundance, pest control, and coffee yield. Ecology Letters 16, 13391347.
Karp, D.S., Ziv, G., Zook, J., Ehrlich, P.R., Daily, G.C., 2011. Resilience and stability
in bird guilds across tropical countryside. Proceedings of the National Academy
of Sciences of the USA 108, 2113421139.
Kassam, A., Friedrich, T., Shaxson, F., Pretty, J., 2009. The spread of conservation
agriculture: Justication, sustainability and uptake. International Journal of
Agricultural Sustainability 7, 292320.
Kenmore, P.E., Cario, F.O., Perez, C.A., Dyck, V.A., Gutierezz, A.P., 1984. Population
regulation of the rice brown planthopper (Nilaparvata lugens Stal) within rice elds
in the Philippines. Journal of Plant Protection in the Tropics 1, 1937.
Klein, A.-M., Brittain, C., Hendrix, S.D., et al., 2012. Wild pollination services to
California almond rely on semi-natural habitat. Journal of Applied Ecology 49,
723732.
Klein, A.M., Steffan-Dewenter, I., Tscharntke, T., 2003. Fruit set of highland coffee
increases with the diversity of pollinating bees. Proceedings of the Royal Society
of London. Series B: Biological Sciences 270, 955961.
Klein, A.-M., Vaissiere, B.E., Cane, J.H., et al., 2007. Importance of pollinators in
changing landscapes for world crops. Proceedings of the Royal Society B:
Biological Sciences 274, 303313.
Kremen, C., 2005. Managing ecosystem services: What do we need to know about
their ecology? Ecology Letters 8, 468479.
Kremen, C., Miles, A., 2012. Ecosystem services in biologically diversied versus
conventional farming systems: Benets, externalities, and trade-offs. Ecology and
Society 17, 40.
Kremen, C., Ostfeld, R., 2005. A call to ecologists: Measuring, analyzing, and
managing ecosystem services. Frontiers in Ecology and the Environment 3,
540548.
Kremen, C., Williams, N., Aizen, M., et al., 2007. Pollination and other ecosystem
services produced by mobile organisms: A conceptual framework for the effects
of land-use change. Ecology Letters 10, 299314.
Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P., Thorp, R.W., 2004. The area
requirements of an ecosystem service: Crop pollination by native bee
communities in California. Ecology Letters 7, 11091119.
Kruess, A., Tscharntke, T., 1994. Habitat fragmentation, species loss, and biological
control. Science 264, 15811584.
Lalibert, E., Legendre, P., 2010. A distance-based framework for measuring
functional diversity from multiple traits. Ecology 91, 299305.
Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve
natural enemies of arthropod pests in agriculture. Annual Review of Entomology
45, 175201.
Lemos, M.C., Agrawal, A., 2006. Environmental governance. Annual Review of
Environment and Resources 31, 297325.
Letourneau, D.K., Jedlicka, J.A., Bothwell, S.G., Moreno, C.R., 2009. Effects of natural
enemy biodiversity on the suppression of arthropod herbivores in terrestrial
ecosystems. Annual Review of Ecology, Evolution, and Systematics 40, 573592.
Liverman, D., 2004. Who governs, at what scale and at what price? Geography,
environmental governance, and the commodication of nature. Annals of the
Association of American Geographers 94, 734738.
Lonsdorf, E., Kremen, C., Ricketts, T., et al., 2009. Modelling pollination services
across agricultural landscapes. Annals of Botany 103, 15891600.
Macedo, M.N., DeFries, R.S., Morton, D.C., et al., 2012. Decoupling of deforestation
and soy production in the southern Amazon during the late 2000s. Proceedings
of the National Academy of Sciences of the USA 109, 13411346.
Mader, E., Shepherd, M., Vaughan, M., Black, S.H., LeBuhn, G. (Eds.), 2011.
Attracting Native Pollinators: Protecting North America's Bees and Butteries.
Portland, OR: The Xerces Society Guide. Storey Publishing.
Majanen, T., Friedman, R., Milder, J.C., 2011. Innovations in market-based
watershed conservation in the United States: Payments for watershed services for
agricultural and forest landowners. Report prepared for U.S. Endowment for
Forestry and Communities, Inc. and US Department of Agriculture, Ofce of
Environmental Markets. Washington, DC: EcoAgriculture Partners
Mandelik, Y., Winfree, R., Neeson, T., Kremen, C., 2012. Complementary habitat use
by wild bees in agro-natural landscapes. Ecological Applications 22, 15351546.
Matson, P., Parton, W., Power, A., Swift, M., 1997. Agricultural intensication and
ecosystem properties. Science 277, 504509.
McDonald, A.J., Hobbs, P., Riha, S., 2006. Does the system of rice intensication
outperform conventional best management?: A synopsis of the empirical record.
Field Crops Research 96, 3136.
MEA (Millennium Ecosystem Assessment), 2005. Ecosystems and human well-being:
Our human planet. Summary for decision-makers. Millennium Ecosystem
Assessment. Washington, DC: Island Press.
Melo, F.P.L., Arroyo-Rodrguez, V., Fahrig, L., Martnez-Ramos, M., Tabarelli, M.,
2013. On the hope for biodiversity-friendly tropical landscapes. Trends in
Ecology and Evolution 28, 462468.
Mendenhall, C.D., Kappel, C., Ehrlich, P.R., 2013. Countryside biogeography. In:
Levin, S.A. (Ed.), Encyclopedia of Biodiversity, second ed. Wlatham, MA:
Academic Press, pp. 347360.
Mendenhall, C.D., Sekercioglu, C.H., Oviedo, F., Ehrlich, P.R., Daily, G.C., 2011.
Predictive model for sustaining biodiversity in tropical countryside. Proceedings
of the National Academy of Sciences of the USA 108, 1631316316.
Milder, J.C., Garbach, K., DeClerck, F.A.J., Montenegro, M., Driscoll, L., 2012. An
Assessment of the Multi-Functionality of Agroecological Intensication. Ithaca,
NY: EcoAgriculture Partners.
Milder, J.C., Scherr, S.J., Bracer, C., 2010. Trends and future potential of payment
for ecosystem services to alleviate rural poverty in developing countries. Ecology
and Society 15, 4.
Montagnini, F., Nair, P., 2004. Carbon sequestration: An underexploited
environmental benet of agroforestry systems. Agroforestry Systems 61,
281295.
Mooney, H.A., Ehrlich, P.R., 1997. Ecosystem services: A fragmentary history. In:
Daily, G.C. (Ed.), Nature's Services: Societal Dependence on Natural Ecosystems.
Washington, DC: Island Press, pp. 1119.
Muradian, R., Corbera, E., Pascual, U., Kosoy, N., May, P.H., 2010. Reconciling
theory and practice: An alternative conceptual framework for understanding
payments for environmental services. Ecological Economics 69, 12021208.
Nabhan, G.P., Buchmann, S.L., 1997. Services provided by pollinators. In: Daily, G.
C. (Ed.), Nature's Services: Societal Dependence on Natural Ecosystems.
Washington, DC: Island Press, pp. 133150.
Naeem, S., Li, S., 1997. Biodiversity enhances ecosystem reliability. Nature 390,
507509.
Naiman, R.J., Dcamps, H., 1997. The ecology of interfaces: Riparian zones. Annual
Review of Ecology and Systematics 28, 621658.
Narain, P., Kumar, P., 2005. Prospects and limitations of reduced tillage in arid
zone. In: Abrol, I.P., Gupta, R.K., Malik, R.K. (Eds.), Conservation Agriculture:
Status and Prospects. New Delhi, India: Centre for Advancement of Sustainable
Agriculture, National Agriculture Science Centre, pp. 191198.
National Academies, 2006. Status of Pollinators in North America. Washington, DC:
National Academy Press.
Naylor, R., Ehrlich, P.R., 1997. Natural pest control services and agriculture. In:
Daily, G.C. (Ed.), Nature's Services: Societal Dependence on Natural Ecosystems.
Washington DC: Island Press, pp. 151174.
Oerke, E.-C., 2005. Crop losses to pests. Journal of Agricultural Science 144,
3143.
Paul, E.A., Clark, F.E., 1996. Soil Microbiology and Biochemistry. New York, NY:
Academic Press.
Perfecto, I., Vandermeer, J.H., Wright, A., 2009. Nature's Matrix: Linking Agriculture,
Conservation, and Food Sovereignty. London: Cromwell Press Group.
Philpott, S.M., et al., 2008. Biodiversity loss in Latin American coffee landscapes:
Review of the evidence on ants, birds, and trees. Conservation Biology 22,
10931105.
Pimentel, D., Acquay, H., Biltonen, M., et al., 1992. Environmental and economic
costs of pesticide use. BioScience 42, 750760.
Pimentel, D., Zuniga, R., Morrison, D., 2005. Update on the environmental and
economic costs associated with alien-invasive species in the United States.
Ecological Economics 52, 273288.
Power, A.G., 2010. Ecosystem services and agriculture: Tradeoffs and synergies.
Philosophical Transactions of the Royal Society B: Biological Sciences 365,
29592971.
Pretty, J.N., Noble, A., Bossio, D., et al., 2006. Resource-conserving agriculture
increases yields in developing countries. Environmental Science and Technology
40, 11141119.
Ramankutty, N., Rhemtulla, J., 2012. Can intensive farming save nature? Frontiers in
Ecology and the Environment 10, 455.
Rapidel, B., DeClerck, F., Le Coq, J.-F., Beer, J., 2011.In: Rapidel, B., DeClerck, F.,
Le Coq, J.-F., Beer, J. (Eds.), Ecosystem Services from Agriculture and
Agroforestry: Measurement and Payment. London: Earthscan, pp. 115.
Ribaudo, M., Greene, C., Hansen, L., Hellerstein, D., 2010. Ecosystem services from
agriculture: Steps for expanding markets. Ecological Economics 69, 20852092.
Ricketts, T.H., et al., 2008. Landscape effects on crop pollination services: Are there
general patterns? Ecology Letters 11, 499515.
Ricketts, T.H., Daily, G.C., Ehrlich, P.R., Michener, C.D., 2004. Economic value of
tropical forest to coffee production. Proceedings of the National Academy of
Sciences of the USA 101, 1257912582.
Riechert, S.E., Bishop, L., 1990. Prey control by an assemblage of generalist
predators: Spiders in garden test systems. Ecology 71, 14411450.
Rockstrm, J., Steffen, W., Noone, K., et al., 2009. A safe operating space for
humanity. Nature 461, 472475.
Rost, S., Gerten, D., Hoff, H., et al., 2009. Global potential to increase crop
production through water management in rainfed agriculture. Environmental
Research Letters 4, 044002.
39
Snchez-Azofeifa, G.A., Pfaff, A., Robalino, J.A., Boomhower, J.P., 2007. Costa
Rica's payment for environmental services program: Intention, implementation,
and impact. Conservation Biology 21, 11651173.
Schiesari, L., Waichman, A., Brock, T., Adams, C., Grillitsch, B., 2013. Pesticide use
and biodiversity conservation in the Amazonian agricultural frontier. Philosophical
Transactions of the Royal Society B: Biological Sciences 368, 20120378.
Seufert, V., Ramankutty, N., Foley, J.A., 2012. Comparing the yields of organic and
conventional agriculture. Nature 485, 229232.
Shand, H., 1997. Human nature: Agricultural biodiversity and farm-based food
security. Report by the Rural Advancement Foundation International (RAFI) for the
Food and Agriculture Organization of the United Nations, Rome, Italy.
Staver, C., Guharay, F., Monterroso, D., Muschler, R.G., 2001. Designing pestsuppressive multistrata perennial crop systems: Shade-grown coffee in Central
America. Agroforestry Systems 53, 151170.
Sundriyal, M., Sundriyal, R., 2004. Wild edible plants of the Sikkim Himalaya:
Nutritive values of selected species. Economic Botany 55, 286299.
Swinton, S., Lupi, F., Robertson, G., Hamilton, S., 2007. Ecosystem services and
agriculture: Cultivating agricultural ecosystems for diverse benets. Ecological
Economics 64, 245252.
TEEB (The Economics of Ecosystems and Biodiversity), 2010. Mainstreaming the
economics of nature: A synthesis of the approach, conclusions and
recommendations of TEEB synthesized by P. Sukhdev and TEEB team. Malta:
Progress Press.
The Royal Society, 2009. Reaping the Benets: Science and the Sustainable
Intensication of Global Agriculture. London, UK: The Royal Society.
Thies, C., Tscharntke, T., 1999. Landscape structure and biological control in
agroecosystems. Science 285, 893895.
Tillman, P.G., Smith, H.A., Holland, J.M., 2012. Cover crops and related methods
for enhancing agricultural biodiversity and conservation biocontrol: Successful
case studies. In: Gurr, G.M., Wratten, S.D., Snyder, W.E., Read, D.M.Y. (Eds.),
Biodiversity and Insect Pests: Key Issues for Sustainable Management. New
York, NY: John Wiley & Sons, pp. 309327.
Tilman, D., 1999. Global environmental impacts of agricultural expansion: The need
for sustainable and efcient practices. Proceedings of the National Academy of
Sciences of the USA 96, 59956000.
Tilman, D., Lehman, C.L., Bristow, C.E., 1998. Diversity-stability relationships:
Statistical inevitability or ecological consequence? American Naturalist 151,
277282.
Tscharntke, T., Klein, A., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005.
Landscape perspectives on agricultural intensication and biodiversity-ecosystem
service management. Ecology Letters 8, 857874.
UNEP-WCMC (United Nations Environment Programme World Conservation
Monitoring Centre), 2011. Review of the Biodiversity Requirements of Standards
and Certication Schemes, Technical Series No. 63. Montreal: Secretariat of the
Convention on Biological Diversity.
UN Water (United Nations Water), 2013. Agriculture and Food Security. United
Nations, Rome, Italy. Available at: www.unwater.org/statistics (accessed
15.01.14).
USDA ERS (U.S. Department of Agriculture Economic Research Service), 2013. Farm
Practices, Management, and Irrigation Water Use, Washington, DC. Available at:
www.ers.usda.gov/topics/farm-practices-management/irrigation-water-use
(accessed 15.01.14).
Vance-Chalcraft, H.D., Rosenheim, J.A., Vonesh, J.R., Osenberg, C.W., Sih, A.,
2007. The inuence of intraguild predation on prey suppression and prey release:
A meta-analysis. Ecology 88, 26892696.
Van den Putte, A., Govers, G., Diels, J., Gillijns, K., Demuzere, M., 2010. Assessing
the effect of soil tillage on crop growth: A meta-regression analysis on European
crop yields under conservation agriculture. European Journal of Agronomy 33,
231241.
Von Randow, C., Manzi, A., Kruijt, B., et al., 2004. Comparative measurements
and seasonal variations in energy and carbon exchange over forest and
pasture in South West Amazonia. Theoretical and Applied Climatology
78, 526.
Walker, B., Kinzig, A., Langridge, J., 1999. Plant attribute diversity, resilience, and
ecosystem function: The nature and signicance of dominant and minor species.
Ecosystems 2, 95113.
Welbank, P., 1963. A comparison of competitive effects of some common weed
species. Annals of Applied Biology 51, 107125.
Werling, B.P., Gratton, C., 2010. Local and broadscale landscape structure
differentially impact predation of two potato pests. Ecological Applications 20,
11141125.
Weston, L.A., Duke, S.O., 2003. Weed and crop allelopathy. Critical Reviews in
Plant Sciences 22, 367389.
40
Winfree, R., Kremen, C., 2009. Are ecosystem services stabilized by differences
among species? A test using crop pollination. Proceedings of the Royal Society
B: Biological Sciences 276, 229237.
World Bank, 2008a. Agriculture for Development. Washington, DC: World Bank.
World Bank, 2008b. Sustainable Land Management Sourcebook. Washington, DC:
World Bank.
Zhang, W., Ricketts, T., Kremen, C., Carney, K., Swinton, S., 2007. Ecosystem
services and dis-services to agriculture. Ecological Economics 64, 253260.
Zhu, Y., Chen, H., Fan, J., et al., 2000. Genetic diversity and disease control in rice.
Nature 406, 718722.
Glossary
Biochory Passive, unintentional transport of spores, eggs,
microbial cells, or small animals by organisms that move in
the litter and soil, thereby promoting the dispersal of almost
immobile organisms.
Bioturbation Soil mixing carried out by organisms in
soils, mainly earthworms, termites, and ants, plus a few
Coleoptera, nymphal Cicadidae, Isopoda, or Grylotalpidae
(mole crickets). Bioturbation may be effected by ingesting
the soil and passing it through the animal gut (earthworms
and humivorous termites), or by constructing mounds,
digging galleries and chambers to accommodate colonies
and food reserves (ants and foraging and fungus-growing
termites). Roots also affect some degree of bioturbation
through creating holes that are further used by other
organisms as habitats and passageways for movement once
the root has died and disappeared.
Catena of soils A succession of soils arrayed down a slope,
with proles changing according to their topographic
position. The low-lying parts of the catena generally have a
higher moisture status and receive elements eluviated,
detached, and transported from the higher parts. The upper
parts of the catena may become depleted in clay and
nutrients by these processes.
Chemolithotrophy The ability to use energy obtained by
the oxidation of inorganic compounds.
Comminution The physical transformation of leaf and
root litter with limited chemical (digestive) decomposition.
This is an essential process in litter recycling whereby
large plant-derived structures, such as leaves, are
progressively fragmented into increasingly smaller pieces,
thereby increasing the surface area exposed to microbial
attack.
Drilosphere A word coined by Bouch (1972) that
describes the functional domain created within soil by
earthworms (drilos in Greek) and is analogous to the wellrecognized rhizosphere, the sphere of inuence of roots.
The drilosphere is thus the sum of earthworms and the
structures that they create in soil as casts, galleries, and pores
of different sizes and shapes, together with the communities
of smaller organisms, invertebrates, and microorganisms
that inhabit the habitats thus constructed. The earthworm
gut is the critical component of the drilosphere in which
earthworm digestion in conjunction with microorganism
activity provides the energy necessary to maintain this
structure.
Geophagous An organism that ingests soil. Endogeic
earthworms and humivorous termites are the main groups
doi:10.1016/B978-0-444-52512-3.00019-X
41
42
Introduction
The Green Revolution boosted agricultural production approximately 2.5 times and was associated with an approximately
40% price reduction in the cost of food (MA, 2005). Following
on the euphoria of this success there has been increasing pressure to diversify production and to improve the planets environment (Hubert et al., 2010). Successful realization of this
pressure will require better soil management. However, current
conditions are very different from what they were 50 years ago.
The success of the Green Revolution came at the expense of the
natural capital, such that 18 of the 24 currently acknowledged
ecosystem services have been impaired. Although soils have
aided climate regulation by sequestering an estimated 2 Gt
carbon (C) per annum from fossil fuel burning, they have lost
part of their capacity to regulate hydrological uxes and nutrient
cycles and therefore to support plant production.
The soils of the earth are now being asked to produce 70%
more food over the next 35 years, while also producing biofuels, regulating climate through further C sequestration, and
helping to conserve biodiversity. However, the other side of
this coin is the declining amount of land remaining available
for conversion to agroecosystems and the increased cost of
energy, which has led to a substantial increase in the price of
fertilizers. Further, world sources of phosphorus (P) are being
rapidly depleted and the toxic effects of pesticides are now
forcing the replacement of these former pillars of intensive
agriculture with new technical options.
Agriculture now needs to sustain high levels of production
while preserving or restoring the natural capital of the soil.
Maintenance of an appropriate level of soil biodiversity is
critical to achieving this goal, but in order to protect the soil
resource and optimize its long-term use, new land use practices are needed to be developed, based on much greater
understanding of the factors controlling its functioning.
This article summarizes the current knowledge of the
composition and taxonomic richness of the soil biota. It then
examines the participation of the soil biota in the major soil
functions and discusses ways to reconcile the conservation
and/or improvement of this natural capital with the production of critical ecosystem goods and services.
Mesofauna
Microflora/microfauna
100 m
Bacteria
43
2 mm
Fungi
Nmatoda
Protozoa
Acari
Collembola
Diplura
Symphyla
Enchytraedae
Isoptera / formicoidea
Diptera
Isopoda
Myriapoda
Arachnida
Coleoptera
Mollusca
Oligochaeta
Vertebrata
1
16
32
16
32
mm
Body size
Figure 1 Representation of the main taxonomic groups of soil organisms on a body size basis. Reproduced from Decans, T., 2010.
Macroecological patterns in soil communities. Global Ecology and Biogeography 19, 287302 after Swift, M.J., Heal, O.W., Anderson, J.M., 1979.
Decomposition in Terrestrial Ecosystems. Oxford: Blackwell Scientic.
44
Table 1
Functional group
Microorganisms
Micro-fauna
Meso-fauna
Macrofauna
Body width
Taxa
0.320 mm
Bacteria and fungi
Hydrobiont
Antibiosis mutualism
competition
Very limited
0.210 mm
Microarthropods
Enchytraeidae
Hygrobiont
Predation
410 mm
Termites earthworms myriapoda, ants, etc.
Water relationships
Interactions with
microorganisms
Ability to change the physical
environment
Resistance to environmental
stresses
Intrinsic digestive capabilities
o0.2 mm
Proctoctists
nematodes
Hydrobiont
Predation
Intermediate
Low
Low
Hygrobiont
Mutualism (external rumen and facultative/obligate
internal mutualism)
Limited (fecal pellets) High (galleries, burrows, and macro-aggregates)
None
High (cysts,
spores, etc.)
Intermediate
Source: Reproduced from Lavelle, P., Spain, A.V., 2001. Soil Ecology. Amsterdam: Kluwer Scientic Publications.
1000
100
10
0.1
0.01
Bacteria
Fungi
Nematoda
Protozoa
Acari
Collembola
Diplura
NE
Symphyla
Enchytraeidae
Body size
Isoptera
Formicoidea
Diptera
Isopoda
NE
Chilopoda
NE
Dermaptera
NE
Blattoidea
NE
Diplopoda
Arachnida
NE
Coleoptera
NE
Mollusca
Pauropoda
NE
Oligochaeta
Caecilian
NE
Squamata
Mammalia
NE
NE
Described species
Undescribed species
Figure 2 Biodiversity range in dominant soil-dwelling organisms. NE, not estimated. Reproduced from Decans, T., 2010. Macroecological
patterns in soil communities. Global Ecology and Biogeography 19, 287302.
45
Taxa
Functional groups
References
Bacteria
Bacteria
N cycle: e.g., N2
xers, nitriers,
amoniers, and
denitriers
Fungi
Antagonists
Saprophytes
Symbiotic
Pathogenic
Nematodes
Collembola
Acari
Earthworms
Termites
Bacterivores
Epiedaphic
12 groups based
Epigeic
Wood feeders
Ants
Omnivorous
S: Oxidation of sulfur,
thiosulphate,
tetrathionate or
sulphides
Reduction of sulfate
ions to hydrogen
sulde
Fungivores
Root feeders
Carnivores
Mixed feeders
Hemiedaphic
Euedaphic
on: Occurrence of phoresy, feeding habits, demography, and type of reproduction
Anecic
Endogeic
Fungus growers
Humivores
Litter feeders
Predators
Fungus growers
Homoptera
breeders
Moreira and
Cassia (2013)
Wainwright
(1988)
Banage (1966)
Gisin (1943)
Siepel (1994)
Bouch (1977)
Waller and
LaFage (1987)
Korasaki et al.
(2013)
46
Ecosystem Engineers
Earthworms have been classied into three groups (epigeics,
endogeics, and anecics) according to their main feeding habits
and habitats. A suite of biological traits (morphology, anatomy, feeding regime, and demographic prole) is associated
with these basic adaptive strategies. Epigeics are very active,
small, and thoroughly pigmented earthworms that feed on
fresh leaf litter and live within the surface litter itself. Their
small size and use of a relatively rich food allow fast growth
and active reproduction, a necessary demographic strategy
in the face of high mortality from predators and the
unstable moisture conditions that occur within their habitat.
In contrast, Endogeics live in the soil and feed on it, having a
purely geophagous regime based on the consumption of soils
of high (polyhumic), medium (mesohumics), or low (oligohumics) organic matter contents (Lavelle, 1983). Anecics are
very large earthworms (4 20 cm in length) with an anterodorsal pigmentation. They live in vertical galleries that open at
the soil surface and feed on a mixture of partly decomposed
leaves and soil. The conditions of the humid tropics favor
communities of large dominant mesohumic and oligohumic
endogeic populations, whereas with the declining temperature
the proportion of epigeics and polyhumics increases. The decrease in the efciency at lower temperatures of the mutualistic
digestion based on interactions with ingested soil bacteria
47
Ecosystem
services
Soil catenas
Structures
created
5
Soil horizon
Biogenic
structures
4
Intermediate
aggregates
Ecosystem
3
Microbial
aggregates
Community
of ecosystem engineers
2
Ecosystem
engineer
1
Microfoodwebs
Microorganisms
Organisms
Figure 3 Self-organizing systems in soils at different scales from microbial biolms and aggregates (1) to intermediate aggregates, (2) individual
ecosystem engineer functional domains, (3) mosaics of functional domains in an ecosystem, (4) landscape, (5) and the biosphere (6, not
represented), where ecosystem services are delivered along soil catenas. A community of interacting organisms, a set of physical structures that
they inhabit and, in some cases, have created themselves, and the processes that operate at this scale of time and space dene each scale.
Modied from Lavelle, P., Decaens, T., Aubert, M., et al., 2006. Soil invertebrates and ecosystem services. European Journal of Soil Biology 42,
S3S15.
48
A
B
A
A
B
B
A
Gelisols
Alfisols
Entisols
Histosols
Inceptisols
Mollisols
Oxisols
Vertisols
Spodosols
Aridisols
Ultisols
49
5000
MAP (mm.y1)
4000
3000
Tropical
forest
Ant, Earthworms,
termites, millipedes
Fire, drought, and
conversion
Temperate forest
2000
Boreal
forest
Enchytraeids
1000
Savanna
mites, collembola
Enchytraeids
Tundra
0
15
Earthworms
(deciduous, mixed)
Ants
(coniferous)
Grassland
Earthworms, ants
Warming, fire
Termites
Fire, invasives
Warming
Desert
Termites
5
Warming
15
Termites
25
MAT (C)
Figure 5 Dominant groups in soil faunal communities across a climate gradient. Reproduced from Brussaard, L., 2012. Ecosystem services provided
by the soil biota. In: Wall, D.H., Bardgett, R.D., Behan-Pelletier, V., et al. (Eds.), Soil Ecology and Ecosystem Services. Oxford, UK: OUP, pp. 4558.
Microflora
*
22
Catabolic diversity
20
18
16
NV
PF
Grasslands
Crops
50
g m-2
Pastures
60
Brach + kudzu
50
Others
Savana
40
Ants
Termites
30
20
Earthworms
Brach.
Grazed
Natural
10
Annual crops
0
Macroinvert
SR
4255
39
55
1825
Figure 7 Density per m of soil ecosystem engineers and other components of the macrofauna in soils from the Llanos Orientales de Colombia
under six different plant covers. Reproduced from Decaens, T., Lavelle, P., Jaen, J.J.J., Escobar, G., Rippstein, G., 1994. Impact of land
management on soil macrofauna in the oriental Llanos of Colombia. European Journal of Soil Biology 30 (4), 157168.
1000
100
Hygroscopic water
Hygroscopic coefficient
Wilting point
10
Capillary water
1
Field capacity
0.1
Gravitational water
0.01
0.00001
0.0001
0.001
0.01
0.1
51
Nitrogen-xing prokaryotes
Nitrogen is the element required in the largest quantities by
plants. The sources of N in soil are: organic matter, usually
very low, especially in tropical ecosystems; articial nitrogen
fertilizers, quite expensive and potential pollutants; and
biological nitrogen xation. Biological nitrogen xation, the
conversion of gaseous N2 into ammonium, is one of the most
important functions for the sustainability of life on the planet.
Only some groups of bacteria and archaea are able to x
N2 symbiotically. These prokaryotes can live freely in soil
and water or in mutualistic relationships with fungi, lichens,
and certain plants. The most important among these relationships are those of rhizobial bacteria with some legumes
(Leguminosae). This is due to the economic relevance of many
nitrogen-xing legumes as crops, as well as their widespread
occurrence in natural ecosystems. Development of molecular
techniques in the last three decades has allowed a signicant
increase in the knowledge of rhizobial diversity: from the 6
species in a single genus known in 1984 to approximately two
hundred species in 12 genera today. The mutualistic relationships between legumes and rhizobial species range from very
specic to rather promiscuous. This diversity must be considered in the selection of specic bacterial strains to produce
effective inoculum for a given plant species.
Mycorrhizal fungi
Although not required in such large quantities as nitrogen,
phosphorus is usually the nutrient element mostly limiting
plant growth in tropical ecosystems. The low availability of
phosphorus is due to its immobilization through strong
chemical xation on components of weathered soils to form
insoluble inorganic calcium, aluminum, and iron phosphates.
Phosphorus also has a very low mobility in soil, which further
limits its availability.
Mycorrizal fungi can establish mutualistic relationships
with the majority of plant species (Read, 1991). Hyphae infect
the roots of plants and spread through the soil exploring a
soil volume much larger than that which could be explored
by the roots alone. They thereby scavenge nutrients such as
phosphorus and zinc from sources very distant from the root
system. There are seven types of mycorrhizal fungi, but the
most important ones are arbuscular or endomycorrhizas and
ectomycorrhizas. They also enhance plant resistance to various
stresses, such as heavy metal contamination and drought, as
well as provide some protection against pathogens.
The use of rhizobial nitrogen xation by legumes to replace
articial nitrogen fertilizers is an outstanding example of the
contribution of biological processes within sustainable agriculture (Sileshi et al., 2008). For example, the inoculation
of soybeans in Brazil with selected Bradyrhizobium strains
completely replaces nitrogen fertilizers, saving billions of
US dollars annually. Unfortunately, this practice is virtually
restricted to soybean (99%) and only 1% is applied to the
bean Phaseolus vulgaris.
52
Enhanced nutrient release in fresh casts that are then subsequently colonized by plant ne roots (Lavelle et al., 1992;
Chapuis-Lardy et al., 1998; Decans et al., 1999);
Improved soil physical conditions, which enhance plant
water supply;
Enhanced root mycorrhizal colonization;
Direct control of plant parasites;
Production of hormone-like compounds (Blouin et al.,
2005).
Scale 5: Landscape
The organization of eco-efcient landscapes that combine satisfactory economic performance with equitable and adequate
impacts may not be visible for many years (Hector et al., 1999;
Hector, 2002).
In general, agroecosystems that mimic the original system
for example, agroforestry systems in a forest area or an improved pasture in a savanna area are better at conserving
biodiversity than those based on monocultures of annual
crops. For example, in the savannas of the Colombian Orinoco, macro-invertebrate communities are greatly enhanced,
both in total density and species richness in improved pastures
with African grasses (Decaens et al., 1994; Figure 6). Under
such conditions, annual crops have highly deleterious effects,
whereas perennial tree crops do not differ signicantly from
the original savanna. Similar patterns are observed in rainforest areas where agroforestry systems generally have larger
communities of invertebrates than annual crops (Barros et al.,
2002).
Some plants directly stimulate organisms (e.g., legumes for
biological N xation), whereas others have more systemic effects at keeping soil covered with their stolons and litter production, upper tree canopy shade, or by sustaining generalist
predators that will control pests and make applications of toxic
agrochemicals unnecessary (Velasquez et al., 2012; Settle et al.,
1996; Leakey, 2014).
Plants affect soil biodiversity through the amount and
quality of organic material they contribute to the soil as dead
leaves and roots (Vohland and Schroth, 1999; Lavelle et al.,
2001). They also have a direct effect on soils through the
deposition of root exudates, exfoliation of tip cells, and death
of ne roots. In some cases, the addition of particular plant
species may greatly enhance, or decrease, specic elements of
the soil community. This is the case in the approximately
20 000 species within the family Leguminosae, which produce
grains, wood, gums, and green manure and which establish
symbioses with N-xing rhizobial bacteria. These legumes
have high N contents (43%) that can be released during organic matter decomposition, or be transferred to other species
by the hyphae of mycorrhizal fungi that form root connections
and supply N to other plants. Legumes also enhance earthworm activities, with subsequent effects on soil aggregation
and physical properties. For example, in Amazonian pastures
that contain Brachiaria brizantha, the partial or total substitution by the legume fodder plant Arachis pintoi allows earthworm density to signicantly increase from 217 to 365
individuals per square meter (68%), with a subsequent 87%
increase in the fraction of biogenic aggregates to 25.3% and a
15% decrease in non-macro-aggregated soil. Plant-available
water in these soils increased 20%, from 79 to 95 g kg1
(Velasquez et al., 2012).
In contrast, some plants may have intrinsic detrimental
effects on soil biota. Particular attention has recently been
brought to new cultivars of soybean that no longer favor
rhizobial associations and to rice cultivars that do not respond favorably to earthworm or organic matter additions
(McCouch, 2004; Noguera et al., 2011).
Polycultures (e.g., agroforestry) with diverse plant community composition have greater rhizosphere diversity than
monocultures, as signicantly greater amounts of carbon
substrates are released by roots. This stimulates greater biodiversity among the invertebrate litter decomposers (Vohland
and Schroth, 1999) and primary consumers living close to the
53
Tillage
Tillage and other soil mechanical preparations are a further
critical element of agroecosystems that may profoundly inuence soil-living communities. The recurrent destruction
of soil structure by plowing maintains soils at an early successional stage, according to Hollings (2002) adaptive cycle
paradigm. Under such conditions, species that require stable
environmental conditions and mutualistic relationships with
other organisms for their development are progressively
eliminated as negative interactions (competition and predation) prevail. Tillage affects soil biota both directly by killing
them and indirectly by decreasing the food resource base and
destroying their habitat. This is illustrated by the mortality of
large invertebrates and the destruction of fungal networks
(Cavigelli et al., 2012) and the signicant reduction of earthworm numbers and diversity with its consequent negative
impacts on soil physical properties (Wardle, 1995; Figure 10).
Similar results have been reported for a variety of soil invertebrates (Marchao et al., 2009) in cropping systems derived
from the Cerrado vegetation of Brazil, where, with the exception of termites and ants, most groups benet from a shift
from tillage to no-till systems. Nevertheless, Dominguez et al.
(2009) reported that no-till systems had a lower population
density than the natural grassland (70 individuals per square
meter as compared to 297 in the original ecosystem).
Systems with reduced tillage can have higher microbial
biomass and higher fungi:bacteria (F:B) ratios (Beare et al.,
1997), but recent studies suggest that this is not the general
situation. In Laos, for example, in no-till and cover crops
systems in tropical grasslands, Lienhard et al. (2012) did not
nd a change in the F:B ratio, although a clear relationship was
observed between the density and the quantity of microbial
groups and diversity of crop residues (Figure 11). Overall
genetic diversity of the microbial community showed a different pattern linked to soil chemical parameters, such as soil
acidity (exchangeable Al, pH, and CEC) and C:N ratio. Similarly, Strickland and Rousk (2009) had indicated that these
results were far from general. However, Helgason et al. (2009)
did not nd that effect of tillage in intensive tilled versus
untilled soils of the Great North plains (Beare et al., 2009).
54
20
% of studies
40 60 80
100
Resource base
Organic C
Organic N
Microflora
Fungi
Bacteria
Microbes (total)
Microfauna
Fungal-feeding
nematodes
Bacterial-feeding
nematodes
Predatory and omnivorous
nematodes
Total nematodes
Mesofauna
Collembola
Cryptostigmatid mites
Mesostigmatid mites
Prostigmatid mites
Astigmated mites
Total mites
Enchytraeids
Macrofauna
Earthworms
Carabid beetles
Spiders
Key:
V< 0.67
V > 0.67
Figure 10 Effect of tillage on abundance or biomass of soil organism populations. V is the ratio of no-till to control tilled systems. Reproduced
from Kladivko, E.J., 2001. Tillage systems and soil ecology. Soil and Tillage Research 61, 6176.
30
[a]
[b]
[ab]
[ab] [ab]
1.2E+10
1E+10
25
55
8E+08
7E+08
[a]
[b]
[b]
[b]
[ab]
[a]
[b]
[b]
[ab] [ab]
6E+08
8E+09
20
5E+08
+
15
6E+09
+
10
+
+
4E+09
4E+08
3E+08
+
1E+08
0
CT
(a)
NT1
NT2
NT3
PAS
2E+08
2E+09
+
0E+00
CT
(b)
CT
(c)
Figure 11 Effect of tillage on microbial diversity in crops from Laos (Lienhardt et al., 2010). Box and whisker representation of (a) molecular
biomass (micrograms and per gram of soil), (b) bacterial density (copy of 16S rDNA per gram of soil), and (c) fungal density (copy of 18S rDNA
per gram of soil) recorded in natural pasture land (PAS), conventional tillage (CT), and no-till systems (NT (1, 2, and 3)). Letters in brackets
indicate signicant differences (KruskalWallis test (Po0.05, Bonferroni corrections).
Organic amendments
As a generalization, organic inputs increase the species richness
and abundance of soil organisms as compared with conventional cropping systems (Bengtsson et al., 2005; Hole et al.,
2005), although in some cases no response has been observed
(Cavigelli et al., 2012). This may result from the absence
of species that would have beneted from the improved
conditions.
A large part of the detrimental effects of intensive agriculture on soil organisms is due to starvation. Although residue inputs are severely decreased by weeding and the
exportation of large part of the above-ground plant biomass,
the use of chemical fertilizers reduces food sources even more
(Lavelle et al., 2004). In contrast, organic agriculture based
on diverse materials, such as animal and green manures,
56
into farming systems as companion crops to provide ecological/environmental goods and services is also widely implemented to enhance production. Some introduced species
have physical roles, forming erosion-control barriers or
windbreaks, whereas others may be N-xing legumes included
for soil fertility management. Such plants may be so effective
that N xed in these articial systems is equal to 1.5 times N
xed in natural ecosystems (Lavelle et al., 2005; MA, 2005).
Other plants may be used as traps for pests, especially phytoparasitic nematodes, parasitic weeds like Striga, and cereal
stem borers (Khan et al., 2007; Cook et al., 2007).
Inoculation of earthworms has been widely practiced to
improve exotic grass pastures in New Zealand (Edwards and
Bohlen, 1996). Likewise, earthworm inoculation has been
used as part of the FBO (Fertilization Bio Organique) patented
technology (Senapati et al., 1999) in which earthworms are
inoculated into trenches where the highly organic conditions
create small islands of favorable soil functionality (Brown
et al., 1999). Interestingly, in addition to occasional spectacular increases in production, this technology also improved
the organoleptic quality of tea from plantations in India
and China by 1530%.
harmful effects for human health and one for plants. Out of
18 nonbacterial preparations, only 33% increased maize
growth, whereas in soybean only 22% of tested products were
effective (Jefwa et al., 2013).
However, many countries have developed legislative frameworks to control the quality and efciency of inoculants and a
large proportion of the products are delivered with detailed
instructions for an efcient use.
Indicators
The need for indicators: Synthesis of existing approaches
and a proposal for establishing a unique set of tools with
ISO labeling
A large and diverse number of biological, chemical, physical,
and synthetic indicators of soil quality and ecosystem services
have been proposed in the literature (Turb et al., 2010).
However, a comparative analysis of the respective advantages
and disadvantages of these indicators is needed before testing.
57
Conclusion
The conservation and management of soil biodiversity is
central to the attainment of agriculture that is productive and
sustainable over long periods. From this, it follows that greater
effort is now needed to maximize the benets owing from a
wise and conservative use of natural capital. This particularly
applies to the soil taht has become seriously degraded both in
fertility and agroecological function and is responsible for the
declining productivity that is the main cause of the nutritional
insecurity and poverty prevalent in many developing countries
(Leakey, 2012). Urgent tasks are, therefore, to prevent further
resource degradation by maintaining diverse soil covers
and adding organic inputs to the soils. Ultimately, a better
understanding of ecological processes is required, including
the improved, naturally based management of pests and diseases. This, together with a reduction in pollution, is necessary
to reverse declining fertility and improve crop yields in ways
that have much improved environmental and social consequences for local people, as well as the global community.
Once understood, these mechanisms should be urgently
58
References
Andersen, A.N., 1995. A classication of Australian ant communities, based on
functional groups which parallel plant life-forms in relation to stress and
disturbance. Journal of Biogeography 22 (1), 1529.
Auclerc, A., Nahmani, J., Aran, D., et al., 2012. Changes in soil macroinvertebrate
communities following liming of acidied forested catchments in the Vosges
Mountains (North-eastern France). Ecological Engineering 42, 260269.
Banage, W.B., 1966. Nematode distribution in some British upland moor soils with
a note on nematode parasitizing fungi. Journal of Animal Ecology 35,
31493361.
Barois, I., Lavelle, P., 1986. Changes in respiration rate and some physicochemical
properties of a tropical soil during transit through Pontoscolex corethrurus
(Glossoscolecidae, Oligochaeta). Soil Biology & Biochemistry 18 (5), 539541.
Barrios, E., Sileshi, G.W., Shepherd, K., Sinclair, F.L., 2012. Agroforestry and soil
health: Linking trees, biota, and ecosystem services. In: Wall, D.H., Bardgett,
R.D., Behan-Pelletier, V., et al. (Eds.), Soil Ecology and Ecosystem Services.
Oxford: Oxford University Press, pp. 315330.
Barros, E., Pashanasi, B., Constantino, R., Lavelle, P., 2002. Effects of land use
system on the soil macrofauna in western Brasilian Amazonia. Biology and
Fertility of Soils 35, 338347.
Beare, M.H., Hus, S., Coleman, D.C., Hendrix, P.F., 1997. Inuences of mycelial
fungi on soil aggregation and organic matter storage in conventional and notillage soils. Applied Soil Ecology 5, 211219.
Bengtsson, J., Ahnstrom, J., Weibull, A.C., 2005. The effects of organic agriculture
on biodiversity and abundance: A meta-analysis. Journal of Applied Ecology 42
(2), 261269.
Bignell, D.E., Constantino, R., Csuzdi, C., et al., 2008. Macrofauna. In: Moreira, F.
M.S., Huising, E.J., Bignell, D.B. (Eds.), A Handbook of Tropical Soil Biology
Sampling & Characterization of Below-ground Biodiversity 2008. London, UK:
Earthscan, pp. 4383.
Blackwood, C.B., Paul, E.A., 2003. Eubacterial community structure and population
size within the soil light fraction, rhizosphere and heavy fraction of several
agricultural systems. Soil Biology & Biochemistry 35, 12451255.
Blanchart, E., Lavelle, P., Braudeau, E., Le Bissonnais, Y., Valentin, C., 1997.
Regulation of soil structure by geophagous earthworm activities in humid
savannas of Cote dIvoire. Soil Biology & Biochemistry 29, 431439.
Bongers, T., 1990. The maturity index: An ecological measure of environmental
disturbance based on nematode species compostion. Oecologia 83, 1419.
Bouch, M.B., 1977. Stratgies lombriciennes. In: Lohm, U., Persson, T. (Eds.), Soil
Organism as Components of Ecosystems. Stockolm: Ecology Bulletin,
pp. 122132.
Braga, R.F., Korasaki, V., Andresen, E., Louzada, J., 2013. Dung beetle community
and functions along a habitat-disturbance gradient in the Amazon: A rapid
assessment of ecological functions associated to biodiversity. PLoS ONE 8 (2),
e57786. doi:10.1371/journal.pone.00577.
Brown, G.G., Barois, I., Lavelle, P., 2000. Regulation of soil organic matter
dynamics and microbial activity in the drilosphere and the role of interactions
with other edaphic functional domains. European Journal of Soil Biology
36 (34), 177198.
Brown, G., Pashanasi, B., Villenave, C., et al., 1999. Effects of earthworms on plant
production in the tropics. In: Lavelle, P., Brussaard, L., Hendrix, P. (Eds.),
Earthworm Management in Tropical Agroecosystems. Wallinford, UK: CABI,
pp. 87147.
Cavigelli, M.A., Maul, J.E., Szlavecz, K., 2012. Managing soil biodiversity and
ecosystem services. In: Wall, D.H. (Ed.), Soil Ecology and Ecosystem Services.
Oxford: Oxford University Press, pp. 337356.
Chapuis-Lardy, L., Brossard, M., Lavelle, P., Schouller, E., 1998. Phosphorus
transformations in a ferralsol through ingestion by Pontoscolex corethrurus, a
geophagous earthworm. European Journal of Soil Biology 34 (2), 6167.
Chauvel, A., Grimaldi, M., Barros, E., et al., 1999. Pasture damage by an Amazonian
earthworm. Nature 398, 3233.
Clarholm, M., 1985. Interactions of bacteria, protozoa and plant leading to
mineralization of soil nitrogen. Soil Biology & Biochemistry 17, 181187.
Cook, S.M., Khan, Z.R., Pickett, J.A., 2007. The use of push-pull strategies in
integrated pest management. Annual Review of Entomology 52, 375400.
Jesus, E., da, C., Marsh, T.M., Tiedje, J.M., Moreira, F.M., 2009. Changes in land
use alter the structure of bacterial communities in Western Amazon soils. ISME
Journal 3, 10041011.
Jimenez, J.J., Decaens, T., Rossi, J.P., 2006. Stability of the spatio-temporal
distribution and niche overlap in neotropical earthworm assemblages. Acta
Oecologica-International Journal of Ecology 30, 299311.
Kadimaliev, D.A., Nadezhina, O.S., Parshin, A.A., Atykyan, N.A., Revin, V.V., 2010.
Change in phospholipid composition and phospholipase activity of the fungus
Lentinus tigrinus vkm f_3616d during growth in the presence of phenol and
lignocellulosic substrates. Biochemistry (Moscow). ISSN 0006_2979 75 (11),
13421351.
Khan, Z.R., Midega, C.A.O., Hassanali, A., Pickett, J.A., Wadhams, L.J., 2007.
Assessment of different legumes for the control of Striga hermonthica in maize
and sorghum. Crop Science 47, 730734.
Korasaki, V., De Morais, J.W., Braga, F., 2013. Macrofauna. In: Moreira, F.M.,
Zanetti, R., Strmer, S.L. (Eds.), O ecosistema do solo. Lavras, Brazil: Editora
UFLA, pp. 119138.
Kremer, R.J., Means, N.E., 2009. Glyphosate and glyphosate resistant crop
interactions with rhizosphere microorganisms. European Journal of Agronomy 31,
153161.
Lavelle, P., 1983. The structure of earthworm communities. In: Satchell, J.E. (Ed.),
Earthworm Ecology: From Darwin to Vermiculture. London: Chapman & Hall,
pp. 449466.
Lavelle, P., 2012. Soil as a habitat. In: Wall, D.H., Bardgett, R.D., Behan-Pelletier,
V., et al. (Eds.), Soil Ecology and Ecosystem Services. Oxford, UK: Oxford
University Press.
Lavelle, P., et al., 2005. Nutrient Cycling. In: Hassan, R., Scholes, R., Ash, N.
(Eds.), Millennium Ecosystem Assessment. Volume 1: Ecosystems and Human
Well-being. Washington, DC: Island Press, pp. 333353.
Lavelle, P., Barros, E., Blanchart, E., et al., 2001a. SOM management in the tropics:
Why feeding the soil macrofauna? Nutrient Cycling in Agroecosystems 61, 5361.
Lavelle, P., Barros, E., Blanchart, E., et al., 2001b. Soil organic matter management
in the tropics: Why feeding the soil macrofauna? Nutrient Cycling in
Agroecosystems 61, 5361.
Lavelle, P., Bignell, D., Lepage, M., et al., 1997. Soil function in a changing world:
the role of invertebrate ecosystem engineers. European Journal of Soil Biology
33, 159193.
Lavelle, P., Blanchart, E., Martin, A., et al., 1993. A hierarchical model for
decomposition in terrestrial ecosystems Application to soils of the humid
tropics. Biotropica 25 (2), 130150.
Lavelle, P., Blouin, M., Boyer, J., et al., 2004. Plant parasite control and soil fauna
diversity. Comptes Rendus Biologies 327, 629638.
Lavelle, P., Decaens, T., Aubert, M., et al., 2006. Soil invertebrates and ecosystem
services. European Journal of Soil Biology 42, S3S15.
Lavelle, P., Lapied, E., 2003. Endangered earthworms of Amazonia: An homage to
Gilberto Righi. Pedobiologia 47 (56), 419427.
Lavelle, P., Lattaud, C., Trigo, D., Barois, I., 1995. Mutualism and biodiversity in
soils. Plant and Soil 170, 2333.
Lavelle, P., Melendez, G., Pashanasi, B., Schaefer, R., 1992. Nitrogen mineralization
and reorganization in casts of the geophagous tropical earthworm Pontoscolex
corethrurus (Glossoscolecidae). Biology and Fertility of Soils 14, 4953.
Lavelle, P., Pashanasi, B., 1989. Soil macrofauna and land management in Peruvian
Amazonia (Yurimaguas, Loreto). Pedobiologia 33, 283291.
Lavelle, P., Rodrguez, N., Arguello, O., et al., 2014. Soil ecosystem services and
land use in the rapidly changing Orinoco River Basin of Colombia. Agriculture,
Ecosystems and Environment 185, 106117.
Lavelle, P., Spain, A.V., 2001. Soil Ecology. Amsterdam: Kluwer Scientic
Publications.
Leakey, R.R.B., 2012. Living with the Trees of Life Towards the Transformation of
tropical Agriculture. Wallingford, UK: CABI.
Leakey, R.R.B, 2014. The role of trees in agroecology and sustainable agriculture in
the tropics. Annual Review of Phytopathology. 52.
Leal, P.L., Siqueiraa, J.O., Strmer, S.L., 2013. Switch of tropical Amazon forest to
pasture affects taxonomic composition but not species abundance and diversity
of arbuscular mycorrhizal fungal community. Applied Soil Ecology 71, 7280.
doi.org/10.1016/j.apsoil.2013.05.010.
Lienhard, P., Tivet, F., Chabanne, A., et al., 2013. No-till and cover crops shift soil
microbial abundance and diversity in Laos tropical grasslands. Agronomy and
Sustainable Development 33, 375384.
Lima, A.S., Nbrega, R.S.A., Barberi, A., et al., 2009. Nitrogen-xing bacteria
communities occurring in soils under different uses in the Western Amazon
Region as indicated by nodulation of siratro (Macroptilium atropurpureum). Plant
and Soil 319, 127145.
59
Loranger, G., Ponge, J.F., Blanchart, E., Lavelle, P., 1998. Impact of earthworms on
the diversity of microarthropods in a vertisol (Martinique). Biology and Fertility
of Soils 27, 2126.
Marchao, R.L., Lavelle, P., Celini, L., et al., 2009. Soil macrofauna under integrated
crop-livestock systems in a Brazilian Cerrado Ferralsol. Pesquisa Agropecuaria
Brasileira 44, 10111020.
Marschner, H., Rmheld, V., Horst, W.J., Martin, P., 1986. Root-induced changes in
the rhizosphere: Importance for the mineral nutrition of plants. Zeitschrift fr
Panzenernhrung und Bodenkunde 149, 441456.
Martin, A., Mariotti, A., Balesdent, J., Lavelle, P., 1992. Soil organic matter
assimilaion by a geophagous tropical earthworm based on 13C measurments.
Ecology 73, 118128.
McCouch, S., 2004. Diversifying selection in plant breeding. PLoS Biology 2,
15071512.
Menendez, I., Caniego, J., Gallardo, J.F., Olechko, K., 2005. Use of fractal scaling to
discriminate between and macro- and meso-pore sizes in forest soils. Ecological
Modelling 182, 323335.
Millennium Ecosystem Assessment (MA), 2005. Ecosystems and Human Wellbeing:
Synthesis. Washington, DC: Island Press.
Mimet, A., Houet, T., Julliard, R., Simon, L., 2013. Assessing functional
connectivity: A landscape approach for handling multiple ecological requirements.
Methods in Ecology and Evolution 4, 453463.
Moore, J.C., Berlow, E.L., Coleman, D.C., et al., 2004. Detritus, trophic dynamics
and biodiversity. Ecology Letters 7 (7), 584600.
Myers, R.J.K., Palm, C.A., Cuevas, E., Gunatileke, I.U.N., Brossard, M., 1994. The
synchronization of nutrient mineralisation and plant nutrient demand. In:
Woomer, P.L., Swift, M.J. (Eds.), The Biological Management of Tropical
Fertility. Chichester: Wiley-Sayce, pp. 81116.
Nelson, E., Mendoza, G., Regetz, J., et al., 2009. Modeling multiple
ecosystem services, biodiversity conservation, commodity production, and
tradeoffs at landscape scales. Frontiers in Ecology and the Environment 7,
411.
Noguera, D., Laossi, K.R., Lavelle, P., et al., 2011. Amplifying the benets
of agroecology by using the right cultivars. Ecological Applications 21,
23492356.
Potthoff, M., Asche, N., Stein, B., Muhs, A., Beese, F., 2008. Earthworm
communities in temperate beech wood forest soils affected by liming. European
Journal of Soil Biology 44, 247254.
Rantalainen, M.L., Haimi, J., Fritze, H., Setala, H., 2006. Effects of small-scale
habitat fragmentation, habitat corridors and mainland dispersal on soil
decomposer organisms. Applied Soil Ecology 34 (23), 152159.
Read, D.J., 1991. Mycorrhizas in ecosystems. Experientia 47, 376391.
Rossi, J.P., 2003. The spatiotemporal pattern of a tropical earthworm species
assemblage and its relationship with soil structure. Pedobiologia 47,
497503.
Rousk, J., Baath, E., Brookes, P.C., et al., 2010. Soil bacterial and fungal communities
across a pH gradient in an arable soil. ISME Journal 4, 13401351.
Ruiz, N., Mathieu, J., Clini, L., et al., 2011. IBQS: A synthetic index of soil quality
based on soil. Soil Biology & Biochemistry 43 (10), 20322045.
Sabatier, D., Grimaldi, M., Prvost, M.-F., et al., 1997.The inuence of soil cover
organization on the oristic and structural heterogeneity of a Guianan rain forest.
Plant Ecology 131, 81108.
Scheu, S., 2003. Effects of earthworms on plant growth: patterns and perspectives.
Pedobiologia 47, 846856.
Senapati, B.K., Lavelle, P., Giri, S., et al., 1999. In-soil earthworm technologies for
tropical agroecosystems. In: Lavelle, P., Brussaard, L., Hendrix, P. (Eds.), The
Management of Earthworms in Tropical Agroecosytems. Wallingford, UK: CAB
International, pp. 189227.
Setl, H., Huhta, V., 1991. Soil fauna increase Betula pendula growth: Laboratory
experiments with coniferous forest oor. Ecology 72 (2), 665671.
Settle, W.H., Ariawan, H.A., Astuti, E.F., et al., 1996. Managing tropical rice pests
trough conservation of generalist natural ennemies and alternative preys. Ecology
77, 19751988.
Siepel, H., 1994. Life-history tactics of soil microarthropods. Biology and Fertility of
Soils 18, 263278.
Sileshi, G., Akinnifesi, F.K., Ajayi, O.C., Place, F., 2008. Meta-analysis of maize
yield response to planted fallow and green manure legumes in sub-Saharan
Africa. Plant and Soil 307, 119.
Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis, third ed. New York, NY:
Academic Press, 800 pp.
Strickland, M.S., Rousk, J., 2009. Considering fungal:bacterial dominancein soils
Methods, controls, and ecosystem implications. Soil Biology & Biochemistry 42,
13851395.
60
Stromberger, M.E., Klose, S., Ajwa, H., Trout, T., Fennimore, S., 2005.
Microbial populations and enzyme activities in soils fumigated with
methylbromide alternatives. Soil Science Society of America Journal 69,
19871999.
Strmer, S.L., Siqueira, J.O., 2011. Species richness and spore abundance of
arbuscular mycorrhizal fungi across distinct land uses in Western Brazilian
Amazon. Mycorrhiza 21, 255267. doi:10.1007/s00572-010-0330-6.
Swift, M.J., Anderson, J.M., 1994. Biodiversity and ecosystem function in
agricultural systems. In: Schulze, E.D., Mooney, H.A. (Eds.), Biodiversity and
Ecosystem Function. Berlin: Springer-Verlag, pp. 1541.
Swift, M.J., Heal, O.W., Anderson, J.M., 1979. Decomposition in Terrestrial
Ecosystems. Oxford: Blackwell Scientic.
Turb, A., De Toni, A., Benito, P., et al., 2010. Soil biodiversity: functions, threats
and tools for policy makers. Report for European Commission (DG Environment).
Brusells, Belgium: European Commission, 249 p.
Velasquez, E., Fonte, S.J., Barot, S., et al., 2012. Soil macrofauna-mediated impacts
of plant species composition on soil functioning in Amazonian pastures. Applied
Soil Ecology. 56, 4350.
Vohland, K., Schroth, G., 1999. Distribution patterns of the litter macrofauna in
agroforestry and monoculture plantations in central Amazonia as affected by plant
species and management. Applied Soil Ecology 13, 5768.
Wainwright, M., 1988. Metabolic diversity of fungi in relation to growth and mineral
cycling in soil A review. Transactions of the British Mycological Society 90,
159170.
Waller, D.A., LaFage, J.P., 1987. Nutritional ecology of termites. Nutritional ecology
of insects. In: Slansky Jr., F., Rodriguez, J.G. (Eds.), Mites and Spiders. New
York, NY: John Wiley and Sons, pp. 487532.
Wardle, D.A., 1995. Impacts of disturbance on detritus food webs in agroecosystems of contrasting tillage and weed management practices. Advances in
Ecological Research 26, 105185.
Wardle, D., Lavelle, P., 1997. Linkages between soil biota, plant litter quality and
decomposition. In: Cadisch, G., Giller, K.E. (Eds.), Driven by Nature. Wallingford,
UK: CAB-International, pp. 107125.
Wurst, S., De Deyn, G., Orwin, K., 2012. Soil biodiversity and function. In: Wall, D.
H., Bardgett, R.D., Behan-Pelletier, V., et al. (Eds.), Soil Ecology and Ecosystem
Services. Oxford: Oxford University Press, pp. 2844.
Zanaroli, G., Di Toro, S., Todaro, D., et al., 2010. 1DICASM, Faculty of Engineering,
University of Bologna, via Terracini 28, 40131 Bologna, Italy.
Relevant Website
www.globalsoilbiodiversity.org/
Global Soil Biodiversity Iniciative.
Glossary
Biosecurity All hygienic practices (measures) designed to
prevent the occurrence of infectious disease.
Equine herpesvirus 1 neurological disease (Equine herpes
myeloencephalopathy, EHM) It is rare in the horse
population but apparently increasing in incidence now
occurring as outbreaks rather than as individual cases.
Infectious disease Pathogens spread easily from subject to
subject either directly or indirectly; in general the index
subject has the disease but may be a carrier.
Methicillin-resistant Staphylococcus aureus (MRSA) An
emerging pathogen of the horse particularly associated with
wounds and surgical site infections.
Introduction
Infectious diseases are a constant threat to the health and
welfare of horses. Several diseases have assumed greater importance as the performance and pleasure horse populations
and equine activities have increased and there are new owners
who do not understand the implications of equine infectious
disease outbreaks to their animals. In addition, emerging diseases have beset the equine species in recent years in North
America. Firstly, the introduction of the Old World West Nile
virus to a susceptible population has made the the virus to be
considered as endemic. Secondly, the change in the antigenicity of equine herpesvirus-1 (EHV-1) to induce a more
aggressive form of neurological disease may affect clusters of
horses than the eld strain encountered previously. Fortunately, North America has been spared the infection caused by
the paramyxovirus responsible for Hendra virus infection
spread by ying foxes (bats), which is a zoonotic disease and a
deadly infection of horses in Australia. However, other infectious diseases are more likely to emerge among horses in
North America in the next decade as pathogens and vectors
move into and become accustomed to new climate zones. The
threat of emergent diseases is apparent in the UK, where a
warming climate could precipitate a northward spread of those
Culicoides spp. responsible for African horse sickness among a
highly susceptible population.
Vaccination and preventive management procedures are
critical to disease prevention, but these need to be more widely
adopted, complied with, and promulgated. The National
Animal Health Monitoring System (1998) survey raised the
specter that a signicant number of horses throughout the
United States do not receive regular vaccinations and preventive health is not part of the owners protocol. Therefore,
much work remains to be done in communicating the message
before a devastating outbreak of infectious disease among
horses takes hold. Unfortunately, vaccines are unavailable or
are inefcient for several infectious diseases in the United
States. Successful vaccines to protect against equine herpes
Biosecurity
Biosecurity represents an important part of the veterinarians
responsibilities in the clinic or practice facility, at farms,
stables, barns, and at shows and events, where horses commingle from multiple locations. Technicians, owners, and
caretakers must understand the implications, share the responsibilities, and implement specic management procedures. Communication with and education of all personnel
doi:10.1016/B978-0-444-52512-3.00135-2
61
62
Table 1
Viral
Equine coronavirus
EHV-1 respiratory disease
EHV-1 neurological disease (EHM) (E)
EHV-4 respiratory disease
Equine inuenza
West Nile virus (Z not by horses) (E)
Vesicular stomatitis virus (multiple species)
Equine viral arteritis
Rabies (Z)
Eastern/Western equine encephalitis (Z not by horse)
Equine infectious anemia
Foreign animal diseases (viral)
based on the evaluations of risk assessment, resource management, and horse management. All personnel must be
familiar with and preferably certied on the infectious disease protocol for the premises. Risk assessment is the
knowledge of ongoing disease outbreaks elsewhere and the
potential for their spread. Resource management includes
devising and establishing a chain of command with dened
responsibilities, for example, to identify isolation and biosecurity capabilities both on- and off-site; to insure the
availability of diagnostic sampling materials, disinfectants,
and biocontainment materials; and to inspect facilities
recently vacated after another equine or livestock event for
adequate sanitation (decontamination) and waste removal
before animals are readmitted (this includes transport
vehicles and trailers/vans). Horse management involves
publicizing and enforcing health requirements for access to
the facility and implementing an equine identication and
tracking system.
If an infectious disease is suspected, the veterinarian must
make decisions and assume responsibilities according to the
devised plan. The clinician should communicate to all individuals (key personnel, technicians, and owners at the premises) the established plan and indicate that diagnostic testing is
valuable but can take time. The clinician must think biosecurity by not making the situation worse, for example, avoid
rushing into a barn/stall without having a plan to leave it and
must respond to the worst-case scenario until a diagnosis is
made.
In the case of a positive (suspect) diagnosis, management
procedures based on disease-specic guidelines must be
adopted. If there is no diagnosis, biosecurity measures must be
maintained for a minimum of 2128 days after the last case
had developed, the differential diagnosis list must be expanded, and infectious disease experts and state health ofcials must be contacted.
Biosecurity measures have assumed a much greater level
of signicance based on the experiences gained by many
veterinarians and support personnel engaged in managing
outbreaks of life-threatening equine salmonellosis mainly in
referral hospitals and, more recently, neurological disease
associated with EHM at racetracks, showgrounds with large
horse populations, and tertiary referral hospitals. Most tertiary referral hospitals, particularly those at universities,
have infectious disease control policies and procedures
for horses and other species that are updated regularly.
Infectious disease control strategies (policies and procedures) should be developed for private practices (and individual equine operations) to cover on-site horse health
admissions, accommodation, patterns of personnel and animal trafc on-site, disinfection, waste management, and offsite farm/stable/barn precautions by veterinarians and other
personnel.
Biosecurity is only as effective as the acceptance of and
compliance with regulations by all personnel, for example, the
equine inuenza outbreak that emanated from a quarantine
center in Australia. Moreover, biosecurity measures however
well developed and accepted cannot be taken for granted, for
example, spread of foot-and-mouth disease virus from Pirbright, England (foot-and-mouth disease virus World Reference
Laboratory) on the tires of contractors vehicles.
63
64
Neurological Signs
Expression of clinical signs in the relatively small number of
EHM cases is a consequence of vasculitis followed by
hemorrhage, thrombosis, hypoxia, and secondary ischemic
degeneration in the central nervous system.
Signs include progressive or acute onset ataxia (incoordination) or recumbency approximately 1 week after viral
exposure that affects a single animal or group of at least 2 years
of age. Signs may progress rapidly over 2448 h. Pyrexia and
depression are usually noted 34 days before the onset of
neurological signs, which include pelvic limb ataxia, paresis, or
paralysis and may affect all four limbs. Signs are usually more
severe in the pelvic limbs than in the thoracic limbs and may
lateralize. There may be signs consistent with lower motor
neuron dysfunction, urinary incontinence, reduced tail tone,
penile or vulval accidity, and loss of perineal sensation. Tetraplegia and death may supervene. Paralysis and recumbency
carry an increasingly poor prognosis. Horses rarely show abnormal mentation or develop cranial nerve signs. Most horses
exhibit mild to moderate neurological signs and stabilize
rapidly becoming normal 36 months after onset of clinical
signs, although residual decits may persist.
EHV infections are ubiquitous. Most animals are infected
during the rst year of life. The pathogen is latent. Up to 80%
of horses (possibly more) are purported to be latently infected
with EHV-1 or EHV-4, cannot easily be identied, and serve as
important reservoirs.
EHM outbreaks have occurred in late fall through late
spring, possibly coinciding with pregnancy and lactation associated with abortigenic EHV-1 in mares and respiratory EHV4 transmission among foals. EHM outbreaks may be
dependent on the reactivation of latent EHV-1, EHV-4, or both
viruses on introducing a new animal into a population and
associated stress. EHV-1 (and possibly EHV-4) can remain latent for the horses entire life. Under stress conditions, the
virus may replicate and is shed in nasal secretions. Other
horses can be exposed and infected without necessarily the
shedder becoming ill. Outbreaks may represent new infections
with a virulent strain that occurs in a large number of horses
over a short period of time.
Immunology
High virus-neutralizing titers (humoral immune response) are
detected within a few days of the onset of neurological signs.
However, there is no correlation between the level of serum
antibody titers and virus protection. Viremia occurs in the
presence of neutralizing antibodies, as apparent in vaccinated
or naturally immune horses. Cellular immunity is critical and
Therapy
Supportive therapy may be needed for several weeks to
months and includes slinging the horse if it is weak in the
pelvic limbs or is recumbent. Ataxic horses that remain
standing may be better on a (rm) ground surface than in a
stall. Use of nonsteroidal anti-inammatory drugs), such as
unixin meglumine, makes the patient feel better, and the
antiherpesvirus drugs widely used in human patients, acyclovir
and valocyclovir, may be benecial early in the course of the
disease or prophylactically.
Prognosis
Many horses stabilize and recover completely in weeks to
months. Some retain residual neurological decits. The prognosis is worse if the horse is recumbent in the rst 24 h.
Prevention
Efcacy of EHV-1 vaccines is questionable and randomized
controlled studies are lacking. Vaccine products provide varying levels of protection against respiratory disease (modied
live virus (MLV) and killed) and abortion (killed and some
MLV). Anecdotal evidence suggests that vaccination may offer
reasonable protection against a are up of respiratory disease
(although few data exist). Protection against abortion is less
clear as the prevalence is extremely low. Current EHV-1, EHV4, or EHV-1/4 vaccines are not effective against the neurological disease. At best the vaccinated horse that develops
neurological disease will shed fewer virus particles and be less
likely to spread the disease to other horses. There is evidence of
an association between neurological disease and recent and
regular vaccinations with mono- or bivalent killed vaccines.
On premises with conrmed EHM, exposed horses should
not receive booster vaccinations. However, the immune status
of nonexposed horses and those that must enter the premises
if not vaccinated against EHV-1 within the past 60 days should
be enhanced by booster vaccination. The reduced nasal shedding of infectious EHV-1 by recently vaccinated horses may
indirectly help to protect other horses by reducing the dose of
exposed virus.
Regulations
State animal health ofcials provide information on enhanced
requirements in the face of an outbreak.
Several states require reporting of EHV-1 (known as EHM)
and quarantine of affected and in-contact horses.
Clinical Outcomes
Clinical outcomes in EHM outbreaks are modulated by many
risk factors, including the host immune system (vaccination,
cytotoxic T-lymphocytes, and major histocompatability complex), stress (lactation, double infections, and racing), and the
genetic characteristics of virus isolates. The proportion of
animals showing neurological signs when infected with the
neuropathic strain varies with each outbreak. Neurological
diseases outbreaks are relatively rare compared with nonneurological disease outbreaks, suggesting that the majority of
EHV-1 strains encode the nonneuropathic strain.
Diagnostic Testing
Identication of the pathogen requires nasal swab (shedding
may be of short duration) and whole blood sample (for buffy
coat) at the onset of clinical signs (temperature). Polymerase
chain reaction provides the most rapid testing. Real-time
polymerase chain reaction (RT-PCR) assays are used to detect
and differentiate neuropathic from nonneuropathic EHV-1
strains.
RT-PCR assays detect only viral genomic deoxyribonucleic
acid in the specimens tested and are unable to distinguish
between lytic, dead, or latent virus and do not predict clinical
outcome. Interpretation of PCR viral detection for EHV-1
should be done only in the context of the presenting signs for
disease in the horse being tested. The signicance of a positive
PCR in an asymptomatic horse is unknown.
Horses with high fevers and signs of coughing or mild nasal
discharge, with or without neurological decits, should be
tested for EHV-1 by PCR diagnostics if there are no other explanations for their signs of disease. Detection of a positive
PCR for EHV-1 in such instances should warrant isolation and
limited movement of exposed horses.
65
66
Pathogenesis
Strangles in Horses
This is not an emerging disease of horses, although it remains
an important infectious disease for susceptible individuals or
populations. The causative agent is S. equi subspecies equi,
(Lanceeld Group C, Gram positive -hemolytic bacterium).
There is a close genetic relationship between Streptococcus equi
subspecies equi and Streptococcus zooepidemicus, the former
being a clone of the more genetically diverse S. zooepidemicus
and isolates of these two organisms show at least 92% homology. Immunity is species specic; immunization with S.
zooepidemicus does not protect against challenge by S. equi equi.
Streptococcus equi (as subsequently described) is not a normal
inhabitant of the equine upper respiratory tract. PCR may aid
in conrming S. equi isolates but not active infection.
Clinical Signs
The incubation period is 26 days, typically with fever
(4103 F), lethargy, depression, and serous nasal discharge
that becomes mucopurulent. Submandibular and retropharyngeal lymph nodes initially rm become uctuant and
rupture after 710 days (retropharyngeal lymph node abscesses may rupture internally into a guttural pouch).
Lymphadenopathy, if severe, may lead to dysphagia and
respiratory distress, hence the term strangles.
Pus in the guttural pouches may become inspissated,
leading to chondroid formation enabling S. equi to persist for
up to several years and be transmitted to nave horses. There is
a soft moist cough occasionally. The average course of the
disease is 3 weeks. Atypical infection is associated with mild
signs and minimal lymph node abscess development.
Pyrexia is the consequence of the acute phase inappropriate
immune response generated by S. equi and can be monitored
and detected in the absence of bacterial shedding. Once a
strangles outbreak is conrmed, presumptively infected pyrexic
horses may be identied and isolated before the organism is
passed on to in contacts.
Epidemiology
Diagnosis
Treatment
Treatment is contentious and is a function of the stage of the
disease. Penicillin is the drug of choice, although the organism
is sensitive to many antimicrobials. Treatment plans have been
developed, for example, (1) Horse exposed: penicillin helps to
prevent seeding of the pharyngeal lymph nodes. It should be
Complications
The major complications are:
1. Bastard strangles, in which metastatic (internal) abscesses
occur in the mesentery or parenchymatous organs and even
in the brain promulgated by inadequate antimicrobial
therapy, although abscesses can occur naturally at those
sites following infection. Clinical signs include intermittent
colic, periodic pyrexia, anorexia, depression, weight loss,
and neurological dysfunction.
2. PH an aseptic vasculitis following reexposure to S. equi by
natural infection or vaccination. Affected animals have
higher IgA titers to SeM and to nonspecic proteins in the
S. equi culture supernatant and immune complexes of IgA
and M-like proteins. There is an association with the attenuated live intranasal S. equi vaccine. Clinical signs include a mild transient reaction to a severe and fatal form,
with pitting edema of limbs, trunk, and head; petechiation
and ecchymoses of mucosae; and colic. Vasculitis may lead
to skin sloughing and infarcts of skeletal muscle. Death can
result from pneumonia, cardiac arrhythmias, renal failure,
or gastrointestinal disorders.
Other complications of strangles include guttural pouch
empyemia and chondroid formation; septicemia, development of infectious arthritis, pneumonia, and encephalitis;
retropharyngeal abscesses; laryngeal hemiplegia; tracheal
compression following abscesses in the cranial mediastinal
lymph nodes; endocarditis or myocarditis following abscess
formation; suppurative necrotic bronchopneumonia; and two
types of myopathies (myositis) one a vasculitis with infarction of skeletal muscle and pulmonary and gastrointestinal
tissues characterized by unrelenting pain; the second affecting
quarter horses showing malaise, signicant muscle atrophy,
and chronic active rhabdomyolysis.
67
Prevention
Less immunity is provided following vaccination than that
following recovery from natural disease.
The intramuscular killed (S. equi extract) vaccine with an
adjuvant is used more widely than the intranasal attenuated
S. equi live culture, which should not be administered with
parenteral injections or at the time of invasive procedures. No
current vaccine guarantees prevention of strangles in vaccinated horses.
Vaccination of infected animals during an outbreak may be
associated with PH, and vaccination during an outbreak is
controversial.
The 2005 American College of Veterinary Internal Medicine
Consensus Statement recommends measuring SeM-specic
antibody titers by ELISA before vaccination and to not vaccinate if titers Z1:3200. Horses previously given the intranasal
vaccine, nonthoroughbreds and nonwarmbloods, are signicantly more likely to have higher titers (41:1600).
Generation of an immune response to multiple protective
epitopes may be required to achieve the greatest protection.
Development of a strangles vaccine (ideally with differential
diagnostic potential) benetting from an improved immunogenicity and safety prole is a priority to achieve widespread
protection against strangles.
References
Ainsworth, D.M., Hacket, R.P., 2004. Streptococcus equi infections (strangles). In:
Reed, S.M., Bayly, W.M., Sellon, D.C. (Eds.), Equine Internal Medicine, second
ed. St. Louis, MO: Saunders, pp. 308312.
Anderson, M.E.C., Lefebvre, S.L., Rankin, S.C., et al., 2009. Retrospective
multicentre study of methicillin-resistant Staphylococcus aureus infections in 115
horses. Equine Veterinary Journal 41, 401405.
Axon, J.E., Carrick, J.B., Barton, M.D., et al., 2011. Methicillin-resistant
Staphylococcus aureus in a population of horses in Australia. Australian
Veterinary Journal 89, 221225.
Boyle, A.G., 2011. Streptococcus equi subspecies equi infection (strangles) in
horses. Compendium Continuing Education for Veterinarians 33, E1E8.
Dunowska, M., Morley, P.S., Traub-Dargatz, J.L., Van Metre, D.C., 2007.
Biosecurity. In: Sellon, D.C., Long, M.T. (Eds.), Equine Infectious Diseases. St.
Louis, MO: Elsevier, pp. 528539.
Harrington, D.J., Sutcliffe, I.C., Chanter, N., 2002. The molecular basis of
Streptococcus equi infection and disease. Microbes and Infection 4,
501510.
Jordan, D., Simon, J., Fury, S., et al., 2011. Carriage of methicillin-resistant
Staphyloccus aureus by veterinarians in Australia. Australian Veterinary Journal
89, 152159.
National Animal Health Monitoring System (NAHMS) USDA-APHIS; VS, 1998. Part
1: Baseline Reference of 1998 Equine Health and Management, 29.
Sweeney, C.R., Timoney, J.F., Newton, J.R., et al., 2005. Streptococcus equi
infections in horses: Guidelines for treatment, control and prevention of
strangles. Journal of Veterinary Internal Medicine 19, 123134.
Timoney, J.F., Kumar, P., 2008. Early pathogenesis of equine Streptococcus equi
infection (strangles). Equine Veterinary Journal 40, 637642.
68
Waller, A.S., Jolley, K.A., 2007. Getting a grip on strangles: Recent progress
towards improved diagnostics and vaccines. Veterinary Journal 173, 492501.
Waller, A.S., Paillot, R., Timoney, J.F., 2011. Streptococcus equi: A pathogen
restricted to one host. Journal of Medical Microbiology 60, 12311240.
Weese, J.S., 2007. Staphylococcal infections. In: Sellon, D.C., Long, M.T. (Eds.),
Equine Infectious Diseases. St. Louis, MO: Elsevier, pp. 257263.
Relevant Websites
www.cahfs.ucdavis.edu
California Animal Health and Food Safety Laboratory.
http://www.ca.uky.edu/gluck/BiblioEHV1.asp
Gluck Equine Research Center, Lexington, KY OIE reference laboratory for
EHV-1.
www.vetmed.ucdavis.edu/vme/taqmanservice/diagnostics.html
Real-Time Research and Diagnostic Core Laboratory.
www.vetmed.ucdavis.edu/ceh/ehv1_general.cfm
UC Davis Center for Equine Health.
http://www.vetmed.u.edu/extension/documents/MRSAand horses.pdf
University of Florida MRSA and horses.
www.aphis.usda.gov/animal_health/animal_dis_spec/horses/
USDA-APHIS Center for Epidemiology and Animal Health.
www.aphis.usda.gov/animal_health/animal_dis_spec/horses/
USDA-APHIS Veterinary Services.
Introduction
The ultimate grand challenge of our times is nothing less than
the sustainability of the Biosphere and our place in it. Can we
learn how to meet our needs today without compromising the
ability of future generations to meet theirs? With the 7 billionth member of humanity having joined the planet,
achieving global food security sustainably is the single most
important issue facing civilization and, by implication, the
planet in the next 30 years. Over the coming decades, food and
agricultural production systems must be signicantly enhanced to respond to a number of transformative changes,
such as a growing world population; increasing international
competition; globalization; shifts to increased meat consumption in developing countries; and diet-related disease and
rising consumer demands for improved food quality, safety,
health enhancement, and convenience. New and innovative
techniques will be required to ensure an ample supply of
healthy food by improving the efciency of the global agriculture sector. To confound this situation the inequity between
the afuent and the developing countries will continue to
grow and only a handful of technologies are sufciently scale
neutral to help with redressing this imbalance. Of even greater
concern is the very immediate need of global food security. In
2012, the United Nations issued an unprecedented warning
about the state of global food supplies. They noted that global
food reserves have reached their lowest level in almost 40 years
and that failing harvests in the United States, Ukraine, and
other countries in 2012 have eroded reserves to their lowest
level since 1974 when the global population was much lower.
They warned that world grain reserves are so dangerously low
that another year of severe weather in the United States or
other food-exporting countries could trigger a major hunger
crisis by 2013. Clearly, unprecedented needs require effective
solutions (Eliasson, 2012).
Over the millennia many technologies have been developed and used to enhance productivity of the original coterie of cultivated crops and to bring more into the domestic
fold. In the latter half of the twentieth century, major improvements in agricultural productivity were largely based on
selective breeding programs for plants and animals, intensive
use of chemical fertilizers, pesticides and herbicides, advanced
equipment developments, and widespread irrigation programs. This has been a very successful model for raising
productivity; yet, these improvements have brought the corresponding problems of an increasing narrow genetic base of
crop plants and domestic animals, pests resistant against
chemical pesticides, adverse impacts on environmental quality, and capital-intensive production. In addition, from a global perspective, these advances have been the prerogative of
more afuent regions. Farmers in developing countries
doi:10.1016/B978-0-444-52512-3.00213-8
69
70
technologies are sufciently scale-neutral to help with redressing this imbalance. In October 2009, the United Nations
Food and Agriculture Organization (FAO) determined that
farming in developing countries needs US$83 billion of annual investment for production to feed the world in 2050. The
2008 World Bank Development Report emphasized, Agriculture is a vital development tool for achieving the Millennium Development Goals that calls for halving by 2015 the
share of people suffering from extreme poverty and hunger
(World Bank, 2008). The Report notes that three out of every
four people in developing countries live in rural areas and
most of them depend directly or indirectly on agriculture for
their livelihoods. It recognizes that overcoming abject poverty
cannot be achieved in sub-Saharan Africa (SSA) without a
revolution in agricultural productivity for resource-poor
farmers in Africa, many of whom are women. Likewise the
FAO publication, the State of Food Insecurity in the World
2011, highlights the differential impacts that the world food
crisis of 200608 had on different countries, with the poorest
being most affected. Although some large countries were able
to deal with the worst of the crisis, people in many small
import-dependent countries experienced large price increases
that, even when only temporary, can have permanent effects
on their future earnings capacity and ability to escape poverty.
African smallholder farmers are some of the most impoverished people in the world (43% are women) and they account
for 80% of food production in SSA. Some people argue that
their future will be driven by the private sector the UKs
Department for International Development has been working
to link up businesses with smallholder farmers. Giant food
retailers are also starting to realize that they need to look after
African smallholders to safeguard their future. Although not
the only answer, the technological advances of biotechnology
can help to assist with providing food sufciency and economic independence for such resource-poor regions.
Most of the innovative technologies that have been applied
to production agriculture have come into common usage
without much controversy or even knowledge by the average
consumer. If asked, the majority of respondents would no
doubt agree that this involves at some level new, science-based
products and processes that contribute reliable methods for
improving quality, productivity, and environmental sustainability. In the past we have not regulated changes in agriculture
based on unpredictable socioeconomic consequences. However, some recent innovative technologies, namely biotechnology and more specically recombinant deoxyribonucleic acid
(DNA) technology, have inspired debate in a manner unlike
any other previous technological development. Although
biotechnology has introduced a new dimension to such innovation, offering efcient and cost-effective means to produce a diverse array of novel, value-added products and tools
is not viewed with unmitigated optimism by all existing and
potential stakeholders. The stakeholders involved in this debate are many and diverse, ranging from academic and industrial scientists to conventional and organic producers, to
international, national, federal, state, and local government
and nongovernmental organizations (NGOs) and agencies, to
activist groups and, of course, consumers. How this technology is viewed depends very much on the perspective from
which it is viewed and the goals and objectives of the different
players involved. And this perspective is formed by the complexity of the prism through which it is viewed. Each individuals prism is built of our cumulative life experiences,
educational background, innate prejudices, world view, and,
of course, personal objectives. To most producers, and academic and industrial researchers, biotechnology is seen as offering a new dimension to innovation, providing efcient and
cost-effective means to produce a diverse array of value-added
products and tools. To some of our national and international
markets it is seen as a trading barrier or chip, depending on
which side of the fence one is standing. To others it represents
an unnecessary, and for some, unnatural risk at a broad level
to our food system and environment and at a very fundamental level to a way of life or code of beliefs. Unfortunately,
as in every walk of life, there are some who seize on these
many nuances of perception, and indeed fear, to propagate
their own, covert or otherwise, agenda. Although on the surface scientic facts may appear immutable, how those facts are
presented within a socioeconomic context makes for an
interesting study of the stratagems used by the diverse stakeholders to advance their own agenda for any given target
demographic. These tactics are played out on local and world
stages and often by the same players who customize their
approach depending on the context.
The vast majority of biotechnology products approved to
date are in the area of agronomic traits most specically to
protect against biotic stress. The principal focus in the immediate future will remain on agronomic traits, especially the
area of pest control but with an increasing interest in abiotic
stress tolerance, which is gaining prominence as external
pressures from climate change to land use is challenging
productivity. In 2013, 175.2 million hectares of biotech crops
were grown globally, at an annual growth rate of 3%, up 5
million from 170 million hectares in 2012. Of the 18 million
farmers who grew biotechnology crops in 2013, more than
16.5 million (90%) were in developing countries, which
produced more global biotechnology crops than industrial
countries (52% vs. 48%), and considerable more emerging
economies (19% vs. 8%) grew these crops (James, 2014).
More than 7.5 million small farmers in China and another 7.3
million small farmers in India collectively planted a record
14.5 million hectares of biotechnology crops (Figure 1;
James, 2014). In 2013, Bangladesh approved their rst genetically modied (GM) crop Bt eggplant. The Sudan became
the fourth country in Africa, after South Africa, Burkina Faso,
and Egypt, to commercialize a biotechnology crop Bt cotton
in 2012. Iran and Cuba also planted GM crops, but it is
challenging to document numbers for these countries. In
2010, Pakistan planted Bt cotton, as did Myanmar, and notably Sweden, the rst Scandinavian country to plant a biotechnology crop, planted Amora, a potato with high
amylose starch for industrial applications. Germany briey
resumed adoption of biotechnology crops by planting Amora
in 2010. However, both ceased after Amora was pulled from
the market in 2012. BASF cited opposition to the technology
as their reason for withdrawing the potato. Currently, only one
GMO crop is grown commercially in Europe an insect-resistant variety of maize developed by Monsanto. It is sown on
approximately 100 000 ha (247 000 acres) of farmland,
mainly in Spain.
71
#22
Portugal
<0.05 million ha
#16
Spain*
0.1 million ha
#24
Crech Republic
<0.05 million ha
#27
Slovakia
<0.05 million ha
#26
Romania
<0.05 million ha
#9
Pakistan*
2.8 million ha
Canola, maize,
soybean, sugar beet
Maize
Maize
Maize
Maize
Maize
Cotton
#6
China*
4.2 million ha
#1
USA*
70.1 million ha
Cotton, papaya,
poplar, tomato,
sweet pepper
Maize, soybean,
cotton, canola,
sugar beet, alfalfa
papaya, squash
#4
India*
11.0 million ha
#23
Cuba
<0.05 million ha
Maize
Cotton
#15
Myanmar*
0.3 million ha
#17
Mexico*
0.1 million ha
Cotton
Cotton, soyabean
#12
Philippines*
0.8 million ha
#21
Honduras
<0.05 million ha
Maize
Maize
#13
Australia*
0.6 million ha
#25
Costa Rica
<0.05 million ha
Cotton, canola
Cotton, soybean
#19
Sudan*
0.1 million ha
#18
Colombia*
0.1 million ha
Cotton, maize
Cotton
#11
Bolivia*
1.0 million ha
#14
Burkina Faso*
0.5 million ha
Soybean
Cotton
#20
Chile*
<0.05 million ha
#7
Paraguay*
3.6 million ha
#3
Argentina*
3.6 million ha
#10
Uruguay*
1.5 million ha
#2
Brazil*
40.3 million ha
#8
South Africa*
2.9 million ha
Soybean, maize
Figure 1 Adapted from James, C., 2013. Global Status of Commercialized Biotech/GM Crops: 2012. ISAAA Brief No.44. Ithaca, NY: International
Service for the Acquisition of Agri-biotech Applications. Available at: http://www.isaaa.org/ (accessed 24.02.13).
72
is the principal staple for much of the world and maize is the
largest animal feed source. Bt rice has the potential to increase
yields up to 8%, decrease pesticide use by 80% (17 kg ha1),
and generate US$4 billion in benets annually (James, 2011).
The phytase approval is a major step forward in approvals as it
is the rst transgenic since the FLAVR SAVR tomato focusing
on a quality trait. However, it is far more than this, both
literally and guratively, as this single trait addresses several
issues from nutritional to environmental ones as expanded on
later. Two further quality traits are under consideration for
deregulation: the Arctic apple, which has been modied to
resist oxidation when the apple is cut and the injured cells are
exposed to oxygen activating the polyphenol oxidase (PPO)
gene. To achieve this effect Okangan have co-expressed PPO
genes and have effectively achieved reduced oxidation by silencing the endogenous PPO gene (Carter, 2012). The second
is JR Simplots reduced acrylamide potato, described below.
The rst GM crop to be released for commercial cultivation
in India was Bt cotton, developed by the Maharashtra Seed
Company (Mahyco) in partnership with Monsanto. The approval, which was given in 2002, came after several years of
eld trials following the biosafety procedures laid down by the
government. Three cotton hybrids were granted permission for
eld sowing in six states for 3 years. For the rst season, farmer
demand for Bt cotton seed was very high; it is estimated that
44 500 ha of certied Bt cotton were planted by nearly 55 000
farmers (Choudhary and Gaur, 2008). However, the initial
events thrived in regions that resembled the area in which they
were originally developed but did not perform very well in
growing regions with disparate climate challenges. It was not
until the trait was introgressed into locally adapted varieties
that Bt cotton thrived in all growing regions. Between 2005
and 2006 the biggest impact of this approach was realized.
From 3 Bt cotton hybrids in 2002 to 62 in 2006, the rapid
deployment of Bt cotton hybrids based on different agroclimatic conditions resulted in decreased insecticide sprays by
39% and increased yields 31%, resulting in increased prot per
hectare of 88% or US$250. Over this period of rapid deployment, the average cotton yields increased from 308 kg ha1 to
450 kg ha1 of lint (of this increase, 50% could be attributed
to Bt technology). Over this period raw cotton exports also
rose from 0.9 million bales in 2005 to 4.7 million by 2006
and 5.9 by 2007. By 2009, 5.6 million resource-poor farmers
in India planted 8.4 million hectares of Bt cotton, equivalent
to 87% of the 9.6 million hectare national cotton crop. The
increase from 50 000 ha when Bt cotton was rst commercialized in 2002 to 8.4 million hectares in 2009 represents
an unprecedented 168-fold increase in 8 years (Choudhary
and Gaur, 2010). Between 2002 and 2008, Bt cotton generated
economic benets valued at US$5.1 billion for farmers, halved
insecticide requirements, contributed to the doubling of yield,
and transformed India from a cotton importer to a major exporter. Choudhary and Gaur (2010) contended that the deployment of Bt cotton over the years has resulted in India
becoming the number one exporter of cotton globally as well
as the second largest cotton producer in the world.
However, despite the success of Bt cotton, the expected
successful commercialization of Bt eggplant never materialized
as an effective opposition managed to scupper its approval. Bt
eggplant, or brinjal as it is referred to in India, was found to be
73
effective against fruit and shoot borer (FSB), with 98% insect
mortality in shoots and 100% in fruits compared with less
than 30% mortality in non-Bt counterparts. The multilocation
research trials conrmed that Bt brinjal required, on average,
77% less insecticides than non-Bt counterparts for control of
FSB and 42% less for the control of all insect pests of brinjal.
The benets of Bt brinjal translate to an average increase of
116% in marketable fruits over conventional hybrids and
166% increase over popular open-pollinated varieties. Furthermore, the signicant decrease in insecticide usage reduced
the farmers exposure to insecticides and results in a substantial decline in pesticide residues on brinjal fruits (Bricknel,
2010). Scientists have estimated that Bt brinjal will deliver
farmers a net economic benet ranging from US$330397 per
acre with national benets to India exceeding US$400 million
per year. However, in February 2010 the environmental minister announced a 6-month moratorium citing, There is no
overriding food security argument for Bt brinjal. Our objective
is to restore public condence and trust in Bt brinjal, clearly
articulating the fact that the decision was not based on scientic analysis or risk assessment.
A number of other multi-institutional projects have also
been launched in India, including the development of transgenics for resistance to geminiviruses in cotton, mungbean,
and tomato; resistance to rice tungro disease; development of a
nutritionally enhanced potato with a balanced amino acid
composition; and development of molecular methods for
heterosis breeding. Other transgenic crops that are awaiting
approval for commercial cultivation include transgenic herbicide-tolerant mustard hybrids and nutritionally enhanced
potato varieties. However, despite the resounding success of Bt
cotton, given the experience with Bt brinjal, it is difcult to be
optimistic about the prospects for commercialization of food
crops. To reinforce this notion in 2012 an interim report of the
technical expert committee (TEC) appointed by the Supreme
Court of India recommended a ban on open eld trials, including any ongoing trials, for 10 years, which will result in a
serious impact on the application of biotechnology to Indian
agriculture. However, in October 2012 the Supreme Court
decided that before considering this interim recommendation
they would seek the views of all stakeholders, including the
agriculture ministry and the GM crop industry, on the issue
(Times of India, 2012).
A similar context applies to another potentially valuable
disease resistance system. Late potato blight is one of the most
devastating plant diseases. It is caused by the oomycete Phytophtera infestans, a pathogen of the potato and, to a lesser
degree, the tomato. No potato has been bred to date that has
any measure of resistance to the pathogen. Approximately 15
20% of annual global crop yields of approximately 330 million tonnes fall victim to the disease (and up to 75% in many
LDCs) that was introduced to Europe in the mid-nineteenth
century and was responsible for the Irish potato famine. The
International Potato Center (Lima, Peru) estimates the annual
value of these losses to be US$35 billion, excluding losses
from tomato infestations. In the potato, Solanum tuberosum,
there are four main dominant genes for resistance to blight
infection, R1 through R4. An additional 7 genes were identied, 5 of which are alleles of the complex R3 locus (for a total
of 11 dominant R genes). Hybridization with wild Mexican
74
trait event developed through collaboration between Monsanto and Dow, takes advantage of multiple modes of insect
protection and herbicide tolerance against above- and belowground insects and provides broad herbicide tolerance, including Yieldgard VT Triple (Monsanto), Herculex Xtra (Dow),
RoundUp Ready 2 (Monsanto), and Liberty Link (Dow). It is
currently available for corn, but cotton, soybean, and specialty
crop variations are in the pipeline. It is estimated that this
should require only 5% refuge acres as opposed to the 20%
required of older technologies to militate against pest tolerance (Choudhary and Gaur, 2010).
On the second area of agronomic traits, namely abiotic
stress, there is a meta issue that overlays much of the individual efforts, that is, climate change. This poses a real challenge in terms of available agricultural land and fresh water
use. Apart from the obvious effects of climate change, the
decline of crop yields, ocean acidication, poor plant nutrition
and abiotic stress, population displacement, and threatened
ecosystems are effects underlined by the Stern Report (2006)
as potential consequences of climate change. In addition, there
are also broader, more systemic effects of drought beyond
food insecurity, such as decreased household income, the loss
of assets due to slaughter of livestock, health threats due to the
lack of water for hygiene and household uses, environmental
degradation, and less sustainable land management. These
effects must be considered in the light of growing population
levels. In order to feed the overall population, the world will
have to double its rate of agricultural production over the next
25 years, despite having already quadrupled it in the last 50
years. It is estimated that merely 10% of worlds arable land
may be categorized as free from stress. The rapid change in
environmental conditions is likely to override the adaptive
potential of plants. Such abnormal environmental parameters
include drought, salinity, cold, freezing, high temperature,
waterlogging, high light intensity, ultraviolet (UV) radiation,
nutrient imbalances, metal toxicities, and nutrient deciencies,
which are collectively termed as abiotic stress. Severe drought
accounts for half the worlds food emergencies annually. In
2003, the World Food Program spent US$565 million in response to drought in SSA (Anderson, 2005). In this context,
solutions must be developed to adapt crops to existing but
also evolving conditions, such as deteriorating soils or harsher
conditions, such as cold, heat, drought, and salinity.
The agriculture sector is both a contributor to and provider
of potential solutions to this phenomenon. It impacts two of
the principal components of climate change greenhouse
gases and water. Agriculture is a major source of the former
emissions. Practices such as deforestation, cattle feedlots, and
fertilizer used currently account for approximately 25% of
greenhouse gas emissions. When broken down in total, this
amounts to 14% of carbon dioxide emissions, 48% of methane, and 52% of nitrous oxide emissions (Stern, 2006). In
addition, this sector uses a signicant amount of available
fresh water; approximately 70% of the water currently consumed by humans is used in agriculture, and this is likely to
increase as temperatures rise. The impact between resourcepoor LDCs and developed countries is likely to be asymmetrical with much greater impacts on resource-poor farmers.
Given the potential impacts of climate change on the range
and extent of agricultural productivity and the impact of
agricultural practice itself on global warming, effective technology should play a substantial part in militating against
climate change. This is especially relevant in emerging countries where producers and consumers are more subject to the
mercy of the vagaries of climate uctuations than in the west
where there is greater capability of responding to the effects
and managing resources. Green biotechnology offers a set of
tools that can help producers to limit greenhouse gas emissions as well as adapting their agricultural techniques to
shifting climates. The three major contributions of green biotechnology to the mitigation of the impact of climate change
are greenhouse gas reduction, crop adaptation (environmental
stress and changing niches) crop protection, and yield increase
in less desirable and marginal soils.
On the rst of these issues, greenhouse gas reduction in
addition to carbon dioxide, agriculture contributes two of the
other major greenhouse gases, indeed one of them, nitrous
oxide, has a global warming potential of approximately 300
times that of carbon dioxide. In addition, nitrous oxides stay
in the atmosphere for a considerable period. Nitrous oxide is
produced through bacterial degradation of applied nitrogen
fertilizer, which can also contribute to eutrophication at
ground level, so its reduction is desirable on several levels.
However, nitrogen is essential for crop production because it is
quantitatively the most essential nutrient for plants and a
major factor limiting crop productivity. One of the critical
steps limiting the efcient use of nitrogen is the ability of
plants to acquire it from applied fertilizer. Therefore, the development of crop plants that absorb and use nitrogen more
efciently can serve both the plant and the environment. Arcadia Biosciences of Davis, CA developed nitrogen-efcient
crops by introducing barley AlaAT (alanine aminotransferase)
into both rice and canola. In a report, Arcadias Nitrogen Use
Efciency (NUE) technology produces plants with yields that
are equivalent to conventional varieties but which require
signicantly less nitrogen fertilizer because the AlaAT gene
allows more efcient use. Compared with controls, transgenic
plants also demonstrated signicant changes in key metabolites and total nitrogen content, conrming increased nitrogen
uptake efciency. This technology has the potential to reduce
the amount of nitrogen fertilizer that is lost by farmers every
year due to leaching into the air, soil, and waterways (Omanya
et al., 2008). In addition to environmental pressures, nitrogen
costs can represent a signicant portion of a farmers input
costs and can signicantly impact farmer protability. Farmers
spend US$60 billion annually for 150 million tonnes of fertilizer (Svoboda, 2008). The technology has been licensed to
DuPont for maize and to Monsanto for application in canola.
The second area where green technology can help in a
changing climate is crop adaptation to environmental stress
and changing niches. Under stress, plants divert energy into
survival instead of producing biomass and reproduction, so
addressing this impact should have substantial effect on yield.
In addition, improved stress tolerance allows an expanded
growing season, especially earlier planting, and further reduces
yield variability and grower nancial risk. The most critical of
these stresses is water. One of the most effective methods of
addressing water limitation problems, namely irrigation, unfortunately is also one of the major causes of arable land
degradation. It is estimated that 24.7 million acres of farmland
75
76
severe water stress. DroughtGard maize is the rst commercially available transgenic drought-tolerant crop. Hybrid
seed sold under this trademark combines a novel transgenic
trait (based on the bacterial cspB gene, an ribonucleic acid
(RNA) chaperone, which helps to maintain normal physiological performance under stress by binding and unfolding
RNA molecules so that they can function normally) with
Monsantos optimized conventional breeding program. In
eld trials using this approach, maize yields have increased
under water stress by up to 30%. The yield gain of this variety
under drought appears to occur due to slowing of growth,
specically under drought stress such that existing soil moisture is saved for the critical period surrounding owering, resulting in less kernel abortion, higher harvest index, and
greater yield (Castiglioni et al., 2008).
Other approaches include modication of individual genes
involved in stress response and cell signaling. For example,
drought-tolerant canola engineered to reduce the levels poly
(ADP-ribose) polymerase, a key stress-related protein in many
organisms, shows relative yield increases of up to 44%
compared with control varieties. A subset of the transcription
factors, homeodomain leucine zipper proteins (HDZip), plays
a role in regulating adaptation responses, including developmental adjustment to environmental cues, such as water stress
in plants (Deng et al., 2006). One of these effectors is abscisic
acid (ABA), an important plant regulator controlling many
environmental responses, including stomata movement that is
itself modulated by the DREB elements. Some work is being
done on modifying HDZip directly, whereas other works aim
to modify it indirectly, for example, downregulating farnesyltransferase, a signaling system in the production of ABA and
stomata control, which results in stomata closure and water
retention.
Eduardo Blumwald is also working on modifying basic
acid to enhance the tolerance of plants to water decit by
delaying the drought-induced leaf senescence and abscission
during the stress episode. Using tobacco plants expressing an
IPT gene under the control of a stress- and maturation-induced
promoter they showed that delayed drought-induced leaf
senescence resulted in remarkable drought-tolerant phenotypes as well as minimal yield loss when plants were watered
with only 30% of the water used under controlled conditions
(Zhang, 2010). This is now being introduced into rice, among
other crops. This work is being done in conjunction with Arcadia Biosciences. In addition, Bayer CropScience, Pioneer HiBred, BASF, and Dow, among others, are conducting research
on maize, cotton, canola, and rice to develop a new generation
of stress-tolerant, high-performance crop varieties. Clearly,
stress-tolerant traits are of paramount importance in LDCs,
especially sub-Saharan Africa and Asia. Major efforts are already underway on this front. The partnership, known as
Water Efcient Maize for Africa (WEMA), was formed in response to a growing call by African farmers, leaders, and scientists to address the devastating effects of drought on smallscale farmers (Foundation, 2007). Frequent drought leads to
crop failure, hunger, and poverty, which climate change can
only aggravate.
At the other end of the spectrum of climate change impact
is ooding due to changing rain patterns and rising sea levels.
This is already a major cause of rice crop loss. It is estimated
77
Table 1
Examples of crops in research and development with nutritionally improved traits intended to provide health benets for consumers
and animalsa
Trait
Canola (lysine)
Lupin (methionine)
Maize (lysine and methionine)
Potato (methionine)
Sorghum (lysine)
Soybean (lysine and tryptophan)
Potato (inulin)
Rice (amylase)
References
Carbohydrates
Fructans
Frustose, rafnose,
and stachyose
Inulin
Starch
Apple ( stilbenes)
Alfalfa ( resveratrol)
Kiwi ( resveratrol)
Maize (avonoids)
Potato (anthocyanin and alkaloid glycoside, and solanin)
Rice (avonoids and resveratrol)
78
Table 1
Continued
Trait
Mineral availabilities
References
Soybean (avonoids)
Tomato ( resveratrol, chlorogenic acid,avonoids, and
stilbeneanthocynanins)
Wheat (caffeic and ferulic acids and resveratrol)
Alfalfa (phytase)
Lettuce (iron)
Rice (iron)
Maize (phytase and ferritin)
Soybean (phytase)
Wheat (phytase)
Yu et al., 2003
Giovinazzo et al., 2005; Niggeweg et al., 2004; Muir et al.,
2001; Rosati, 2000; Gonzali et al., 2009
UPI, 2002
Austin-Phillips et al., 1999
Goto et al., 2000
Lucca et al., 2002
Drakakaki, 2005; Han, 2009
Denbow et al., 1998
Brinch-Pedersen et al., 2000, 2006
Excludes protein/starch functionality, shelf life, taste/aesthetics, ber quality, and allergen/toxin reduction traits.
Source: Modied from ILSI (International Life Sciences Institute), 2004a. Nutritional and safety assessments of foods and feeds nutritionally improved through biotechnology.
Comprehensive Reviews in Food Science and Food Safety 3, 35104. Available at: http://members.ift.org/NR/rdonlyres/27BE106D-B616-4348-AE3A-091D0E536F40/0/
crfsfsv3n2p00350104ms20040106.pdf (accessed 03.05.14); ILSI (International Life Sciences Institute), 2004b. Nutritional and safety assessments of foods and feeds nutritionally
improved through biotechnology: An executive summary. Journal of Food Science 69, CRH62CRH68; ILSI (International Life Sciences Institute), 2008. Nutritional and safety
assessments of foods and feeds nutritionally improved through biotechnology: Case studies. Comprehensive Reviews in Food Science and Food Safety 7, 5099. Reviewed in
Newell-McGloughlin, M., 2010. Modifying agricultural crops for improved nutrition. New Biotechnology 27 (5), 494504.
evidence that early food regimes can affect health in later life,
for example, some children that survived famine conditions in
certain regions of Africa grew into adults battling obesity and
related problems presumably due to the selective advantage of
the thrifty gene in their early food-stressed environment becoming a hazard during more abundant times, especially if
later diets are calorie dense.
Functional food components are of increasing interest in the
prevention and/or treatment of a number of the leading causes
of death, including but not limited to cancer, diabetes, cardiovascular disease, and hypertension. Many food components are
known to inuence the expression of both structural genes and
transcription factors in humans (Go et al., 2005; Mazzatti et al.,
2008). Examples of these phytochemicals are listed in Table 2
(reviewed in Newell-McGloughlin, 2010). The large diversity of
phytochemicals suggests that the potential impact of phytochemicals and functional foods on human and animal health is
worth examining as targets of biotechnology efforts. From a
health perspective, plant components of dietary interest can be
broadly divided into four main categories, which can be further
broken down into positive and negative attributions for human
nutrition, macronutrients (proteins, carbohydrates, lipids (oils),
and ber), micronutrients (vitamins, minerals, and phytochemicals), anti-nutrients (substances such as phytate that limit
bioavailability of nutrients), allergens, intolerances, and toxins.
There are approximately 25 000 metabolites (phytochemicals), of the 200 000 or so produced by plants, with known
effect in the human diet (Go et al., 2005). Analysis of these
metabolites (most specically metabolomic analysis) is a
valuable tool in better understanding of what has occurred
during crop domestication (lost and silenced traits) and in
designing new paradigms for more targeted crop improvement
that is better tailored to current needs (Hall et al., 2008). In
addition, with modern techniques, we have the potential to
seek out, analyze, and introgress traits of value that were
limited in previous breeding strategies. Research to improve
the nutritional quality of plants has historically been limited
by a lack of basic knowledge of plant metabolism and the
Table 2
79
Class/components
Sourceb
Carotenoids
Alpha-carotene
Carrots
Beta-carotene
Lutein
Lycopene
Zeaxanthin
Dietary ber
Insoluble ber
Beta glucanc
Wheat bran
Oats
Soluble berc
Whole grainsc
Collagen hydrolysate
Psyllium
Cereal grains
Gelatin
Fatty acids
Omega-3 fatty acids docosahexaenoic acid/
eicosapentaenoic acid
Conjugated linoleic acid
Flavonoids
Anthocyanidins: cyanidin
Berries
Hydroxycinnamates
Wheat
Flavanones
Citrus
Flavones: quercetin
Fruits/vegetables
Phenolics
Stilbenes Resveratrol
Grapes
Epicatechin
Cacao
Plant Stanols/sterols
Stanol/sterol esterc
Prebiotic/probiotics
Fructans, Inulins, and Fructooligosaccharides
(FOS)
Lactobacillus
Saponins
Soybean Protein
80
Table 2
Continued
Class/components
Sourceb
Phytoestrogens
Isoavones Daidzein and Genistein
Lignans
Suldes/thiols
Diallyl sulde
Cruciferous vegetables
Tannins
Proanthocyanidins
Macronutrients: Protein
The FAO estimates that 850 million people worldwide suffer
from undernutrition, of which insufcient protein in the diet
is a signicant contributing factor (FAO, 2004, 2011). Protein
energy malnutrition is the most lethal form of malnutrition
and affects every fourth child worldwide according to the
WHO (2006). Most plants have a poor balance of essential
amino acids relative to the needs of animals and humans. The
cereals (maize, wheat, rice, etc.) tend to be low in lysine,
whereas legumes (soybean and peas) are often decient in the
sulfur-rich amino acids, methionine and cysteine. Successful
examples of improving amino acid balance to date include
high-lysine maize (Eggeling et al., 1998; OQuinn et al., 2000)
canola, and soybeans (Falco et al., 1995). Free lysine is signicantly increased in high-lysine maize by the introduction of
the dapA gene (cordapA) from Corynebacterium glutamicum,
which encodes a form of dihydrodipicolinate synthase that is
insensitive to lysine feedback inhibition. Consumption of
foods made from these crops potentially can help to prevent
malnutrition in developing countries, especially among
children.
Another method of modifying storage protein composition
is to introduce hetero- or homologous genes that code for
proteins containing elevated levels of the desired amino acid,
such as the sulfur-containing amino acids (methionine and
cysteine) or lysine. An interesting solution to this is to create a
completely articial protein containing the optimum number
of the essential amino acids methionine, threonine, lysine, and
leucine in a stable, helical conformation designed to resist
81
82
SCN, 2004). Even mild levels of micronutrient malnutrition may damage cognitive development and lower disease
resistance in children and increase incidences of childbirth
mortality. The costs of these deciencies, in terms of diminished quality of life and lives lost, are large (Pfeiffera and
McClafferty, 2007). Such deciencies prevent children from
reaching their full potential as adults; malnutrition, especially
during the 1000 days between pregnancy and age 2 years,
can lead to irreversible physical stunting and cognitive impairment. However, children who are well nourished are able
to grow, learn, and prosper. They achieve more in school, are
better able to survive illnesses, and tend to earn more as adults
(Kraemer, 2012). The clinical and epidemiological evidence is
clear that select minerals (iron, calcium, selenium, and iodine)
and a limited number of vitamins (folate, vitamins E, B6, and
A) play a signicant role in maintenance of optimal health and
are limiting in diets (Asensi-Fabado, 2010).
As with macronutrients, one way to ensure an adequate
dietary intake of nutritionally benecial phytochemicals is to
adjust their levels in plant foods. Using various approaches,
including genomics, vitamin E levels are being increased in
several crops, including soybean, maize, and canola, whereas
rice varieties are being developed with the enhanced vitamin A
precursor, beta-carotene, to address vitamin A deciency that
leads to macular degeneration and impacts development.
Golden Rice II accumulates up to 37 mg of beta-carotene per
gram of rice (23-fold more than the original). This betacarotene has been shown to be bioavailable in sufcient
amounts that 100200 g per day can provide adequate provitamin A to ameliorate against deciency (Tang et al., 2009).
It is estimated that Golden rice will nally be approved for
commercialization in the Philippines by 2014. A number of
other staple crops on which many depend almost exclusively
for calories have been produced enriched in beta-carotene,
including maize, cassava, millet, and sorghum (Harjes et al.,
2008; Welsch et al., 2010; Yan et al., 2010). Cassava is being
eld tested in Nigeria. Ameliorating another major deciency
in LDCs, namely minerals such as iron and zinc, has also been
addressed. Iron is the most commonly decient micronutrient
in the human diet, and iron deciency affects an estimated 1 to
2 billion people. Anemia, characterized by low hemoglobin, is
the most widely recognized symptom of iron deciency, but
there are other serious problems, such as impaired learning
ability in children, increased susceptibility to infection, and
reduced work capacity. Drakakaki et al. (2005) demonstrated
endosperm-specic co-expression of recombinant soybean
ferritin and Aspergillus fumigatus phytase in maize, which resulted in signicant increases in the levels of bioavailable iron.
A similar end was also achieved with lettuce (Goto et al.,
2000). The Africa Biofortied Sorghum (ABS) Project developed the worlds rst sorghum transformation system as
well as the rst golden sorghum that had elevated provitamin
A levels, reduced phytate, raised grain protein prole, and
raised absorbability of zinc and iron (Blaine, 2011).
A rather interesting approach was taken by Connolly et al.
(2008) to increase the levels of calcium in crop plants by using
a modied calcium (Ca)/proton antiporter (known as short
cation exchanger 1 (sCAX1) to increase Ca transport into
vacuoles. They also demonstrated that consumption of such
Ca-fortied carrots results in enhanced Ca absorption. This
83
Micronutrients: Phytochemicals
Unlike for vitamins and minerals, the primary evidence for the
health-promoting roles of phytochemicals comes from epidemiological studies, and the exact chemical identity of many
active compounds has yet to be determined. However, for
select groups of phytochemicals, such as non-provitamin A
carotenoids, glucosinolates, and phytoestrogens, the active
compound or compounds have been identied and rigorously
studied. Epidemiologic studies have suggested a potential
benet of the carotenoid lycopene in reducing the risk of
prostate cancer, particularly the more lethal forms of this
cancer. Five studies support a 3040% reduction in risk associated with high tomato or lycopene consumption in the
processed form in conjunction with lipid consumption, although other studies with raw tomatoes were not conclusive
(Giovannucci, 2002). As carotenoids are lipid soluble and
cooking breaks down carotenoid-binding proteins, this is not
an unexpected outcome. In a study by Mehta et al. (2002) to
modify polyamines to retard tomato ripening they found an
unanticipated enrichment in lycopene with levels up by 2- to
3.5-fold compared with conventional tomatoes. This is a
substantial enrichment, exceeding that so far achieved by
conventional means. This approach may work in other fruits
and vegetables. Flavonoids meanwhile are soluble in water,
and foods containing both water-soluble and fat-dissolved
antioxidants are considered to offer the best protection against
disease. Anthocyanins offer protection against certain cancers,
cardiovascular disease, and age-related degenerative diseases.
There is evidence that anthocyanins also have anti-inammatory activity, promote visual acuity, and hinder obesity and
diabetes. Both Gonzali et al. (2009) and Butelli et al. (2008)
used snapdragon transcription factors to achieve high levels of
the reactive oxygen scavengers, anthocyanins expression in
tomatoes. In a pilot test, the lifespan of cancer-susceptible
mice was signicantly extended when their diet was supplemented with the purple tomatoes compared with supplementation with normal red tomatoes.
Other phytochemicals of interest include related polyphenolics such as resveratrol, which has been demonstrated to
inhibit platelet aggregation and eicosanoid synthesis in addition to protecting the sirtuins, genes implicated in DNA
modication and life extension; avonoids, such as tomatoes
expressing chalcone isomerase that show increased contents of
the avanols rutin and kaempferol glycoside; glucosinolates
and their related products, such as indole-3 carbinol (I3C);
catechin and catechol; isoavones, such as genistein and
daidzein; anthocyanins; and some phytoalexins. Table 1
summarizes activities in improving nutritional characteristics
of various crops worldwide. A comprehensive list of phytochemicals are outlined in Table 2 (reviewed in NewellMcGloughlin, 2010). To reiterate, although there is a growing
84
Protecting Plants
Plants produce many defense strategies to protect themselves
from predators. Many, such as resveratrol and glucosinate,
which are primarily pathogen-protective chemicals, also have
demonstrated benecial effects for human and animal health.
Many, however, have the opposite effect. For example, phytate,
a plant phosphate storage compound, is considered an antinutrient as it strongly chelates iron, calcium, zinc, and other
divalent mineral ions, making them unavailable for uptake.
Nonruminant animals generally lack the phytase enzyme
needed for digestion of phytate. Poultry and swine producers
add processed phosphate to their feed rations to counter this.
Excess phosphate is excreted into the environment, resulting in
water pollution. When low-phytate soybean meal is utilized
along with low-phytate maize for animal feeds the phosphate
excretion in swine and poultry manure is halved. A number of
groups have added heat- and acid-stable phytase from A.
fumigatus inter alia to make the phosphate and liberated ions
bioavailable in several crops (Potrykus, 1999). To promote the
reabsorption of iron, a gene for a metallothionein-like protein
has also been engineered. Low-phytate maize was commercialized in the United States in 1999 (Wehrspann, 1998).
In November 2009, the Chinese company Origin Agritech
announced the nal approval of the worlds rst GM phytaseexpressing maize (Han, 2009). Research indicates that the
protein in low-phytate soybeans is also slightly more digestible
than the protein in traditional soybeans. In a poultry-feeding
trial, better results were obtained using transgenic plant material than with the commercially produced phytase supplement (Keshavarz, 2003). Poultry grew well on an
engineered alfalfa diet without any inorganic phosphorus
supplement, which shows that plants can be tailored to increase the bioavailability of this essential mineral. A similar
effect was achieved in wheat by a Danish group where temperature-tolerant phytase resisted boiling (Brinch-Pedersen
et al., 2006).
One of the rst products modied for safety was submitted
for petition for determination of nonregulated status in 2013.
The submission was by JR Simplot for a potato that has three
specic modications for quality improvement. They use what
they term Innate technology, basically utilizing RNAi (to silence genes related to expression of black spot bruise, asparagine, and reducing sugars in tubers).
The three traits modied are important from a commercial
perspective as they greatly improve the quality of the potato,
making them more appealing to both producers and consumers. The rst of those traits, reduced black spot from
bruising and browning, is achieved through RNAi suppression
of PPO effectively reducing oxidation by silencing the endogenous PPO gene. Not alone is this more appealing for the
consumer, it will help to reduce waste for growers as fewer
potatoes will be discarded.
(McCue et al., 2003). Work has also been done to reduce cyanogenic glycosides in cassava through expression of the cassava enzyme hydroxynitrile lyase in the roots (Siritunga and
Sayre, 2003). When disarming plants natural defenses in this
way one must be aware of potentially increased susceptibility
to pests, diseases, and other stressors, so that the recipient
germplasm should have input traits to counter this.
Improvement of crop nutritional quality is a technical
challenge hampered by a lack of basic knowledge of plant
metabolism and the need to resolve the complexity of intersecting networks of thousands of metabolic pathways. With
the tools now available through the eld of genomics, proteomics, lipomics, glycobiomics, metabolomics, and bioinformatics, we have the potential to study and manipulate
genes and pathways at the metalevel while simultaneously
studying the expression and interaction of transgenes on tens
of thousands of endogenous genes. With these newly evolving
tools we are beginning to dissect the global effects of metabolic engineering on metabolites, enzyme activities, and
uxes. For essential macro- and micronutrients that are limiting in various regional diets, the strategies for improvement
are clear and the concerns, such as pleiotropic effects and safe
upper limits, are easily addressed. However, for many putative
health-promoting phytochemicals, clear links with health
benets are yet to be demonstrated. In addition, one must be
careful when extrapolating attributes from an individual substance acting independently to that substance acting within a
complex milieu. However, if such links can be established it
will make it possible to identify the precise compound or
compounds to target and which crops to modify to achieve the
greatest nutritional impact and health benet. With rapidly
emerging technologies the increase in our understanding and
ability to manipulate plant metabolism during the coming
decades should place plant researchers in the position of being
able to modify the nutritional content of major and minor
crops to improve many aspects of human and animal health
and well-being.
Barriers to Introduction
Commercialization of the rst generation of products of recombinant DNA technology was another facet in a long history of human intervention in nature for agricultural and food
production purposes. Hence, the same parameters of riskbased assessment should apply. Commercialization of products must be undertaken within a regulatory framework that
ensures adequate protection of the consumer, the environment, and alternate production systems while not stymieing
innovation. The rst generation of such crops focused largely
on input agronomic traits; the next generation will focus more
on value-added output traits.
There is almost universal agreement that innovation is essential for sustaining and enhancing agricultural quality and
productivity. There also would be general concurrence that this
involves at some level new, science-based products and processes that contribute reliable methods for improving quality,
productivity, and environmental sustainability. Most of the
innovative technologies that have been applied to production
agriculture have come into common usage without much
85
86
imagine many of the traits described ever reaching the marketplace. This discourages research on anything but the most
mundane of crops and traits and is a real disincentive to creative research. For all intent and purposes there is just one trait
from a public institution that has successfully traversed the
regulatory mineelds and been translated into a commercially
viable commodity and that is the viral coat protein protection
system initially developed for the papaya ringspot virus
(PRSV) pandemic in Hawaii. Papaya is a major tropical fruit
crop in the Asian region. However, production in many
countries is set back by the prevalence of the PRSV disease as
well as postharvest losses. The PRSV-resistant papaya, based on
RNAi suppression of the coat protein expression, literally
saved the US$17 million economy in Hawaii and although the
disease is of signicant importance in Taiwan and other SE
Asian countries, it has yet to be approved. Coat protein-based
resistance is a demonstration of what is known as PTGS later
determined to be RNAi, as described earlier. A 20-year effort to
combat plum pox virus (PPV) disease through PTGS resistance
paid off. In 1990, the USDA/Agricultural Research Service
(ARS) scientists began their efforts with a papaya ringspot virus
coat protein gene obtained from Dennis Gonsalves. This gene
shows 70% homology to the plum pox gene and has been
used to control other viruses similarly related to papaya ringspot. Based on this, the USDA developed a transgenic plum
line C5, which contains multiple copies of the PPV-CP transgene and is stably resistant to the virus (Scorza et al., 2009)
This has been deregulated by Animal and Plant Health Inspection Service (APHIS) and rather incongruously the construct within the trees is registered as a pesticide under EPA
FIFRA (Federal Insecticide, Fungicide, and Rodenticide Act)
and nurseries that produce them are designated pesticide
producing establishments (U.S. Environmental Protection
Agency, 2010). However, irrespective of the mechanism, it
is important that resistance based on a single gene is managed
well and alternate control mechanisms are introduced to
reduce pressure on the development of viral resistance.
Other approaches include expression of the genes for RNAreplicating enzymes of the virus, expression of satellite RNA,
replicating RNA molecules that are molecular parasites of the
virus, or the use of protease inhibitors to interfere with processing of the viral proteins.
Rather interestingly, Gonsalves (2003) reported that the
transgenic papaya has helped growers to raise nontransgenic
papaya in Puna by reducing the overall virus pressure in Puna
and serving as buffer zones, suggesting that virus-resistant
transgenic crops can directly control the virus and also serve as
a tool to minimize infection to nontransgenic crops that are
grown in the area. It has been reported that organic papaya
growers now surround their plots with the transgenic rainbow
variety as the PTGS system proves to be a most effective
method to reduce the viral reservoir, thus protecting susceptible varieties through a mechanism that is similar to herd
immunity in mammalian systems (Summers, 2014). The late
blight resistant potatoes discussed above could feasibly provide the same cooperative resistance for organic potato farmers
in Europe, but as BASF has pulled its production in the
European Union, this cannot now be demonstrated. Research
by Hutchison et al. (2010) demonstrates a variation of this
halo effect for Bt maize. As noted to militate against the
87
88
Future Directions
As agriculture must adapt to rapidly changing needs and
growing conditions, we must become more effective at producing more or less with limited resources and only the tools
of biotechnology will allow us to bypass physiological and
environmental limitations to produce sufcient food, feed,
fuels, and ber on ever-diminishing arable land to meet everincreasing demand. The challenges going forward are foremost
technical as we strive to modify qualitative as opposed to
quantitative traits and intricate metabolic pathways and networks as opposed to single genes; the scientic hurdles to
achieve these aims are not trivial. However, with the tools now
coming on line in the elds of genomics, proteomics, metabolomics, and bioinformatics, we have the potential to make
major modications to introgress desirable traits. For example,
tools such as genome editing (using articial nucleases such as
Zn ngers, transcription activator-like effector nucleases, and
clustered regularly interspaced short palindromic repeats),
next-generation sequencing, RNAi, Tfs, minichromosomes,
non-integrating vectors, combinatorial transformation, epigenetic modication, network engineering, synthetic biology,
and systems biology will allow us to apply both reductive and
holistic approaches to identify, modify, introgress, and subsequently simultaneously study the expression and interaction
of transgenes on tens of thousands of endogenous genes in
elite germplasm backgrounds. With rapidly emerging technologies, the increase in our understanding of, and ability to,
manipulate plant metabolism during the coming decades
should place plant researchers in the position of being able to
modify crop traits to respond to the diverse needs from minimizing environmental impact to optimizing productivity and
quality output.
89
References
Abbadi, A., Domergue, F., Bauer, J., et al., 2004. Biosynthesis of very-long-chain
polyunsaturated fatty acids in transgenic oilseeds: Constraints on their
accumulation. Plant Cell 16, 27342748.
Agarwal, P.K., Agarwal, P., Reddy, M.K., Sopory, S.K., 2006. Role of DREB
transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell
Reports 25, 12631274.
Agius, F., Gonzalez-Lamothe, R., Caballero, J.L., et al., 2003. Engineering increased
vitamin C levels in plants by overexpression of a D-galacturonic acid reductase.
Nature Biotechnology 21, 177181.
Anai, T., Koga, M., Tanaka, H., et al., 2003. Improvement of rice (Oryza sativa L.)
seed oil quality through introduction of a soybean microsomal omega-3 fatty
acid desaturase gene. Plant Cell Reports 21, 988992.
Anderson, K., Ann Jackson, L., 2005. Some implications of GM food technology
policies for sub-Saharan Africa. Journal of African Economies 14 (3),
385410.
Arcadia Biosciences and Bioriginal Food and Science Corp, 2008. Enter Strategic
Alliance to Market High GLA Safower Oil. Business Wire. Available at: http://
www.arcadiabio.com/news/press-release/arcadia-biosciences-and-bioriginal-foodand-science-corp-enter-strategic-alliance (accessed 22.02.08).
Asensi-Fabado, M.A., Munn-Bosch, S., 2010. Vitamins in plants: Occurrence,
biosynthesis and antioxidant function. Trends in Plant Science 15, 582592.
Atanassov, A., Bahieldin, A., Brink, J., et al., 2004. To reach the poor Results
from the ISNAR-IFPRI Next Harvest study on GM crops, public research, and
policy implications. In: EPTD Discussion Paper. Washington, DC: Environment
and Production Technology Division, International Food Policy Research
Institute.
90
FAO (Food and Agriculture Organization of the United Nations), 2004. The State of
Food and Agriculture 20032004, Agricultural Biotechnology, Meeting the Needs
of the Poor? FAO Agricultural Series, vol. 35. Rome: FAO, pp. 1209.
FAO (Food and Agriculture Organization of the United Nations), 2011. The State of
Food Insecurity in the World 2011. FAO Agricultural Series. Rome: FAO.
Foundation, A.A.T., 2007. Combining Breeding and Biotechnology to Develop Water
Efcient Maize for Africa (WEMA).
Fraser, P.D., Romer, S., Kiano, J.W., et al., 2001. Elevation of carotenoids in tomato
by genetic manipulation. Journal of the Science of Food and Agriculture 81,
822827.
Froman, B., Ursin, V., 2002. Genetic modication of oils for improved health
benets: Production of long chain omega-3 fatty acids in plants. Abstracts of
Papers of the American Chemical Society 223, U35.
Galili, G., Galili, S., Lewinsohn, E., Tadmor, Y., 2002. Genetic, molecular, and
genomic approaches to improve the value of plant foods and feeds. Critical
Reviews in Plant Sciences 21, 167204.
German, J.B., Watkins, S.M., Fay, L.-B., 2005. Metabolomics in practice: Emerging
knowledge to guide future dietetic advice toward individualized health. Journal of
the American Dietetic Association 105, 14251432.
Giliberto, L., Perrotta, G., Pallara, P., et al., 2005. Plant manipulation of the blue
light photoreceptor cryptochrome 2 in tomato affects vegetative development,
owering time, and fruit antioxidant content. Plant Physiology 137, 199208.
Giovannucci, E., 2002. A review of epidemiologic studies of tomatoes, lycopene, and
prostate cancer. Experimental Biology and Medicine 227, 852859.
Giovinazzo, G., dAmico, L., Paradiso, A., et al., 2005. Antioxidant metabolite proles
in tomato fruit constitutively expressing the grapevine stilbene synthase gene.
Plant Biotechnology Journal 3, 5769.
Go, V.L.W., Nguyen, C.T.H., Harris, D.M., Lee, W.-N.P., 2005. Nutrient-gene
interaction: Metabolic genotype-phenotype relationship. Journal of Nutrition 135,
3016S3020S.
Gonzali, S., Mazzucato, A., Perata, P., 2009. Purple as a tomato: Towards high
anthocyanin tomatoes. Trends in Plant Science 5, 237241.
Goto, F., Yoshihara, T., Saiki, H., 2000. Iron accumulation and enhanced growth in
transgenic lettuce plants expressing the iron-binding protein ferritin. Theoretical
and Applied Genetics 100, 658664.
Green, R.E., Cornell, S.J., Scharlemann, J.P.W., Balmford, A., 2005. Farming and
the fate of wild nature. Science 307, 550555.
Hajirezaei, M., Sonnewald, U., Viola, R., et al., 1994. Transgenic potato plants with
strongly decreased expression of pyrophosphate:fructose-6-phosphate
phosphotransferase show no visible phenotype and only minor changes in
metabolic uxes in their tubers. Planta 192, 1630.
Hall, R.D., Brouwer, I.D., Fitzgerald, M.A., 2008. Plant metabolomics and its potential
application for human nutrition. Physiologia Plantarum 132 (2), 162175.
Han, G., 2009. Origin agritech announces nal approval of worlds rst genetically
modied phytase corn. Business Wire, 21 November 2009. Available at: http://
www.allbusiness.com/science-technology/biology-biotechnology-genetic/
13453842-1.html (accessed 19.02.10).
Harjes, C.E., Rocheford, T.R., Bai, L., et al., 2008. Natural genetic variation in
lycopene epsilon cyclase tapped for maize biofortication. Science 319,
330333.
Hartwig, E.E., Kuo, T.M., Kenty, M.M., 1997. Seed protein and its relationship to
soluble sugars in soybeans. Crop Science 37, 770773.
Hellwege, E.M., Czapla, S., Jahnke, A., Willmitzer, L., Heyer, A.G., 2000. Transgenic
potato (Solanum tuberosum) tubers synthesize the full spectrum of inulin
molecules naturally occurring in globe artichoke (Cynara scolymus) roots.
Proceedings of the National Academy of Sciences of the United States of
America 97, 86998704.
Hellwege, E.M., Gritscher, D., Willmitzer, L., Heyer, A.G., 1997. Transgenic potato
tubers accumulate high levels of 1-kestose and nystose: Functional identication
of a sucrose 1-fructosyltransferase of artichoke (Cynara scolymus) blossom
discs. Plant Journal 12, 10571065.
Helm, R.M., Cockrell, G., Connaughton, C., et al., 2000. Mutational analysis of the
IgE-binding epitopes of P34/Gly m Bd 30 K. Journal of Allergy and Clinical
Immunology 105, 378384.
Herman, E.M., Helm, R.M., Jung, R., Kinney, A.J., 2003. Genetic modication
removes an immunodominant allergen from soybean. Plant Physiology 132,
3643.
Hipskind, J.D., Paiva, N.L., 2000. Constitutive accumulation of a resveratrolglucoside in transgenic alfalfa increases resistance to Phoma medicaginis.
Molecular PlantMicrobe Interactions 13, 551562.
Hutchison, W.D., Burkness, E.C., Mitchell, P.D., et al., 2010. Areawide suppression
of European corn borer with Bt maize reaps savings to non-Bt maize growers.
Science 330, 222225.
91
ILSI (International Life Sciences Institute), 2004a. Nutritional and safety assessments
of foods and feeds nutritionally improved through biotechnology. Comprehensive
Reviews in Food Science and Food Safety 3, 35104. Available at: http://
members.ift.org/NR/rdonlyres/27BE106D-B616-4348-AE3A-091D0E536F40/0/
crfsfsv3n2p00350104ms20040106.pdf (accessed 03.05.14).
ILSI (International Life Sciences Institute), 2004b. Nutritional and safety assessments
of foods and feeds nutritionally improved through biotechnology: An executive
summary. Journal of Food Science 69, CRH62CRH68.
ILSI (International Life Sciences Institute), 2008. Nutritional and safety assessments
of foods and feeds nutritionally improved through biotechnology: Case studies.
Comprehensive Reviews in Food Science and Food Safety 7, 5099.
Jalani, B.S., Cheah, S.C., Rajanaidu, N., Darus, A., 1997. Improvement of palm oil
through breeding and biotechnology. Journal of the American Oil Chemists
Society 74, 14511455.
James, C., 2011. Global Status of Commercialized Biotech/GM Crops: 2010. ISAAA
Briefs 42-2010. Ithaca, NY: ISAAA. Available at: http://www.isaaa.org/resources/
publications/briefs/42/executivesummary/default.asp (accessed 03.05.14).
James, C., 2013. Global Status of Commercialized Biotech/GM Crops: 2012. ISAAA
Brief No. 44. Ithaca, NY: International Service for the Acquisition of Agri-biotech
Applications. Available at: http://www.isaaa.org/ (accessed 24.02.13).
James, M.J., Ursin, V.M., Cleland, L.G., 2003. Metabolism of stearidonic acid in
human subjects: Comparison with the metabolism of other n-3 fatty acids.
American Journal of Clinical Nutrition 77, 11401145.
Juma, C., 2012. Biotechnology and Africas Strategic Interests. The Chicago Council
on Global Affairs. Available at: http://globalfoodforthought.typepad.com/globalfood-for-thought/ (accessed 03.05.14).
Jung, K.H., Seo, Y.S., Walia, H., et al., 2010. The submergence tolerance regulator
Sub1A mediates stress-responsive expression of AP2/ERF transcription factors.
Plant Physiology 152, 16741692.
Katsube, T., Kurisaka, N., Ogawa, M., et al., 1999. Accumulation of soybean
glycinin and its assembly with the glutelins in rice. Plant Physiology 120,
10631074.
Keshavarz, K., 2003. The effect of different levels of nonphytate phosphorus with and
without phytase on the performance of four strains of laying hens. Poultry
Science 82, 7191.
Kinney, A.J., Knowlton, S., 1998. Designer oils: The high oleic acid soybean. In:
Roller, S., Harlander, S. (Eds.), Genetic Modication in the Food Industry.
London, UK: Blackie Academic and Professional, pp. 193213.
Kobayashi, S., Ding, C.K., Nakamura, Y., Nakajima, I., Matsumoto, R., 2000.
Kiwifruits (Actinidia deliciosa) transformed with a Vitis stilbene synthase gene
produce piceid (resveratrol-glucoside). Plant Cell Reports 19, 904910.
Kraemer, K., 2012. Tackling Malnutrition and Micronutrient Deciencies. The
Chicago Council on Global Affairs. Available at: http://globalfoodforthought.
typepad.com/global-food-for-thought/ (accessed 03.05.14).
Kramer, P.J., 1980. Drought, stress, and the origin of adaptations. In: Turner, N.C.,
Kramer, P.J. (Eds.), Adaptations of Plants to Water and High Temperature Stress.
New York, NY: John-Wiley & Sons, pp. 720.
Lai, J.S., Messing, J., 2002. Increasing maize seed methionine by mRNA stability.
Plant Journal 30, 395402.
Li, L., Liu, S.M., Hu, Y.L., Zhao, W.P., Lin, Z.P., 2001. Increase of sulphurcontaining amino acids in transgenic potato with 10 ku zein gene from maize.
Chinese Science Bulletin 46, 482484.
Liu, Q., Singh, S., Green, A., 2002. High-oleic and high-stearic cottonseed oils:
Nutritionally improved cooking oils developed using gene silencing. Journal of
the American College of Nutrition 21, 205S211S.
Long, M., Millar, D.J., Kimura, Y., et al., 2006. Metabolite proling of carotenoid
and phenolic pathways in mutant and transgenic lines of tomato: Identication of
a high antioxidant fruit line. Phytochemistry 67, 17501757.
Lopez-Bucio, J., Nieto-Jacobo, M.F., Ramirez-Rodriguez, V.V., Herrera-Estrella, L.,
2000. Organic acid metabolism in plants: From adaptive physiology to transgenic
varieties for cultivation in extreme soils. Plant Science 160, 113.
Lucca, P., Hurrell, R., Potrykus, I., 2002. Fighting iron deciency anemia with ironrich rice. Journal of the American College of Nutrition 21, 184S190S.
Luciani, G., Altpeter, F., Wofford, D.S., 2005. Over-expression of a soybean
vegetative storage protein gene in bahiagrass (Paspalum notatum var. Flugge).
Poster presented at Florida Genetics; November 30December 1, 2005,
Gainesville, FL, USA. Available at: http://www.ufgi.u.edu/Symposium/
FG2005program_rev.pdf (accessed 14.06.06).
Lukaszewicz, M., Matysiak-Kata, I., Skala, J., et al., 2004. Antioxidant capacity
manipulation in transgenic potato tuber by changes in phenolic compounds
content. Journal of Agricultural and Food Chemistry 52, 15261533.
Mathers, J.C., 2006. Plant foods for human health: Research challenges.
Proceedings of the Nutrition Society 65, 198203.
92
Diseases of Fruit Crops, 510 July. Neustadt, Germany: Julius Khn- Institut,
Agroscience Ltd. and German Phytomedical Society (DPG).
Svenier, R., Hall, R.D., van der Meer, I.M., et al., 1998. High level fructan
accumulation in a transgenic sugar beet. Nature Biotechnology 16, 843846.
Shewmaker, C.K., Sheehy, J.A., Daley, M., Colburn, S., Ke, D.Y., 1999. Seedspecic overexpression of phytoene synthase: Increase in carotenoids and other
metabolic effects. Plant Journal 20, 401412.
Shin, D.W., Baigorria, G.A., Lim, Y.-K., et al., 2009. Assessing crop yield
simulations with various seasonal climate data. Science and Technology Infusion
Climate Bulletin. Norman, OK: NOAAs National Weather Service.
Shin, Y., Park, H., Yim, S., et al., 2006. Transgenic rice lines expressing maize C1
and R-S regulatory genes produce various avonoids in the endosperm. Plant
Biotechnology Journal 4, 303315.
Shintani, D., DellaPenna, D., 1998. Elevating the vitamin E content of plants through
metabolic engineering. Science 282, 20982100.
da Silva, J.G., 2012. Remarks by FAOs Director-General. Rome: UN ofcials stress
link between food security and peace in Sahel UN News Centre. Available at:
http://www.un.org/apps/news/story.aspNewsID=43713&Cr=sahel&Cr1=#.
UMl1mXfsLF0 (accessed 03.05.14).
Siritunga, D., Sayre, R.T., 2003. Generation of cyanogen-free transgenic cassava.
Planta 217, 367373.
Smeekens, S., 1997. Engineering plant metabolism. Trends in Plant Science 2,
286287.
Smuts, C.M., Huang, M., Mundy, D., et al., 2003. A randomized trial of
docosahexaenoic acid supplementation during the third trimester of pregnancy.
Obstetrics & Gynecology 101, 469479.
Sottosanto, J.B., Saranga, Y., Blumwald, E., 2007. Impact of AtNHX1, a vacuolar
Na /H antiporter, upon gene expression during short and long term salt
stress in Arabidopsis thaliana. BMC Plant Biology 7, 18.
Sprenger, N., Schellenbaum, L., van Dun, K., Boller, T., Wiemken, A., 1997. Fructan
synthesis in transgenic tobacco and chicory plants expressing barley sucrose:
Fructan 6-fructosyltransferase. FEBS Letters 400, 355358.
Stark-Lorenzen, P., Nelke, B., Hanssler, G., Muhlbach, H.P., Thomzik, J.E., 1997.
Transfer of a grapevine stilbene synthase gene to rice (Oryza sativa L.). Plant
Cell Reports 16, 668673.
Stearidonic Acid (SDA), 2011. Monsanto Omega-3 Soybeans. Available at: http://
www.monsanto.com/products/Pages/sda-omega-3-soybeans.aspx (accessed
03.05.14).
Stern, N., 2006. Review on the economics of climate change. London, UK: HM
Treasury.
Storozhenko, S., De Brouwer, V., Volckaert, M., et al., 2007. Folate fortication of
rice by metabolic engineering. Nature Biotechnology 25, 12771279.
Summers, 2014. GM halo effect: Can GM crops protect conventional and organic
farming? Genetic Literacy Project.
Sun, L., Yuan, B., Zhang, M., et al., 2012. Fruit-specic RNAi-mediated suppression
of SlNCED1 increases both lycopene and beta-carotene contents in tomato fruit.
Journal of Experimental Botany 63 (8), 30973108.
Svoboda, E., 2008. The Future of Farming is in Nitrogen Efciency Fastcompany.
Available at: http://www.fastcompany.com/magazine/129/seed-money.html
(accessed 15.01.14).
Tang, G., Qin, J., Dolnikowski, G.G., Russell, R.M., Grusak, M.A., 2009. Golden
Rice is an effective source of vitamin A. American Journal of Clinical Nutrition
89, 17761783.
Times of India, 2012. No moratorium on GM crop trials till stakeholders heard: SC.
Available at: http://timesondia.indiatimes.com/india/No-moratorium-on-GM-croptrials-till-stakeholders-heard-SC/articleshow/17011950.cms (accessed 15.01.14).
Trewavas, A., 2008. The cult of the amateur in agriculture threatens food security.
Trends in Biotechnology 26 (9), 475478. oGo to ISI4://000259324200002
AND. Available at: http://www.ask-force.org/web/Discourse/Trewavas-CultAmateur-Agriculture-2008.pdf (accessed 15.01.14).
Turnbaugh, P.J., Hamady, M., Yatsunenko, T., et al., 2009. A core gut microbiome
in obese and lean twins. Nature 457, 480484.
Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., Dubcovsky, J., 2006. A NAC gene
regulating senescence improves grain protein, zinc, and iron content in wheat.
Science 314, 12981301.
UN SCN, 2004. Nutrition for improved development outcomes. 5th Report on the
World Nutrition Situation. Geneva, Switzerland: United Nations System Standing
Committee on Nutrition.
UPI, 2002. Wheat Inhibits Colon Cancer. Washington, DC: United Press International
Vistive Gold Soybeans. Available at: http://www.monsanto.com/products/Pages/
vistive-gold-soybeans.aspx (accessed 15.01.14).
Ursin, V., 2000. Genetic modication of oils for improved health benets.
Presentation at conference Dietary Fatty Acids and Cardiovascular
93
Relevant Website
http://www.pgeconomics.co.uk/pdf/2012globalimpactstudynal.pdf
PG Economics Limited.
Glossary
Auxinic herbicide A herbicide such as 2,4dichlorophenoxyacetic acid that acts as a synthetic form of
the plant hormone indoleacetic acid (auxin).
Deregulation The approval of a transgenic crop by
regulatory agencies for its commercialization.
Dicotyledonous A owering plant with two cotyledons in
the seed.
Gene stacking The process of inserting more than one
functional transgene into an organism by genetic
engineering.
Introduction
In the developed world, weeds have been managed primarily
with herbicides since the middle of the past century. The rst
highly successful herbicide 2,4-dichlorophenoxyacetic acid
(2,4-D) killed most dicotyledonous weeds, but at the same
time it did not injure monocotyledonous crops or turf. Subsequently, companies involved in herbicide discovery screened
for selective compounds that kill important weeds without
signicantly injuring crops. Such products usually killed only a
fraction of the important weeds in a crop, so that another
selective herbicide with a different weed species spectrum also
had to be used in the crop if the farmer was to rely on
herbicides for weed management. Minor crop injury commonly occurred with selective herbicides, but farmers were
willing to accept this risk in return for good weed management, as weeds can devastate a crop if not controlled. Nonselective herbicides that kill all plants, like paraquat or
glyphosate, were usually used with crops only before planting
or after harvesting.
Except for auxinic herbicides such as 2,4-D and grass-killing
herbicides inhibiting acetyl-CoA carboxylase (ACCase), the
mechanism of crop selectivity did not involve resistance at the
molecular target site of the herbicide. Most selective herbicides
did little harm to the crop because the crop metabolically
degraded the active ingredient much more rapidly than the
weed. For example, triazine herbicides are quickly degraded by
maize (Esser et al., 1975), the crop of their primary use, even
though these herbicides are active at the D-1 site of photosystem II (PSII) of all plants. For most selective herbicides,
phytotoxicity to a crop is variable, depending on factors that
might inuence metabolic degradation of the herbicide, such
as climatic conditions. A concern of herbicide manufacturers
was that the selective herbicide might cause unacceptable
problems in cultivars for which it had not been tested. Use of
compounds that induce increased metabolism of the herbicide
by the crop (herbicide safeners) to provide protection has been
one approach to protect the crop from unacceptable herbicide
damage (Rosinger et al., 2012). This approach further
94
doi:10.1016/B978-0-444-52512-3.00218-7
95
96
Glufosinate-Resistant Crops
Table 1
Transgenic herbicide-resistant crops that have been or are
now available for planting in the US
Herbicide
Crop
Year of introduction
Bromoxynila
Cotton
Canola
Canola
Maize
Cotton
Soybean
Soybean
Canola
Cotton
Maize
Sugar beet
Alfalfab
1995
2000
1995
1997
2004
2011
1996
1996
1997
1998
2008
2005
Glufosinate
Glyphosate
All bromoxynil resistant crops have been withdrawn from the market.
Removed from market by court order in 2007 but returned to the market by a US
Supreme Court ruling and after further USDA/Animal and Plant Health Inspection
Service examination in 2011.
b
97
glufosinate and GR canola (both transgenic) and imidazolinone-resistant canola (nontransgenic) are grown from commercial seeds that have only one of these resistances. Yet, all
combinations of these resistances have been found in individual volunteer canola plants, both outside and within canola
elds (Knispel et al., 2008; Schafer et al., 2012b). Gene ow
can also occur between glufosinate-resistant canola and weedy
relatives (Song et al., 2010). Fully introgressed bar genes into
weeds have not been documented. This scenario requires that
the F1 and subsequent backcrosses be t in the absence of
glufosinate or that each cross be subjected to glufosinate. F1
hybrids of some canola/weedy relative combinations are not
very t (e.g., Schefer and Dale, 1994), yet there are reports of
introgression of the cp4 glyphosate-resistance gene from
commercial canola into a weed relative Brassica rapa (Warwick
et al., 2008). The gene was persistent in the population more
than a 6-year period, despite the tness cost of hybridization
and absence of glyphosate use (with the exception of one
possible exposure). Nevertheless, gene ow from HR canola to
weedy relatives has not created a major weed problem.
There are potential benets of glufosinate-resistant crops in
addition to weed management. Glufosinate is fungitoxic (Liu
et al., 1998) and bactericidal (Pline et al., 2001) and provides
some level of protection from plant diseases in glufosinateresistant crops. For example, glufosinate reduced the severity
of rice blast and brown leaf spot in glufosinate-resistant rice
(Ahn, 2008). The herbicide also provides some degree of
protection to glufosinate-resistant soybean from Pseudomonas
syringae pv. glycinea at eld rates (Pline et al., 2001). Glufosinate also reduces fungal diseases in glufosinate-resistant
bentgrass (Agrostis spp.) (Liu et al., 1998; Wang et al., 2003).
There may be similar benets of glyphosate in GR crops with
some plant pathogens.
As mentioned earlier, the bar gene is used extensively as a
selectable marker in transgenic plant production. Therefore,
any crop could be made glufosinate resistant (e.g., peppermint
Li et al., 2001 and wheat y et al., 2012). However, the
current costs in gaining approval for commercialization of
transgenic crops, as well as variety development costs, preclude
the introduction of many more glufosinate-resistant crop
species. At least in the foreseeable future, new glufosinateresistant crops will more likely be existing glufosinate-resistant
crops (canola, cotton, maize, and soybean) with genes for
resistance to other herbicides stacked with them.
Glyphosate-Resistant Crops
Glyphosate: The herbicide
Glyphosate (N-(phosphonomethyl)glycine) is the most successful herbicide in history in terms of market share and customer satisfaction (Duke and Powles, 2008). Before GR crops
were available, glyphosate was a successful herbicide, but its
use grew substantially due to its use in glyphosate-resistant
(GR) crops. Because glyphosate is a very good nonselective
herbicide, it could only be used with agronomic crops before
planting, after crop maturity or harvest, or with devices that
did not allow the herbicide to reach the foliage of the crop
(e.g., shielded sprayers and rope-wick applicators). It was also
heavily used in perennial horticultural crops (e.g., grapes and
98
tree crops) when foliage had not appeared in the crop or with
ground spraying below the crop foliage. It was also used in
many noncrop situations. It is considered a very safe herbicide,
as its acute toxicity is lower than that of aspirin or NaCl. The
vast majority of toxicological studies have found glyphosate to
be very safe to mammals from both an acute and a chronic
standpoint (Mink et al., 2012; Williams et al., 2000, 2012).
Glyphosate is the only herbicide that kills plants by inhibition of the enzyme 5-enolpyruvylshikimate-3-phosphate
synthase (EPSPS). The fact that there is no secondary mode of
action at doses of glyphosate used in the eld is clear from the
nding that plants with a transgene that encodes a resistant
form of EPSPS are approximately 50-fold more resistant to
glyphosate than untransformed plants (Nandula et al., 2007).
EPSPS is a critical enzyme of the shikimate pathway, from
which the three aromatic amino acids (phenylalanine, tyrosine, and tryptophan) are derived. The sequence of events
causing death of the plant after inhibition of EPSPS is not
entirely clear. The most rapid effect is the accumulation
of shikimate acid and benzoates in affected plant tissues
(Amrhein et al., 1980; Lydon and Duke, 1988). Inhibition of
carbon xation can also be very rapid in some species (e.g.,
Servaites et al., 1987), apparently due to the loss of carbon
intermediates, which, in turn, is caused by the loss of regulation of carbon ow into the shikimate pathway (Siehl,
1997). Certainly, levels of aromatic amino acid are reduced, so
is the synthesis of auxin from tryptophan and many secondary
products that are derived from aromatic amino acids. Thus,
many physiological functions are compromised by this
herbicide. Glyphosate is perhaps the most slow-acting herbicide that is sold. Its slow action allows it to translocate
throughout the plant, like sucrose, to metabolic sinks (Gougler
and Geiger, 1981), such as meristems, where it concentrates.
Thus, all growing points of the plant are killed, eliminating
regrowth. This makes it very effective on perennial weeds with
subterranean rhizomes or stolons that make these species less
vulnerable to other herbicides.
99
100
Soybean
Cotton
80
Maize
60
40
20
0
1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Year
Figure 1 Adoption of GR crops in the US by year. Data from http://www.ers.usda.gov/data-products/adoption-of-genetically-engineered-crops-inthe-us.aspx
2.5
80
2
60
1.5
40
1
0.5
20
0
2.5
0
100
(a)
(b)
80
1.5
60
40
0.5
20
0
100
1.4
Pounds of active ingredients
per planted acre
1.2
80
1
60
0.8
0.6
40
0.4
20
0.2
(c) 0
1996
100
100
0
1998
2000
2004
2002
2006
2008
Year
Figure 2 Quantity of glyphosate (dark symbols) and all other herbicides (gray symbols) used on the US crop areas (A, maize; B, cotton; and C,
soybean). Open symbols are percent adoption of GR crop. Reproduced with permission of the National Academies Press from Ervin, D.E., Carrire,
Y., Cox, W.J., et al., 2010. The Impact of Genetically Engineered Crops on Farm Sustainability in the United States. Washington, DC: National
Research Council, The National Academies Press, 250 pp.
101
160
140
120
100
80
900
825
750
675
600
525
45
40
35
30
25
1980
1985
1990
1995
2000
2005
2010
Year
Figure 3 The US yields of the three crops over the past 30 years that are now grown mostly as GR cultivars. The shaded represents the years
since the introduction of each GR crop. Reproduced with permission from Duke, S.O., Lydon, J., Koskinen, W.C., et al., 2012b. Glyphosate effects
on plant mineral nutrition, crop rhizosphere microbiota, and plant disease in glyphosate-resistant crops. Journal of Agricultural and Food Chemistry
60, 1037510397. Copyright 2012 American Chemical Society.
102
% GM
100
90
80
70
Percent of GM surface
EIQ
EIQ
35
EIQ
30
60
25
50
40
30
20
20
10
15
0
1990 1992 1994 1996 1998 2000 2002 2004 2006
Table 2
103
Crop
Disease organism
Effect
Reference
Soybean
Phakopsora pachyrhizi
Decreased
Decreased
Decreased
Decreased
Decreased
Increased
Increased
No effect
No effect
No effect
No effect
No effect
No effect
Decreased
Decreased
Decreased
Decreased
No effect
No effect
No effect
No effect
Decreased
Decreased
Decreased
No effect
No effect
No effect
Mixed resultsa
No effect
Myrothecium roridum
Erysiphe diffusa
Fusarium spp.
Fusarium virguliforme
Schlerotinia sclerotiorum
Cotton
Wheat
Alfalfa
Sugar beet
Rhizoctonia solani
Rhizoctonia solani
Puccinia triticina
Puccinia striiformis
Rhizoctonia solani
Rhizopus oryzae
Pythium ultimum
Gaeumannomyces graminis
Uromyces striatus
Phoma medicaginis
Colletotrichum trifolii
Rhizoctonia solani
Fusarium oxysporum
a
Proof of a direct effect of glyphosate on ASR was obtained by measuring shikimate levels in ASR-infected soybeans
with and without glyphosate treatment (Dill et al., 2010). No
shikimate accumulated in noninfected plants treated with
glyphosate or in non-ASR-inoculated plants without glyphosate, but high levels did accumulate in inoculated plants
treated with glyphosate. These results are most clearly interpreted as the shikimate being derived from inhibition of
fungal EPSPS.
Johal and Huber (2009) and Kremer and Means (2009)
had suggested that glyphosate treatment of GR soybeans
increases fungal root diseases (e.g., Fusarium spp.).
However, several studies reported no effects of glyphosate
on Fusarium virguliforme (formerly known as F. solani) in GR
soybeans (Table 2). Powell and Swanton (2008) concluded
that there was insufcient evidence to conclude that
glyphosate promotes infection of GR soybeans by Fusarium
spp.
An extensive analysis of the published data concluded that
the baseline disease resistance or susceptibility of the host
plant variety is the major contributor to disease susceptibility
in GR crops regardless of the presence of the glyphosate resistance gene or treatment with glyphosate (Duke et al.,
2012b). In fact, the reports listed in Table 2 would suggest that
glyphosate treatment can reduce the effects of many plant
pathogens on GR crops, whereas having no effect on most
others.
104
Glyphosate-resistant species
25
20
15
10
5
0
1996 1998 2000 2002 2004 2006 2008 2010 2012
Year
Figure 5 Cumulative number of weed species that have evolved
resistance to glyphosate worldwide. Data from Heap, I., 2013.
International Survey of Herbicide Resistant Weeds. Available at: www.
weedscience.org (accessed 30.05.13).
Table 3
105
Weed species
Location (countries)
Year
Amaranthus palmeri
Amaranthus spinosus
Amarnathus tuberculatus (syn rudis)
Ambrosia artemisiifolia
Ambrosia trida
Bromus diandrus
Chloris truncata
Conyza bonariensis
Conyza canadensis
Conyza sumatrensis
Cynodon hirsutus
Digitaria insularis
Echinochloa colona
Eleusine indica
Kochia scoparia
Leptochloa virgata
Lolium multiorum
Lolium perenne
Lolium rigidum
Parthenium hysterophorus
Plantago lanceolata
Poa annua
Sorghum halepense
Urochloa panicoides
USA
USA
USA
USA and Canada
USA and Canada
Australia
Australia
South Africa, Spain, Brazil, Israel, Columbia, USA, Australia, Greece, and Portugal
USA, Brazil, China, Spain, Czech Republic, Poland, Canada, Italy, and Greece
Spain, Brazil, and Greece
Argentina
Paraguay and Brazil
Australia, USA, and Agentina
Malaysia, Colombia, China, USA, and Argentina
USA and Canada
Mexico
Chile, Brazil, USA, Spain, and Argentina
Argentina
Australia, USA, South Africa, France, Spain, Israel, and Italy
Columbia
South Africa
USA
Argentina and USA
Australia
2005
2012
2005
2004
2004
2011
2010
2003
2000
2009
2009
2008
2007
1997
2007
2010
2001
2008
1996
2004
2003
2010
2005
2008
Source: Data from Heap, I., 2103. International Survey of Herbicide Resistant Weeds. Available at: www.weedsci.org (accessed 30.05.13).
106
100
Total HR
90
80
70
60
Glyphosate-HR
50
40
30
Glufosinate-HR
20
Imidazolinone-HR
10
0
1995
1998
2001
2004
2007
2010
Year
Figure 6 Adoption of herbicide-resistant oilseed rape (Brassica napus L.) in Canada: Mainly grown in Alberta, Saskatchewan, and Manitoba.
Reproduced from Beckie, H.J., 2011. Herbicide-resistant weed management: Focus on glyphosate. Pest Management Science 67, 10371048, with
permission from Wiley Press, Chichester, UK.
107
Dicamba-resistant crops
Dicamba (3,6-dichloro-2-methoxybenzoic acid) is an older
auxinic herbicide, killing mainly broadleaf weed species in
monocot grain crops. It is too phytotoxic for its use as a
postemergence herbicide in maize, in which it can only be
used as a preplant herbicide with a delayed planting to avoid
injury to the crop. It controls more weed species than most
other auxinic herbicides, such as 2,4-D, and even controls
more species than glufosinate (Feng et al., 2010). Dicambaresistant crops have been generated by inserting a transgene
from a soil microbe (Stenotrophomonas maltophilia) that encodes dicamba monooxygenase (DMO) (Behrens et al., 2007).
This enzyme demethylates dicamba to form nonphytotoxic
3,6-dichlorosalicylic acid. The gene provides a high level of
resistance to dicamba in both dicots (cotton and soybean) and
monocots including maize (Cao et al., 2011). Dicamba resistance will be stacked with glyphosate and/or glufosinate
resistance in cotton and soybeans in the rst introductions.
Dicamba provides excellent control of some of the weed
species that have evolved resistance to glyphosate, for example,
108
Table 4
Herbicide-resistant crops for which petitions for
deregulated status (approval for commercialization) have been led but
not yet granted (APHIS, 2013)
Year of
application
Maize
2009
2011
2011
Soybean
2009
Herbicides
2009
2009
2010
2011
2012
Cotton
2012
Canola
2011
Glyphosate
introduced in the mid-1940s and sold as amine or ester formulations. These formulations of 2,4-D are still used in large
amounts for weed management. 2,4-D choline, a quaternary
ammonium salt with much lower volatility than previous 2,4D products, is planned to be the only formulation allowed
with 2,4-D-resistant crops. Thus, introduction of this lowvolatility formulation of 2,4-D could even decrease the 2,4-D
drift problem with non-GRC uses.
As pointed out by Egan et al. (2011), there are almost 20
weed species that have evolved resistance to 2,4-D. In fact, the
rst two reported cases of evolved herbicide resistance were of
2,4-D in 1957 (Heap, 2013). Beckie and Tardif (2012) considered 2,4-D and other auxinic herbicides to have a lower risk
for evolution of resistance than some other herbicide classes.
In at least some cases, a single, dominant gene confers resistance to more than one auxinic herbicide (Jugulam et al.,
2005). Considering that auxinic herbicides appear to have
multiple binding sites (Walsh and Schmitzer, 2012), singlegene-based resistance may be due to an enzyme that degrades
the herbicide (Harrington and Wooley, 2006), but other
mechanisms of resistance have apparently evolved (Kelley and
Riechers, 2007). Weeds have had more than 60 years to evolve
resistance to this still heavily used herbicide. Clearly, 2,4-D
resistance neither does not evolve as readily as resistance to
ACCase or ALS inhibitor herbicides does nor perhaps as slowly
as to glyphosate.
ACCase-, and ALS-inhibitor herbicides will probably be commercialized, so these are dealt with separately in this section;
others are discussed in the last section.
109
Some transgenes that have been used to generate herbicide-resistant plants that are unlikely to be commercialized in the near future
Gene/enzymea
Herbicide(s)
Gene sourceb
Reference
Phenylureas
Multiple
Dalapon
Asulam
Pyrimidines
Alachlor, EPTC, and Dimethenamid
Phenmedipham
Fluridone and norurazon
Aciuorfen
Paraquat
Dinitroanilines
Dehalogenase (D)
Dihydropteroate synthase (T)
Esterase (D)
Glutathione S-transferase
Hydrolase (D)
Phytoene desaturase (T)
Protoporphyrinogen oxidase (T)
Superoxide dismutase (D)
-Tubulin (T)
a
110
References
Ahn, I.-P., 2008. Glufosinate ammonium-induced pathogen inhibition and defense
responses culminate in disease protection in bar-transgenic rice. Plant
Physiology 146, 213217.
Amrhein, N., Deus, B., Gehrke, P., Steinrcken, H.C., 1980. The site of the
inhibition of the shikimate pathway by glyphosate. Plant Physiology 66,
830834.
Anderson, J.A., Kolmer, J.A., 2005. Rust control in glyphosate tolerant
wheat following application of the herbicide glyphosate. Plant Disease 89,
11361142.
Bradshaw, L.D., Padgette, S.R., Kimball, S.L., Wells, B.H., 1997. Perspectives on
glyphosate resistance. Weed Technology 11, 189198.
Brookes, G., Barfoot, P., 2006. Global impact of biotech crops: Socio-economic and
environmental effects of the rst ten years of commercial use. AgBioForum 9,
139151.
Brookes, G., Barfoot, P., 2012. The income and production effects of biotech crops
globally 19962010. GM Crops and Food 3, 265272.
Brookes, G., Barfoot, P., 2013. The global income and production effects of
genetically modied (GM) crops 19962011. GM Crops and Food 4,
110.
Buchanan-Wollaston, V., Snape, A., Cannon, F., 1992. A plant selective marker gene
based on the detoxication of the herbicide dalapon. Plant Cell Reports 11,
627631.
Burke, I.C., Yenish, J.P., Pittman, D., Gallagher, R.S., 2009. Resistance of a prickly
lettuce (Lactuca serriola) biotype to 2,4-D. Weed Technology 23, 586591.
Cao, M., Sato, S.J., Behrens, M., et al., 2011. Genetic engineering of maize (Zea
mays) for high-level tolerance to treatment with the herbicide dicamba. Journal of
Agricultural and Food Chemistry 59, 58305834.
Carpenter, J.E., Gianessi, L.P., 2010. Economic impact of glyphosate-resistant
weeds. In: Nandula, V.K. (Ed.), Glyphosate Resistance in Crops and Weeds.
Hoboken, NJ: John Wiley & Sons, Inc., pp. 297312.
de Carvalho, L.B., Cruz-Hipolito, H., Gonzalez-Torralva, F., et al., 2011. Detection of
sourgrass (Digitaria insularis) biotypes resistant to glyphosate in Brazil. Weed
Science 59, 171176.
Castle, L.A., Siehl, D.L., Groton, R., et al., 2004. Discovery and directed evolution of
a glyphosate tolerance gene. Science 304, 11511154.
Cerdeira, A.L., Duke, S.O., 2006. The current status and environmental impacts of
glyphosate-resistant crops: A review. Journal of Environmental Quality 35,
16331658.
Cerdeira, A.L., Gazziero, D.L.P., Duke, S.O., Matallo, M.B., 2011. Agricultural
impacts of glyphosate-resistant soybean cultivation in South America. Journal of
Agricultural and Food Chemistry 59, 57995807.
Chandi, A., Jordan, D.l., York, A.C., et al., 2013. Response of herbicide-resistant
palmer amaranth (Amaranthus palmeri) accessions to drought stress. International
Journal of Agronomy. Available at: http://dxdoi.org/10.1155/2013/823913
(accessed 15.05.13).
Clewis, S.B., Wilcut, J.W., 2007. Economic assessment of weed management in
strip- and conventional-tillage nontransgenic and transgenic cotton. Weed
Technology 21, 4552.
Copping, L.G., Duke, S.O., 2007. Natural products that have been used
commercially as crop protection agents A review. Pest Management Science
63, 524554.
Culpepper, A.S., Grey, T.L., Vencill, W.K., et al., 2006. Glyphosate-resistant palmer
amaranth (Amaranthus palmeri) conrmed in Georgia. Weed Science 54,
620626.
Darmency, H., 2013. Pleiotropic effects of herbicide-resistance genes on crop yield:
A review. Pest Management Science. doi:10.1002/ps.3522.
De Groote, H., Wangare, L., Kanampiu, F., 2007. Evaluating the use of herbicidecoated imidazolinone-resistant (IR) maize seeds to control Striga in farmers'
elds in Kenya. Crop Protection 26, 14961506.
Derpsch, R., Freidrich, T., Kassam, A., Li, H., 2010. Current status of adoption of
no-till farming in the world and some of its main benets. International Journal
of Agricultural and Biological Engineering 3, 125.
Devine, M.D., 2005. Why are there not more herbicide-resistant crops? Pest
Management Science 61, 312317.
Devos, Y., Cougnon, M., Vergucht, S., et al., 2008. Environmental impact of
herbicide regimes used with genetically modied herbicide-resistant maize.
Transgenic Research 17, 10591077.
Dick, R.E., Quinn, J.P., 1995. Glyphosate-degrading isolated from environmental
samples: Occurrence and pathways of degradation. Applied Microbiology and
Biotechnology 43, 545550.
Didierjean, L., Gondet, L., Perkins, R., et al., 2002. Engineering herbicide
metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450
enzyme from Jerusalem artichoke. Plant Physiology 130, 179189.
Dill, G.M., 2005. Glyphosate-resistant crops: History, status and future. Pest
Management Science 61, 219224.
Dill, G.M., CaJacob, C.A., Padgette, S.R., 2008. Glyphosate-resistant crops:
Adoption, use and future considerations. Pest Management Science 64,
326331.
Dill, G.M., Sammons, R.D., Feng, P.C.C., et al., 2010. Glyphosate discovery,
development, applications, and properties. In: Nandula, V.K. (Ed.), Glyphosate
Resistance in Crops and Weeds. Hoboken, NJ: John Wiley & Sons, Inc.,
pp. 133.
111
Dinelli, G., Marotti, I., Bonetti, A., et al., 2008. Physiological and molecular bases of
glyphosate resistance in Conyza bonariensis biotypes from Spain. Weed Research
48, 257265.
Dos Reis Goulart, I.C.G., Pacheco, M.T., Nunes, A.L., Merotto, A., 2012.
Identication of origin and analysis of population structure of eld-selected
imidazolinone-herbicide resistant red rice (Oryza sativa). Euphytica 187, 437447.
Duke, S.O. (Ed.), 1996. Herbicide-Resistant Crops: Agricultural, Environmental, Economic, Regulatory, and Technical Aspects. Boca Raton, FL: CRC
Press.
Duke, S.O., 2011a. Glyphosate degradation in glyphosate-resistant and -susceptible
crops and weeds. Journal of Agricultural and Food Chemistry 59,
58355841.
Duke, S.O., 2011b. Comparing conventional and biotechnology-based pest
management. Journal of Agricultural and Food Chemistry 59, 57935798.
Duke, S.O., 2012. Why have no new herbicide modes of action appeared in recent
years? Pest Management Science 68, 505512.
Duke, S.O., Cerdeira, A.L., 2005. Potential environmental impacts of herbicideresistant crops Collection of Biosafety Review, vol. 2. Trieste, Italy: International
Centre for Genetic Engineering and Biotechnology pp. 66143.
Duke, S.O., Cerdeira, A.L., 2010. Transgenic crops for herbicide resistance. In: Kole,
C., Michler, C.H., Abbott, A.G., Hall, T.C. (Eds.), Transgenic Crop Plants, vol. 2,
Utilization and Biosafety. Berlin: Springer Verlag, pp. 133166.
Duke, S.O., Lydon, J., Koskinen, W.C., et al., 2012b. Glyphosate effects on
plant mineral nutrition, crop rhizophere microbiota, and plant disease in
glyphosate-resistant crops. Journal of Agricultural and Food Chemistry 60,
1037510397.
Duke, S.O., Powles, S.B., 2008. Glyphosate: A once-in-a-century herbicide. Pest
Management Science 64, 319325.
Duke, S.O., Reddy, K.N., Bu, K., Cizdziel, J.V., 2012a. Effects of glyphosate on the
mineral content of glyphosate-resistant soybeans (Glycine max). Journal of
Agricultural and Food Chemistry 60, 67646771.
Duke, S.O., Wedge, D.E., Cerdeira, A.L., Matallo, M.B., 2007. The interactions of
synthetic herbicides with plant disease and microbial herbicides. In: Vurro, M.,
Gressel, J. (Eds.), Novel Biotechnologies for Biocontrol Agent Enhancement and
Management. Dordrecht, The Netherlands: Springer, pp. 277296.
Egan, J.F., Maxwell, B.D., Mortensen, D.A., Ryan, M.R., Smith, R.G., 2011. 2,4Dichlorophenoxyacetic acid (2,4-D)-resistant crops and the potential for evolution
of 2,4-D-resistant weed. Proceedings of the National Academy of Sciences of the
USA 108, E37.
Egan, J.F., Mortensen, D.A., 2012. Quantifying vapor drift of dicamba herbicides
applied to soybean. Environmental Toxicology and Chemistry 31, 10231031.
Ervin, D.E., Carrire, Y., Cox, W.J., et al., 2010. The Impact of Genetically
Engineered Crops on Farm Sustainability in the US. Washington, DC: National
Research Council, The National Academies Press, 250 pp.
Esser, H.O., Dupuis, G., Ebert, E., Vogel, C., Marco, G.J., 1975. s-Triazines.
In: Kearney, P.C., Kaufman, D.D. (Eds.), Herbicides: Chemistry, Degradation,
and Mode of Action, second ed., vol. 1. New York: Marcel Dekker, pp. 129208.
Everman, W.J., Mayhew, C.R., Burton, J.D., York, A.C., Wilcut, J.W., 2009.
Absorption, translocation, and metabolism of glufosinate in transgenic and
nontransgenic cotton, Palmer amaranth (Amaranthus palmeri) and pitted
morningglory (Ipomoea lacunosa). Weed Science 57, 357361.
Fedtke, C., Duke, S.O., 2005. Herbicides. In: Hock, B., Elstner, E.F. (Eds.), Plant
Toxicology. New York: Marcel Dekker, pp. 247330.
Feng, P.C.C., Baley, G.J., Clinton, W.P., et al., 2005. Glyphosate inhibits rust
diseases in glyphosate-resistant wheat and soybean. Proceedings of the National
Academy of Sciences of the United States America 102, 1729017295.
Feng, P.C.C., CaJacob, C.A., Martino-Catt, S.J., et al., 2010. Glyphosate-resistant
crops: Developing the next generation of products. In: Nandula, V.K. (Ed.),
Glyphosate Resistance in Crops and Weeds. Hoboken, NJ: John Wiley & Sons,
Inc, pp. 4565.
Feng, P.C.C., Clark, C., Andrade, G.C., Balbi, M.C., Caldwell, P., 2008. The control
of Asian rust by glyphosate-resistant soybeans. Pest Management Science 64,
353359.
Feng, P.C.C., Martino-Catt, S., Padgette, S.R., 2012. Inhibitors of 5-enolpyruvyl
shikimate 3-phosphate synthase (EPSPS).In: Kraemer, W. (Ed.) Modern Crop
Protection Compounds, second ed., vol. 1. Weinheim, Germany: Wiley-VCH
Verlag GmbH & Co, pp. 406423.
Feng, P.C.C., Ruff, T.G., Rangwala, S.H., Rao, S.R., 1997. Engineering plant
resistance to thiazopyr herbicide via expression of a novel esterase deactivation
enzyme. Pesticide Biochemistry and Physiology 59, 89103.
Feng, P.C.C., Tran, M., Chiu, T., et al., 2004. Investigations into glyphosate-resistant
horseweed (Conyza canadensis): Retention, uptake, translocation, and
metabolism. Weed Science 52, 498505.
112
Fernandez-Cornejo, J., Hallahan, C., Nehring, R., Wechsler, S., 2012. Conservation
tillage, herbicide use, and genetically engineered crops in the US: The case of
soybeans. AgBioForum 15, 231241.
Fernandez-Cornejo, J., Hendricks, C., Mishra, A., 2005. Technology adoption and
off-farm household income: The case of herbicide-tolerant soybeans. Journal of
Agricultural and Applied Economics 37, 549563.
Fernandez-Cornejo, J., McBride, W.D., 2002. Adoption of bioengineered crops.
Agricultural Economic Report No. 810. Washington, DC: USDA, ERS.
Fernandez-Cornejo, J., Mishra, A., Nehring, R., et al., 2007. Off-farm income,
technology adoption, and farm economic performance. ERS Report No. 36.
Washington, DC: USDA, ERS.
Gaines, T.A., Henry, W.B., Byrne, P.F, et al., 2008. Jointed goatgrass (Aegilops
cylindrica) by imidazolinone-resistant wheat hybridization under eld conditions.
Weed Science 56, 3236.
Gaines, T.A., Zhang, W., Wang, D., et al., 2010. Gene amplication confers
glyphosate resistance in Amaranthus palmeri. Proceedings of the National
Academy of Sciences of the USA 107, 10271034.
Gardner, J.G., Nehring, R.F., Nelson, C.H., 2009. Genetically modied crops and
household labor savings in US crop production. AgBioForum 12,
303312.
Gardner, J.G., Nelson, G.C., 2008. Herbicides, glyphosate-resistance and acute
mammalian toxicity: Simulating an environmental effect of glyphosate-resistant
weeds in the USA. Pest Management Science 64, 470478.
Ge, X., d'Avignon, D.A., Ackerman, J.J.H., et al., 2011. Glyphosate-resistant
horseweed made sensitive to glyphosate: Low-temperature suppression of
glyphosate vacuolar sequestration revealed by 31P NMR. Pest Management
Science 67, 12151221.
Ge, X., d'Avignon, D.A., Ackerman, J.J.H., et al., 2012. Vacuolar glyphosatesequestration correlates with glyphosate resistance in ryegrass (Lolium spp.)
from Australia, South America, and Europe: A 31P NMR investigation. Journal of
Agricultural and Food Chemistry 60, 12431250.
Ge, X., d'Avignon, D.A., Ackerman, J.J.H., Sammons, R.D., 2010. Rapid vacuolar
sequestration: The horseweed glyphosate resistance mechanism. Pest
Management Science 66, 345348.
Gealy, D.R., Bradford, K.J., Hall, L., et al., 2007. Implications of gene ow in the
scale-up and commercial use of biotechnology-derived crops: Economic and
policy considerations. Council for Agricultural Science and Technology Issue
Paper 37. Ames, Iowa: CAST, 24 pp.
Givens, W.A., Shaw, D.R., Kruger, G.R., et al., 2009. Survey of tillage trends following
the adoption of glyphosate-resistant crops. Weed Technology 23, 150155.
Gleason, C., Foley, R.C., Singh, K.B., 2011. Mutant analysis provides insight into
the molecular mode of action of auxinic herbicides. PLoS One 6 (3),
e17245.
Goldberg, R., Rissler, J., Shand, H., Hassebrook, C., 1990. Biotechnology's Bitter
Harvest: Herbicide-Tolerant Crops and the Threat to Sustainable Agriculture. New
York: Environmental Defense Fund, Biotechnology Working Group, 73 pp.
Gonzalez-Torralva, F., Rojano-Delgado, A.M., Luque de Castro, M.D., Mulleder, N.,
De Prado, R., 2012. Two non-target mechanisms are involved in glyphosateresistant (Conyza canadensis L. Cronq.) biotypes. Journal of Plant Physiology
169, 16731679.
Goss, G.A., Dyer, W.E., 2003. Physiological characterization of auxinic herbicideresistant biotypes of kochia (Kochia scoparia). Weed Science 51, 839844.
Gougler, J.A., Geiger, D.R., 1981. Uptake and distribution of glyphosate in sugar
beet plants. Plant Physiology 68, 668672.
Grangeot, M., Chauvel, B., Gauvrit, C., 2006. Spray retention, foliar uptake and
translocation of glufosinate in Ambrosia artemisifolia. Weed Research 46,
152162.
Green, J.M., 2009. Evolution of glyphosate-resistant crop technology. Weed Science
57, 108117.
Green, J.M., 2012. The benets of herbicide-resistant crops. Pest Management
Science 68, 13231331.
Green, J.M., Castle, L.A., 2010. Transition from single to multiple herbicide-resistant
crops. In: Nandula, V.K. (Ed.), Glyphosate Resistance in Crops and Weeds.
Hoboken, NJ, USA: John Wiley & Sons, Inc., pp. 6791.
Green, J.M., Hale, T., Pagano, M.A., Andreassi, J.L., Gutteridge, S.A., 2009.
Response of 98140 corn with the gat4621 and hra transgenes to glyphosate and
ALS-inhibiting herbicides. Weed Science 57, 142147.
Green, J.M., Hazel, C.B., Forney, D.R., Pugh, L.M., 2008. New multiple-herbicide
crop resistance and formulation technology to augment the utility of glyphosate.
Pest Management Science 64, 332339.
Green, J.M., Owen, M.D.K., 2011. Herbicide-resistant crops: Utilities and limitations
for herbicide-resistant weed management. Journal of Agricultural and Food
Chemistry 59, 58195829.
Gressel, J., Al-Ahmad, H., 2005. Molecular containment and mitigation of genes
within crop Prevention of gene establishment in volunteer offspring and feral
strains. In: Gressel, J. (Ed.), Crop Ferality and Volunteerism. Boca Raton, FL:
CRC Press, pp. 371388.
Gressel, J., Valverde, B.E., 2009. A strategy to provide long-term control of
weedy rice while mitigating herbicide resistance transgene ow, and its
potential use for other crops with related weeds. Pest Management Science 65,
723731.
Grossmann, K., Ehrhardt, T., 2007. On the mechanism of action and selectivity of
the corn herbicide topramezone: A new inhibitor of 4-hydroxyphenylpyruvate
dioxygenase. Pest Management Science 63, 429439.
Gutteridge, S., Thompson, M.E., 2012. Acetohydroxyacid synthase inhibitors
(AHAS/ALS): Biochemistry of the target and resistance. In: Krmer, W., Schirmer,
U., Jeschke, P., Witschel, M. (Eds.), Modern Crop Protection Compounds, second
ed., vol. 1. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co, pp. 2949.
Hall, J.C., Donnelly-Vanderloo, M.J., Hume, 1996. Triazine-resistant crops: The
agronomic impact and physiological consequences of chloroplast function. In:
Duke, S.O. (Ed.), Herbicide-Resistant Crops: Agricultural, Environmental,
Economic, Regulatory, and Technical Aspects. Boca Raton, FL: CRC Press,
pp. 107126.
Hammer, P.E., Hinson, T.K., Duck, N.B., Koziel, M.G., 2007. Decarboxylases for
inactivation of glyphosate herbicides and their use in conferring herbicide
resistance. US Pat. Application, US 20070107078 A1 20070510.
Harikrishnan, R., Yang, X.B., 2002. Effects of herbicides on root rot and damping-off
caused by Rhizoctonia solani in glyphosate-tolerant soybean. Plant Disease 86,
13691373.
Harrington, K.C., Wooley, D.J., 2006. Investigations of how phenoxy-resistant
Carduus nutans biotypes survive herbicide spraying. New Zealand Journal of
Agricultural Research 49, 465474.
Hashem, A., Dhammu, H.S., 2002. Cross-resistance to imidazolinone herbicides in
clorsulfuron-resistant Raphanus raphanistrum. Pest Management Science 58,
917919.
Hausman, N.E., Singh, S., Tranel, P.J., et al., 2011. Resistance to HPPD-inhibiting
herbicides in a population of waterhemp (Amaranthus tuberculatus) from Illinois,
United States. Pest Management Science 67, 258261.
Heap, I., 2013. International Survey of Herbicide Resistant Weeds. Available at: www.
weedscience.org (accessed 30.05.13).
Henry, R.S., Wise, K.A., Johnson, W.G., 2011. Glyphosate's effect upon mineral
accumulation in soybean. Plant Management Network. doi:10.1994/CM-20111024-01-RS.
Hoffner, A.E., Jordan, D.L., Chandi, A., et al., 2012. Management of palmer
amaranth (Amaranthus palmeri) in glufosinate-resistant soybean (Glycine max)
with sequential applications of herbicides. Agronomy 131650, 7.
Huber, D.M., 2007. What about glyphosate-induced manganese deciency? Fluid
Journal 15, 2022.
Hurley, T.M., Mitchell, P.D., Friswald, G.G., 2009. Effects of weed resistance
concerns and resistance management practices n the value of Roundup Ready
crops. AgBioForum 12, 269280.
Inui, H., Shiota, N., Motoi, Y., et al., 2001. Metabolism of herbicides and other
chemicals in human cytochrome P450 species and in transgenic potato plants
co-expressing human CYP1A!, CYP2B6, and CYP2C19. Nippon Noyaku
Gakkasihi 26, 2840.
Jacob, C.A., Feng, P.C.C., Heck, G.R., et al., 2004. Engineering resistance to
herbicides. In: Christou, P., Klee, H. (Eds.), Handbook of Plant Biotechnology.
Chichester, UK: John Wiley & Sons, Ltd., pp. 353372.
James, C., 2012. 2012 ISAAA report on global status of Biotech/GM Crops.
International Service for the Acquisition of Agri-Biotech Applications Brief
442012. Ithaca, NY: ISAAA.
Joel, D.M., Kleifeld, Y., Losner-Goshen, D., Herzlinger, G., Gressel, J., 1995.
Transgenic crops against parasites. Nature 374, 220221.
Johal, G.S., Huber, D.M., 2009. Glyphosate effects on diseases of plants. European
Journal of Agronomy 31, 144152.
Jones, H.D., Sparks, C.A., 2009. Selection of transformed plants. Methods in
Molecular Biology 478, 2337.
Jugulam, M., McClean, M.D., Hall, J.C., 2005. Inheritance of picloram and 2,4-D
resistance in wild mustard (Brassica kaber). Weed Science 53, 417423.
Kaloumenos, N.S., Capote, N., Aguado, A., Eleftherohorinos, I.G., 2013. Red rice
(Oryza sativa) cross-resistance to imidazolinone herbicides used in resistant rice
cultivars grown in northern Greece. Pesticide Biochemistry and Physiology 105,
177183.
Kanampiu, F., Karaya, H., Burnet, M., Gressel, J., 2009. Needs for and effectiveness
of slow release herbicide seed treatment Striga control formulations for protection
against early season phytotoxicity. Crop Protection 28, 845853.
Kelley, K.B., Riechers, D.E., 2007. Recent developments in auxin biology and new
opportunities for auxinic herbicide research. Pesticide Biochemistry and
Physiology 89, 111.
Kishore, G.M., Jacob, G.S., 1987. Degradation of glyphosate by Pseudomonas sp.
PG2982 via a sarcosine intermediate. Journal of Biological Chemistry 262,
1216412168.
Kita, Y., Hanafy, M.S., Deguchi, M., et al., 2009. Generation and characterization of
herbicide-resistant soybean plants expressing novel phosphinothricin Nacetyltransferase genes. Breeding Science 59, 245251.
Klein, T.C., He, G., 1992. Identication and inheritance of metribuzin tolerance in
wild soybean. Crop Science 32, 684685.
Kleter, G.A., Harris, C., Stephenson, G., Unsworth, J., 2004. Comparison of
herbicide regimes and the associated potential environmental effects of
glyphosate-resistant crops versus what they replace in Europe. Pest Management
Science 64, 479488.
Kleter, G.A., Kuiper, H.A., 2003. Environmental fate and impact considerations
related to the use of transgenic crops. In: Voss, G., Ramos, G. (Eds.), Chemistry
of Plant Protection. Weinheim, Germany: Wiley-VCH, pp. 304321.
Knispel, A.L., McLachlan, S.M., Van Acker, R.C., Friesen, L.F., 2008. Gene ow and
multiple herbicide resistance in escaped canola populations. Weed Science 56,
7280.
Kniss, A.R., Sbatella, G.M., Wilson, R.G., 2012. Volunteer glyphosate-resistant corn
interference and control in glyphosate-resistant sugar beet. Weed Technology 26,
348355.
Kovach, J., Petzoldt, C., Degni, J., Tette, J., 1992. A method to measure the
environmental impact of pesticides; New York Agricultural Experiment Station.
New York's Food and Life Sciences Bulletin 139. Cornell University: Ithaca, NY,
USA, 1992 (regularly updated).
Kremer, R.J., Means, N.E., 2009. Glyphosate and glyphosate-resistant crop
interactions with rhizosphere microorganisms. European Journal of Agronomy 31,
153161.
Kruger, G.R., Davis, V.M., Weller, S.C., Johnson, W.G., 2010. Control of horseweed
(Conyza canadensis) with growth regulator herbicides. Weed Technology 24,
425429.
Larson, R.L., Hill, A.L., Fenwick, A., et al., 2006. Inuence of glyphosate on
Rhizoctonia and Fusarium root rot in sugar beet. Pest Management Science 62,
11821192.
Lawson, A.N., Van Acker, R.C., Friesen, L.F., 2006. Emergence timing of
volunteer canola in spring wheat elds in Manitoba. Weed Science 54,
873882.
Lee, C.D., Penner, D., Hammerschmidt, R., 2000. Inuence of formulated glyphosate
and activator adjuvants on Sclerotinia sclerotiorum in glyphosate-resistant and
-susceptible Glycine max. Weed Science 48, 710715.
Lee, D.R., Miller, D.K., Blouin, C.C., 2009a. Glyphosate-resistant cotton interference
in glyphosate-resistant soybean. Journal of Cotton Science 13, 174177.
Lee, D.R., Miller, D.K., Blouin, D.C., Clewis, S.B., Everman, W.J., 2009b.
Glyphosate-resistant soybean interference in glyphosate-resistant cotton. Journal
of Cotton Science 13, 178182.
Lee, H., Rustgi, S., Kumar, N., et al., 2011. Single nucleotide mutation in the barley
acetohydroxy acid synthase (AHAS) gene confers resistance to imidazolinone
herbicides. Proceedings of the National Academy of Science of the USA 108,
89098913.
Lee, K.Y., Townsend, J., Tepperman, J., et al., 1988. The molecular basis of
sulfonylurea herbicide resistance in tobacco. EMBO Journal 7,
12411248.
Li, X., Gong, Z., Koiwa, H., et al., 2001. Bar-expressing peppermint (Mentha x
Piperita L. var. Black Mitcham) plants are highly resistant to the glufosinate
herbicide Liberty. Molecular Breeding 8, 109118.
Li, X., Nicholl, D., 2005. Development of PPO inhibitor-resistant cultures and crops.
Pest Management Science 61, 277285.
Liu, C.-A., Zhong, H., Vargas, J., Penner, D., Sticklen, M., 1998. Prevention of
fungal diseases in transgenic, bialaphos- and glufosinate-resistant creeping bent
grass (Agrostis palustris). Weed Science 46, 139146.
Liu, C.-M., McLean, P.A., Sookdeo, C.C., Cannon, F.C., 1991. Degradation of the
herbicide glyphosate by members of the family Rhizobiaceae. Applied
Environmental Microbiology 57, 17991804.
Llewellyn, D., Last, D., 1996. Genetic engineering of crops for tolerance to 2,4-D. In:
Duke, S.O. (Ed.), Herbicide-Resistant Crops: Agricultural, Environmental,
Economic, Regulatory, and Technical Aspects. Boca Raton, FL: CRC Press,
pp. 159174.
Locke, M.A., Zablotowicz, R.M., Reddy, K.N., 2008. Integrating soil conservation
practices and glyphosate-resistant crops: Impacts on soil. Pest Management
Science 64, 457469.
113
Loecker, J.L., Nelson, N.O., Gordon, W.B., et al., 2010. Manganese response
in conventional and glyphosate resistant soybean. Agronomy Journal 102,
606611.
Londo, J.P., Bollman, M.S., Sagers, C.I., Lee, E.H., Watrud, L.S., 2011. Changes in
tness-associated traits due to the stacking of transgenic glyphosate-resistance
and insect resistance in Brassica napus L.Heredity 107, 328337.
Lorraine-Colwill, D.F., Powles, S.B., Hawkes, T.R., et al., 2003. Investigations into
the mechanism of glyphosate resistance in Lolium rigidum. Pesticide
Biochemistry and Physiology 74, 6272.
Lydon, J., Duke, S.O., 1988. Glyphosate induction of elevated levels of
hydroxybenzoic acids in higher plants. Journal of Agricultural and Food
Chemistry 36, 813818.
Lydon, J., Duke, S.O., 1999. Inhibitors of glutamine biosynthesis. In: Singh, B.K.
(Ed.), Plant Amino Acids. New York: Marcel Dekker, pp. 445464.
Madsen, K.H., Heitholt, J.J., Duke, S.O., Smeda, R.J., Streibig, J.C., 1995.
Photosynthetic parameters in glyphosate-treated sugar beet (Beta vulgaris L.).
Weed Research 35, 8188.
Marquardt, P., Krupke, C., Johnson, W.G., 2012. Competition of transgenic volunteer
corn with soybean and the effect on western corn rootworm emergence. Weed
Science 60, 193198.
Martino-Catt, S.J., Susan, J., Feng, P.C.C., Padgette, S.R., 2012. Genetically
modied herbicide-resistant crops: Overview. In: Krmer, W., Schirmer, U.,
Jeschke, P., Witschel, M. (Eds.), Modern Crop Protection Compounds, second
ed., vol. 1. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co,
pp. 399406.
Matringe, M., Sailland, A., Pelissier, B., Rolland, A., Zink, O., 2005. pHydroxyphenylpyruvate dioxygenase inhibitor-resistant plants. Pest Management
Science 61, 269276.
McBride, K.E., Kenny, J.W., Stalker, D.M., 1986. Metabolism of the herbicide
bromoxynil by Klebsiella pneumonieae subsp. osaenae. Applied Environmental
Microbiology 52, 325330.
Milligan, A.S., Daly, A., Parry, M.A.J., Lazzeri, P.A., Jepson, I., 2000. The
expression of a maize glutathione S-transferase gene in transgenic wheat confers
herbicide tolerance, both in planta and in vitro. Molecular Breeding 7, 301315.
Mink, P.J., Mandel, J.S., Sceurman, B.K., Lundin, J.I., 2012. Epidemiological
studies of glyphosate and cancer: A review. Regulatory Toxicology and
Pharmacology 63, 440452.
Mortensen, D.A., Egan, J.F., Maxwell, B.D., Ryan, M.R., Smith, R.D., 2012.
Navigating a critical juncture for sustainable weed management. BioScience 62,
7584.
Munier, D.J., Brittan, K.L., Lanini, W.T., 2012. Seed bank persistence of genetically
modied canola in California. Environmental Science and Pollution Research
International 19, 22812284.
Nandula, V.K. (Ed.), 2010. Glyphosate Resistance in Crops and Weeds. Hoboken,
NJ: John Wiley & Sons, Inc.
Nandula, V.K., Manthey, F.A., 2002. Response of kochia (Kochia scoparia) inbreds
to 2,4-D and dicamba. Weed Technology 16, 5054.
Nandula, V.K., Ray, J.D., Ribeiro, D.N., Pan, Z., Reddy, K.N., 2013. Glyphosate
resistance in tall waterhemp (Amaranthus tuberculatus) from Mississippi is due
to both altered target site and non-target site mechanisms. Weed Science 61 (3),
374383.
Nandula, V.K., Reddy, K.N., Rimando, A.M., Duke, S.O., Poston, D.H., 2007.
Glyphosate-resistant and -susceptible soybean (Glycine max) and canola
(Brassica napus) dose response and metabolism relationship with glyphosate.
Journal of Agricultural and Food Chemistry 55, 35403545.
Nelson, D.S., Bullock, G.C., 2003. Simulating a relative environmental effect of
glyphosate-resistant soybeans. Ecological Economics 45, 189202.
Nelson, K.A., Renner, K.A., Hammerschmidt, R., 2002. Cultivar and herbicide
selection affects soybean development and the incidence of Schlerotinia stem rot.
Agronomy Journal 94, 12701281.
Ng, C.H., Wickneswari, R., Salmijah, S., Teng, Y.T., Ismail, B.S., 2003. Gene
polymorphisms in glyphosate-resistant and -susceptible biotypes of Eleusine
indica from Malaysia. Weed Research 43, 108115.
Njiti, V.N., Myers, Jr., O., Schroeder, D., Lightfoot, D., 2003. Roundup ready
soybean: Glyphosate effects on Fusarium solanii root colonization and sudden
death syndrome. Agronomy Journal 95, 11401145.
Oard, J., Cohn, M.A., Linscombe, S., Gealy, D., Gravois, K., 2000. Field evaluation
of seed production, shattering, and dormancy in hybrid populations of transgenic
rice (Oryza sativa) and the weed, red rice (Oryza sativa). Plant Science 157,
1322.
Olofsdotter, M., Valverde, B.E., Madsen, K.H., 2000. Herbicide resistant rice (Oryza
sativa L.): Global implications for weedy rice and weed management. Annals of
Applied Biology 137, 279295.
114
Ortiz-Garca, S., Ezcurra, E., Schoel, B., Acevedo, F., Sobern, J., Snow, A.A., 2005.
Absence of detectable transgenes in local landraces of maize in Oaxaca, Mexico
(20032004). Proceedings of the National Academy of Sciences of the United
States of America 102, 1233812343.
Pankey, J.H., Grifn, J.L., Colyer, P.D., Schneider, R.W., Miller, D.K., 2005.
Preemergence herbicide and glyphosate effects on seedling disease in
glyphosate-resistant cotton. Weed Technology 19, 312318.
Park, K.W., Mallory-Smith, C.A., 2006. psbA mutation (Asn266 to Thr) in Senecio
vulgaris L. confers resistance to several PS II-inhibiting herbicides. Pest
Management Science 62, 880885.
Penna, J.A., Lema, D., 2003. Adoption of herbicide tolerant soybeans in Argentina:
An economic analysis. In: Kalaitzandonakes, N. (Ed.), Economic and
Environmental Impacts of Agrotechnology. New York: Kluwer-Plenum Publishers,
pp. 203220.
Perez-Jones, A., Mallory-Smith, C., 2010. Biochemical mechanisms and molecular
basis of evolved glyphosate resistance in weed species. In: Nandula, V.K. (Ed.),
Glyphosate Resistance in Crops and Weeds. Hoboken, NJ: John Wiley & Sons,
Inc., pp. 119140.
Pline, W.A., Lacy, G.H., Stromberg, V., Hatzios, K.K., 2001. Antibacterial activity of
the herbicide glufosinate on Pseudomonas syringae Pathovar glycinea. Pesticide
Biochemistry and Physiology 71, 4855.
Pollegioni, L., Schonbrunn, E., Siehl, D., 2011. Molecular basis of glyphosate
resistance: Different approaches through protein engineering. FEBS Journal 278,
27532788.
Powell, J.R., Swanton, C.J., 2008. A critique of studies evaluating glyphosate effects
on diseases associated with Fusarium spp. Weed Research 48, 307318.
Powles, S.B., 2008a. Evolution in action: Glyphosate-resistant weeds threaten world
crops. Outlooks on Pest Management 16, 256259.
Powles, S.B., 2008b. Evolved glyphosate-resistant weeds around the world: Lessons
to be learnt. Pest Management Science 64, 360365.
Powles, S.B., Lorraine-Colwell, D.F., Dellow, J.J., Preston, C., 1998. Evolved
resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia. Weed
Science 46, 604607.
Powles, S.B., Yu, Q., 2010. Evolution in action: Plants resistant to herbicides.
Annual Review of Plant Biology 61, 317347.
Pratley, J., Urwin, N., Stanton, R., et al., 1999. Resistance to glyphosate in Lolium
rigidum I.: Bioevaluation. Weed Science 47, 405411.
Preston, C., Belles, D.S., Westra, P.H., Nissen, S.J., Ward, S.M., 2009. Inheritance
of resistance to the auxinic herbicide dicamba in Kochia (Kochia scoparia). Weed
Science 57, 4347.
Prince, J.M., Shaw, D.R., Givens, W.A., et al., 2012. Benchmark study. IV. Survey of
grower practices for managing glyphosate-resistant weed populations. Weed
Technology 26, 543548.
Rahman, A., James, T.K., Trolove, M.R., 2008. Chemical control options for the
dicamba resistant biotype of fathen (Chenopodium album). New Zealand Plant
Protection 61, 287291.
Rajguru, S.N., Burgos, N.R., Shivrain, V.K., Stewart, J.M., 2005. Mutations in the
red rice ALS gene associated with resistance to imazethapyr. Weed Science 53,
567577.
Ransom, J., Kanampiu, F., Gressel, J., et al., 2012. Herbicide applied to
imidazolinone resistant-maize seed as a Striga control option of small-scale
African farmers. Weed Science 60, 283289.
Reddy, K.N., Norsworthy, J.K., 2010. Glyphosate-resistant crop production
systems: Impact of weed species shifts. In: Nandula, V.K. (Ed.), Glyphosate
Resistance in Crops and Weeds. Hoboken, NJ: John Wiley & Sons, Inc,
pp. 165184.
Reddy, K.N., Rimando, A.M., Duke, S.O., Nandula, V.K., 2008.
Aminomethylphosphonic acid accumulation in plant species treated with
glyphosate. Journal of Agricultural and Food Chemistry 56, 21252130.
Reichman, J.R., Watrud, L.S., Lee, E.H., et al., 2006. Establishment of transgenic
herbicide-resistant creeping bentgrass (Agrostis stolonifera L.) in nonagronomic
habitats. Molecular Ecology 15, 42434255.
Robertson, R.J., 2010. Physiological and biochemical characterization of glyphosate
resistant Ambrosia trida L., M.S. Thesis, Purdue University.
Robinson, A.P., Simpson, D.M., Johnson, W.G., 2012. Summer annual weed control
with 2,4-D and glyphosate. Weed Technology 26, 657660.
Rojano-Delgado, A.M., Cruz-Hipolito, H., De Prado, R., Luque de Castro, M.D.,
Franco, A.R., 2012. Limited uptake, translocation and enhance metabolic
degradation contribute to glyphosate tolerance in Mucuna pruriens var. utilis
plants. Phytochemistry 73, 3441.
Rosa, D.D., Basseto, M.A., Cavariani, C., Furtado, E.L., 2010. Efeito de
herbicidas sobre agents topatogenos. Acta Scientiarum Agronomy 32,
379383.
Rosinger, C., Bartsch, K., Shulte, W., 2012. Safeners for herbicides. In: Krmer, W.,
Schirmer, U., Jeschke, P., Witschel, M. (Eds.), Modern Crop Protection
Compounds, second ed., vol. 1. Weinheim, Germany: Wiley-VCH Verlag GmbH
& Co, pp. 371397.
Rosolem, C.A., de Andrade, G.J.M., Lisboa, I.P., Zoca, S.M., 2010. Manganese
uptake and redistribution in soybean as affected by glyphosate. Revista Brasileira
Ciencia Solo 34, 19151922.
Saari, L.L., Mauvais, C.J., 1996. Sulfonylurea-resistant crops. In: Duke, S.O. (Ed.),
Herbicide-Resistant Crops: Agricultural, Environmental, Economic, Regulatory,
and Technical Aspects. Boca Raton, FL: CRC Press, pp. 127142.
Salas, R.A., Dayan, F.E., Pan, Z., et al., 2012. EPSPS gene amplication in
glyphosate-resistant Italian ryegrass (Lolium perenne ssp. multiorum) from
Arkansas. Pest Management Science 68, 12231230.
Samac, D.A., Foster-Hartnett, D., 2012. Effect of glyphosate application on foliar
diseases in glyphosate-resistant alfalfa. Plant Disease 96, 11041110.
Sanchez-Olguin, E.R., Arieta-Espinoza, G., Lobo, J.A., Espinoza-Esqivel, A.M., 2009.
Assessment of gene ow from a herbicide-resistant indica rice (Oryza sativa L.)
to the Costa Rican weedy rice (Oryza sativa) in tropical America: Factors affecting
hybridization rates and characterization of F1 hybrids. Transgenic Research 18,
633647.
Sanogo, S., Yang, X.B., Lundeen, P., 2001. Field response of glyphosatetolerant soybean to herbicides and sudden death syndrome. Plant Disease 85,
773779.
Sanogo, S., Yang, X.B., Scherm, H., 2000. Effects of herbicides on Fusarium solani
f. sp. glycines and development of sudden death syndrome in glyphosate-tolerant
soybean. Phytopathology 90, 5766.
Scarabel, L., Cenghialta, C., Manuello, D., Sattin, M., 2012. Monitoring and
management of imidazolinone-resistant red rice (Oryza sativa L., var. sylvatica) in
cleareld Italian paddy rice. Agronomy 2, 371383.
Schafer, J.R., Hallett, S.G., Johnson, W.G., 2012a. Response of giant ragweed
(Ambrosia trida), horseweed (Conyza canadensis), and common lambsquarters
(Chenopodium album) biotypes to glyphosate in the presence and absence of
soil microorganisms. Weed Science 60, 641649.
Schafer, M.G., Ross, A.A., Londo, J.P., et al., 2012b. The establishment of
genetically engineered canola populations in the US. PLoS One 6 (10), e25736.
doi:10.1371/journal.pone.0025736.
Schefer, J.S., Dale, P.J., 1994. Opportunities for gene transfer from transgenic
oilseed rape (Brassica napus) to related species. Transgenic Research 3,
263278.
Seefeldt, S.S., Zemetra, R., Young, F.L., Jones, S.S., 1998. Production of
herbicide-resistant jointed goat grass (Aegilops cylindrica) x wheat (Triticum
aestivum) hybrids in the eld by natural selection. Weed Science 46,
632634.
Sellers, B.A., Smeda, R.J., Li, J., 2004. Glutamine synthetase activity and
ammonium accumulation inuence by time of glufosinate application. Pesticide
Biochemistry and Physiology 78, 920.
Sen Gupta, A., Heinen, J.L., Holaday, A.S., Burke, J.J., Allen, R.D., 1993. Increased
resistance to oxidative stress in transgenic plants that overexpress Cu/Zn
superoxide dismutase. Proceedings of the National Academy of Sciencees of the
USA 90, 16291633.
Serra, A.P., Marchetti, M.E., da Silva Candido, A.C., Ribiero Dias, A.C.,
Christoffoleti, P.J., 2011. Glyphosate inuence on nitrogen, manganese, iron,
copper and zinc nutritional efciency in glyphosate resistant soybean. Ciencia
Rural, Santa Maria 41, 7784.
Servaites, J.C., Tucci, M.A., Geiger, D.R., 1987. Glyphosate effects on carbon
assimilation, ribulose bisphosphate carboxylase activity, and metabolite levels in
sugar beet leaves. Plant Physiology 85, 370374.
Shah, D.M., Horsch, R.B., Klee, H.J., et al., 1986. Engineering herbicide tolerance in
transgenic plants. Science 233, 478481.
Shaner, D.L., Bascomb, N.F., Smith, W., 1996. Imidazolinone-resistant crops:
Selection, characterization, and management. In: Duke, S.O. (Ed.), HerbicideResistant Crops: Agricultural, Environmental, Economic, Regulatory, and
Technical Aspects. Boca Raton, FL: CRC Press, pp. 143157.
Shaner, D.L., Lindenmeyer, R.B., Ostlie, M.H., 2012. What have the mechanisms of resistance to glyphosate taught us? Pest Management Science 68,
39.
Shaw, D.R., Culpepper, S., Owen, M., Price, A., Wilson, R., 2012. Herbicideresistant weeds threaten soil conservation gains: Finding a balance for soil and
farm sustainability. Council for Agricultural Science and Technology Issue Paper
49. Ames, Iowa: CAST, 16 pp.
Shimizu, M., Goto, M., Hanai, M., et al., 2008. Selectable tolerance to herbicide by
mutate acetolactate synthase genes integrated into the chloroplast genome of
tobacco. Plant Physiology 147, 19761983.
115
Wakelin, A.M., Preston, C., 2006. A target-site mutation is present in a glyphosateresistant Lolium rigidum population. Weed Research 46, 432440.
Walsh, T.A., Schmitzer, P.R., 2012. The molecular mode of action of auxin
herbicides. In: Kraemer, W. (Ed.) Modern Crop Protection Compounds, second
ed., vol. 1. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co, pp. 277287.
Wang, Y., Browning, M., Ruemende, B.A., et al., 2003. Glufosinate reduces fungal
diseases in transgenic glufosinate-resistant bentgrasses (Agrostis spp.). Weed
Science 51, 130137.
Warwick, S.I., Lgre, A., Simard, M.-J., James, T., 2008. Do escaped transgenes
persist in nature? The case of an herbicide resistance transgene in a weedy
Brassica rapa. Molecular Ecology 17, 13871395.
Watrud, L.S., Lee, E.H., Fairbrother, A., et al., 2004. Evidence for landscape-level,
pollen-mediated gene ow from genetically modied creeping bentgrass with
CP4 EPSPS as a marker. Proceedings of the National Academy of Sciences of
the USA 101, 1453314538.
Webster, T.M., Nichols, R.L., 2012. Changes in the prevalence of weed species in
the major agronomic crops of the Southern US: 1994/1995 to 2008/2009. Weed
Science 60, 145157.
Wehrmann, A., van Vilet, A., Opsomer, C., Botterman, J., Schulz, A., 1996. The
similarities of bar and pat gene products make them equally applicable for plant
engineers. Nature Biotechnology 14, 12741278.
Weinberg, T., Stephenson, G.R., McLean, M.D., Hall, J.C., 2006. MCPA (4-chloro-2ethylphenoxyacetate) resistance in hemp-nettle (Galeopsis tetrahit L.). Journal of
Agricultural and Food Chemistry 54, 91269134.
Whitaker, J., York, A.C., Culpepper, A.S., 2007. Glyphosate-resistant Palmer
amaranth distribution and control in North Carolina and Georgia. Proceedings of
the Beltwide Cotton Conferences, pp. 12261227. Memphis, TN: National Cotton
Council of America.
Wiersma, A., 2012. Regional whole plant and molecular response of Kochia scoparia
to glyphosate. M.S. Thesis, Colorado State University, 55 pp.
Wild, A., Wendler, C., 1993. Inhibitory action of glufosinate on photosynthesis.
Zeitscrhift fr Naturforschung 48C, 360373.
Williams, A.L., Watson, R.E., DeSesso, J.M., 2012. Developmental and reproductive
outcomes in humans and animals after glyphosate exposure: A critical analysis.
Journal of Toxicology and Environmental Health, Part B: Critical Reviews 15,
3996.
Williams, G.M., Kroes, R., Munro, I.C., 2000. Safety evaluation and risk assessment
of the herbicide Roundup and its active ingredient, glyphosate, for humans.
Regulatory Toxicology and Pharmacology 31, 117165.
Wright, T.R., Shan, G., Walsh, T.A., et al., 2010. Robust crop resistance to broadleaf
and grass herbicides provided by aryloxyalkanoate dioxygenase transgenes.
Proceedings of the National Academy of Sciences of the USA 107,
2024020245.
Yajima, W., Hall, J.C., Kav, N.N.V., 2004. Proteome-level differences between
auxinic-herbicide-susceptible and -resistant wild mustard (Sinapis arvensis L.).
Journal of Agricultural and Food Chemistry 52, 50635070.
Yu, A., Han, H., Cawthray, G.R., Wang, S.F., Powles, S.B., 2013. Enhanced rates of
herbicide metabolism in low herbicide-dose selected resistant Lolium rigidum.
Plant, Cell and Environment 35, 818827.
Yun, C.-S., Hasegawa, H., Nanamiya, H., Terakawa, T., Tozawa, Y., 2009. Novel
bacterial N-acetyltransferase gene for herbicide detoxication in land plants and
selection marker in plant transformation. Bioscience, Biotechnology, and
Biochemistry 73, 10001006.
Zapiola, M.L., Mallory-Smith, C.A., 2012. Crossing the divide: Gene ow produces
intergenetic hybrid in feral transgenic creeping bentgrass population. Molecular
Ecology 21, 46724680.
Zelaya, I.A., Owen, M.D.K., VanGessel, M.J., 2007. Transfer of glyphosate resistance:
Evidence of hybridization in Conyza (Asteraceae). American Journal of Botany 94,
660673.
Zhang, J., Yin, J.-G., Hang, B.-J., et al., 2012. Cloning of a novel arylamidase gene
from Paracoccus sp. strain FLN-7 that hydrolyzes amid pesticides. Applied and
Environmental Microbiology 78, 48484855.
Zobiole, L.H.S., Kremer, R.J., Oliviera, R.S., Constantin, J., 2011a. Glyphosate
affects chlorophyll, nodulation and nutrient accumulation of second generation
glyphosate-resistant soybean (Glycine max L.). Pesticide Biochemistry and
Physiology 99, 5366.
Zobiole, L.H.S., Kremer, R.J., Oliveira, Jr., R.S., Constantin, J., 2011b. Glyphosate
affects micro-organisms in rhizopheres of glyphosate-resistant soybeans. Journal
of Applied Microbiology 110, 118127.
Zobiole, L.H.S., Kremer, R.J., Oliveira, R.S., Constantin, J., 2012. Glyphosate
effects on photosynthesis, nutrient accumulation, and nodulation in
glyphosate-resistant soybean. Journal of Plant Nutrition and Soil Science 175,
319330.
116
Zobiole, L.H.S., Oliveira, R.S., Huber, D.M., et al., 2010c. Glyphosate reduces shoot
concentrations of mineral nutrients in glyphosate-resistant soybeans. Plant and
Soil 328, 5769.
Zobiole, L.H.S., Oliveira, R.S., Kremer, R.J., Muniz, A.S., Oliviera, A., 2010a.
Nutrient accumulation and photosynthesis in glyphosate-resistant soybeans is
reduced under glyphosate use. Journal of Plant Nutrition 33, 18601873.
Zobiole, L.H.S., Oliviera, R.S., Visentainer, J.V., et al., 2010b. Glyphosate affects
seed composition in glyphosate-resistant soybean. Journal of Agricultural and
Food Chemistry 58, 45174522.
Relavant Websites
http://www.isaaa.org/inbrief/default.asp
International Service for the Acquisition of Agri-Biotech Applications.
http://www.weedscience.org
The International Survey of Herbicide Resistant Weeds.
Biotechnology: Pharming
S Kjemtrup, Monsanto Company, Research Triangle Park, NC, USA
TL Talarico, Medicago USA, Durham, NC, USA
V Ursin, Monsanto Company, Mystic, CT, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Adventitious agent A foreign entity that is introduced
inadvertently or accidentally. It often refers to viruses,
bacteria, or other organisms.
Biopharmaceuticals Drugs based on large biological
molecules.
Bioreactor A closed device or system for the culture of
cells in an aseptic manner.
Good manufacturing practice (GMP) A system for
ensuring that products are consistently produced and
controlled according to quality standards.
Monoclonal antibody Single-cell-originated proteins that
bind foreign target molecules with high specicity to elicit
various immune responses.
N-linked glycosylation Sugar chains added to a secretory
protein at the consensus sequence N-X-(S/T), where X is any
Introduction
Drugs based on large biological molecules, known as biologics
or biopharmaceuticals, have been produced in genetically
engineered animal and bacterial and yeast cells for more than
two decades and the current market for these products exceeds
US$149 billion. The growing global demand for biopharmaceuticals is fueling the development of platforms that increase
safety, capacity, and exibility and decrease production costs.
The tools of modern plant biotechnology now enable a spectrum of recombinant protein products to be produced in
plants, including biopharmaceuticals, and it is widely accepted
that plant-made pharmaceuticals (PMPs), or molecular
pharming, will help to meet the rising demand. Indeed, plants
can now be considered alongside traditional production
platforms and may provide numerous potential advantages
over microbial and mammalian production systems. These
include cost and scale of production, target exibility, intrinsic
safety, and quality of the products. Some of these factors are
contrasted in Table 1. By some estimates, PMPs could be
produced at 10% of the cost of microbial systems and 0.1% of
the cost of mammalian cell culture (Maxmen, 2012). In many
cases, production in plants can allow large-scale production
that can be adapted to the changing demands of the market.
Plants also lack the health risks that can arise from contamination by human pathogens, toxins, or oncogenes that
can be harbored in mammalian expression systems.
Plants, like any host system for protein expression, are not
a suitable host for production of every class of protein therapeutic, and there are a multitude of factors that can inuence
the success of PMP production. The key factors inuencing
protein accumulation include choice of a suitable host species,
design and optimization of the protein-coding sequence,
Products
Pharmaceutical products engineered for production in transgenic plants are primarily comprised of protein and lipid
molecules. In contrast, bioactive small molecules and other
plant chemical entities are isolated from the so-called medicinal crops. As eukaryotes, plants have protein-processing
machinery similar to mammals and are consequently a good
choice to synthesize complex or novel therapeutic proteins.
Here the authors discuss the main classes derived from these
recombinant protein production systems: therapeutic proteins,
vaccines, and antibodies, all with uses that span veterinary and
human pharmaceutical applications.
Therapeutic Proteins
Therapeutic proteins refer to pharmacologics used to treat a
clinical issue derived from a biochemical deciency. Examples
include enzymes, hormones, structural proteins, antimicrobial
agents, etc. (Nagels et al., 2012; Thomas et al., 2011).
The rst demonstration that production of a relevant
therapeutic protein was possible in a variety of plant species
doi:10.1016/B978-0-444-52512-3.00215-1
117
118
Biotechnology: Pharming
Table 1
Scale-up
capacity
Bacteria
Low
High
None
Yeast
Medium
High
Incorrect
Mammalian cell
culture
Transgenic
animals
Plant cell cultures
High
Medium
Correct
High
High
Correct
Viruses;
oncogenes
Viruses/prions
Medium
Medium
Correctb
Low
Acceptance; regulatory
Transgenic Plants
Low
Very high
Correctb
Low/
mycotoxins
Acceptance; regulatory
framework
Hurdles
Endotoxins
Other considerations
Vaccines
Vaccines are biological compounds that elicit immunogenic
responses to diseases, primarily caused by microorganisms.
In the context of PMPs, targeting second-generation vaccine
products (subunits of a microorganism) have been attractive
because the cell biology of plants is well suited for production of the glycoproteins or lipoproteins that typically constitute these antigenic molecules. Most interestingly, the plant
tissue itself has been promoted as the delivery vehicle for
vaccines by mucosal immunity (oral delivery) and this consideration drove initial development in the eld of vaccine
production.
An early example of vaccine production in plants is found
in the patent literature (Curtiss and Cardineau, 1997), where
the main claims concern immunity against pathogenic bacteria
Biotechnology: Pharming
Monoclonal Antibodies
As therapeutic proteins, monoclonal antibodies (MABs) are
single-cell-originated proteins that bind foreign target molecules with high specicity to elicit various immune responses.
Owing to their specicity, antibodies are used to treat diseases
such as arthritis, immune and inammatory diseases, or targetspecic cancers for immune system recognition. Additionally,
MABs are used for diagnostic purposes, disease prevention,
and transplant rejection treatments (Fischer et al., 2004). There
are ve types of antibody (immunoglobulin (Ig)) molecules
produced by mammals (IgG, IgM, IgA, IgD, and IgE). Antibodies of the IgG, IgM, and IgA types are the most commonly
expressed in plant pharmaceuticals, although other classes
such as Fab genes (the variable, epitope-recognizing region of
the antibody molecule) have also been successfully expressed.
IgGs and IgMs are general classes of antibodies that play important roles in protecting the body from pathogenic infection
(Knoll et al., 2012).
Because glycosylation pathways and subcellular protein
targeting and assembly are similar (but with important differences, see Section Purication) between plants and mammals, recombinant production of complex immunoglobulin
molecules was predicted to be feasible. Indeed, the rst report
of antibody production in plants showed that a functional
multimeric IgG could be isolated from a cross from separate N.
tabacum plants stably transformed for the subunit chain
components (Hiatt et al., 1989). Importantly, assembly of this
functional molecule required a secretion signal on both
chains, highlighting the importance of correct subcellular targeting. Production of antibodies has now been demonstrated
in plant species including Arabidopsis, carrot, potatoes, soybean, maize, alfalfa, and various tobacco species, among
others. There are a variety of strategies for expression of these
complex molecules that include a single transformation event
(either stable or transient) from one transfer deoxyribonucleic
acid (T-DNA) as well as utilization of specic subcellular targeting technologies to achieve efcacious glycosylation of the
antibody (De Muynck et al., 2010).
Several plant-produced antibody products have reached
clinical testing stage. A product that prevents tooth decay,
CaroRx, has been tested by Planet Biotechnology. By binding to the bacteria Streptococcus mutans, this antibody keeps
the bacteria from remaining on the teeth, preventing decay.
Another example where pharmaceutical production in plants
provides an advantage is the development of antibody
microbicide directed at human immunodeciency virus infection/acquired immunodeciency syndrome (Lotter-Stark
et al., 2012). This promising therapy is closer to reality as
119
Production Systems
Plant biotechnology has successfully enabled the development
of crops with new or improved attributes through ectopic expression (or suppression) of recombinant proteins, many of
which have achieved commercial success. These include crops
with quantitative changes in intrinsic properties, such as yield,
tolerance to abiotic or biotic stresses, or qualitative changes in
composition, such as accumulation of oils or with altered lipid
proles. The optimal expression of the recombinant protein is
generally determined empirically by conducting phenotypic
analysis, and often very low levels of the recombinant protein
are needed to produce the desired trait without undesired
off-types. In contrast, successful PMP production is largely a
function of maximizing the protein yield, stability, and where
necessary, posttranslational processing of the target protein. It
is generally accepted that there is no reliable way of predicting
a successful plant host, protein expression level, stability and
assembly, and in the case of vaccines, whether the protein will
be antigenic. Therefore, each of these aspects must be determined empirically. Although the range of available plant expression hosts for molecular farming is impressive, the choice
becomes even more varied when the different expression systems are considered Figure 1. In this article, an expression host,
an expression system, and production system are considered as
separate entities: an expression host is dened as a particular
species, whereas an expression system is dened as transformation and expression methods, including posttranslational
strategies that address protein stability and efcacy. Production
system describes the propagation and growth to harvest of the
expression host. The combination of host and expression system results in an expression platform, for example, stably
transformed rice seeds, transiently transformed alfalfa leaves,
stably transformed tobacco suspension cells, virus-infected
spinach leaves, etc. Factors that must be considered to guide
the selection of the expression host and the assembly of
the appropriate expression platform include the intrinsic
properties of the protein; yield and scale-up requirements to
meet expected market demands; speed of development of a
new product; product quality criteria, such as correct protein
folding and glycosylation, to humanize the therapeutic;
downstream processing and purity needs; delivery route; containment issues; and biosafety and regulatory considerations.
For each of these factors, there are specic elements of the
production platform that can be optimized (Figure 2). These
elements will be discussed in the following paragraphs.
Expression Host
A broad range of plant species have been used for the production of therapeutics, including alfalfa, Arabidopsis, banana,
barley, carrot, false ax, ax, lettuce, maize, pea, potato, safower, spinach, soybean, tobacco, and tomato (Twyman et al.,
2013). Advantages of leafy crops, such as alfalfa and tobacco,
include high biomass yield, multiple growth cycles per year,
120
Biotechnology: Pharming
Hairy root
Transgenic cell
culture
Cell culture
Leafy plants
Stable
expression
Transgenic
plants
Seed/Grain
Transplastomic
plants
PMP
Leafy plants
Viral mediated
Transient
expression
Whole plant
Agrobacterium
mediated
Stable transformation
Transient expression
Stable transformation
Similar to mammalian
Similar to mammalian
Similar to mammalian
Scalability
Highly scalable
Moderately scalable
Limited, costly
Processing/GMP
Complex, costly
Complex, costly
Partial containment
Aseptic culture
Ventria bioscience
Stably transformed rice
VEN100 rh-lactoferrin
Phase II
Medicago
Transient expression in
tobacco
Influenza vaccine
Phase II
Protalix
Carrot soot suspension
cells
Elelyso (taliglicerase alfa)
FDA cleared
Criteria
Speed of
development
Glycosylation
Biosafety
Examples
Company
Production system
Compound
Stage of
development
Figure 2 Comparison of key factors associated with different PMP production systems.
Biotechnology: Pharming
Expression Systems
The expression system encompasses the transformation system
and the expression strategy, including posttranslational
modications (PTMs) of PMPs.
121
Transformation
Transformation refers to the process of delivering a recombinant DNA or RNA molecule to cells from which protein is
produced, and the transformation system utilized will impact
the outcome to at least as great an extent as host species.
Transformation can be stable or transient. Stable transformation delivers DNA to either the nuclear or the plastid genomes,
where the genetic material becomes integrated into the genome
and becomes a stable part it. Efcient nuclear transformation
systems have been developed for a broad range of crop plants.
In brief, a DNA cassette containing the genetic code for the
desired protein and instructions for the required spatial and
temporal expression levels and patterns is introduced into the
plant tissue either by direct means, for example, using biolistics, or via cocultivation of plant cells with transgenic Agrobacterium engineered to deliver the DNA expression cassette to
the plant cells. Cells in which the transgenic material has successfully integrated into the nucleus are selectively cultured
away from the surrounding nontransgenic cells, and using
specic hormone regimes, transgenic plants are regenerated
and sampled for protein expression. Plants containing the desired levels of the target protein can be grown to maturity and
assessed for genetic quality and stability. Transgenic plant lines
produced through stable transformation typically exhibit genetic stability over many generations, and accordingly, this plant
production system is highly scalable. Nevertheless, there are
disadvantages to stable transformation. Stable transformation
is a time-consuming and costly process. The recovery of a single
line with the required attributes can take several years. Low
protein yield is the most common problem encountered using
stable nuclear transformation, although optimization strategies
exist to maximize protein yields.
An alternative to stable nuclear transformation is insertion
of the coding material into the chloroplast genome, creating a
so-called transplastomic plant. The presence of up to 100
chloroplasts in a leaf cell and up to 100 genomes per chloroplast allows very high protein accumulation. In one case, it was
reported that levels of proinsulin accumulated between 47%
and 53% of total leaf protein of transplastomic plants. With
these protein yields, it is estimated that one acre of transplastomic tobacco could produce up to 20 million doses of insulin
per day (Boyhan and Daniell, 2011). In another case, the
human papillomavirus antigen was fused with an adjuvant and
successfully expressed in transplastomic tobacco. This outcome
paves the way for the development of low-cost adjuvant-coupled vaccines that may eventually obviate the need for cold
chain and sterile needs (Waheed et al., 2011). A summary of
vaccine antigens against different human diseases expressed in
plastids is presented in Lssl and Waheed (2011). This transformation system has some drawbacks. Because plastids lack
glycosylation, this production system is suited only for nonglycosylated proteins, and the number of species for which
efcient plastid transformation technology exists is very limited. Currently, tobacco and lettuce represent the higher plant
species that have robust chloroplast transformation systems.
An alternative to stable transformation that overcomes
many of the aforementioned limitations is transient expression. Transient expression enables rapid transgene expression and massive protein accumulation, often within days.
For example, at the conclusion of a 30-day manufacturing
122
Biotechnology: Pharming
Expression Methods
Although the intrinsic production capacity of the chosen
production platform cannot be modied easily as it is
dependent on the overall biomass yield of the crop, the
specic yield of recombinant protein per unit of plant biomass
can be inuenced by the optimization of transgene expression,
which is achieved through expression construct design. Gene
expression is regulated at multiple levels in plants. In play
are regulatory processes for transcription, translation, PTM,
Tissue-specific enhancers/suppresors
Promoter
5-Noncoding
Transit Glycosylation
peptide
sequence
Coding region
ER retention
signal
Cleavage/Polyadenylation
signal
3-Noncoding
Vector sequences
Figure 3 Representation of a plant expression vector, containing coding and noncoding elements necessary for protein production and
posttranslational modications.
Biotechnology: Pharming
the high expressing constitutive CaMV 35S or the maize ubiquitin-1 promoter, the polyadenylation sites of the CaMV 35S
transcript, the A. tumefaciens nos gene, or the pea ssu gene are
often used (Ma et al., 2003; Table 2).
Posttranscriptionally, translational efciency of the mRNA
transcript can also have a profound impact on protein accumulation. One of the approaches to increase the translation
efciency in a given host is to optimize the codon usage in the
mRNA, by changing the nucleotide (DNA) sequence without
changing the amino acid sequence, to suit the respective host
(Gustafsson et al., 2004; Desai et al., 2010). Preferred codon
usage differs between monocots and dicots, and it is greatly
different even between nucleus and plastid of the same plants
(Desai et al., 2010). Cryptic splice sites and sequences with the
potential to form hairpins can also be removed from the
construct (Gisby et al., 2011).
There are many modications a protein can undergo posttranslationally, and early consideration of these in a PMP
project is necessary to guide the strategy of expression and purication. PTMs include disulde bond formation, hydroxylation,
lipidation, and importantly, N-linked glycosylation. Disulde
bond formation improves protein stability in the cell, and
during purication, hydroxylation and lipidation are frequently
considered for product delivery, whereas appropriate N-linked
glycosylation of PMPs is important for protein stability. These
modications are determined by subcellular targeting.
Therefore, after promoter choice and codon optimization,
the next most important aspect of construct design is the inclusion of sequences that control subcellular targeting of the
protein. This is another general method to increase the yield
of recombinant proteins because the compartment in which
a recombinant protein accumulates inuences its folding, assembly, and PTM (Ma et al., 2003; Schillberg et al., 2005).
Comparative targeting experiments have shown that the
secretory pathway is a more suitable compartment for folding
Table 2
123
Protein
Tissue
Plant species
Promoter
Cell culture
Tobacco
Inducible: Tetracycline
derepressed
9.31.4 mg g1 fresh
weight
Taliglucerase
B-subunit of the heat-labile
toxin
Cell culture
Hairy root
Carrot
Nicotiana tabacum
330 mg g1 fresh
weight
H1N1
Leaf
HBsAg
Tuber
Nicotiana
benthemenia
Potato
Human transferrin
Seed
Rice
Seed
Arabidopsis
Leaf
Tobacco
Leaf
Potato
a1-Antichymotrypsin protein
CaMV 35S+PB33
(patatin)
rice seed storage
protein glutelin 1
gene promoter
Oleosin promoter
cauliower mosaic
virus 35S (CaMV
35S)
CaMV 35S with
coexpressed
protease inhibitor
Subcellular
localization
Production level
200 mg g1 fresh
weight
1 mg g1
Endomembrane
system
810 mg g1 seed
weight
Oil bodies
Endoplasmic
reticulum stacks
0.7% TSP
Cytosol
124
Biotechnology: Pharming
Biotechnology: Pharming
GlcNAc
Man
Gal
Neu5Ac
Fuc
Xyl
Protein
N-X-S/T
Protein
Human
125
N-X-S/T
Plant
Figure 4 Some key similarities and differences of complex human and plant glycosylation. Note the xylose present on the plant structure, not
present in human structure, and the sialic acid structure at the terminal of the human structure. Structures are elaborated according to Consortium
of Functional Glycomics essential symbols nomenclature: http://www.functionalglycomics.org/static/consortium/Nomenclature.shtml
Thomas, 2012). Finally, a recent report highlights the successful addition of terminal sialic acid residues onto plantproduced glycoproteins by introducing the human pathway
into Nicotiana benthamiana (Castilho et al., 2010).
Another PTM with therapeutic consequences is Oglycosylation. In O-glycosylation, fucose, xylose, mannose,
GlcNAc, galactose, glucose, or N-acetylgalactosamine (GalNAc)
residues are added to the hydroxyl group of serine or threonine
on proteins that have completed their folding in the GA.
In mucin-type O-glycosylation, additional sugars are then
added to these structures. The resultant modication affects
biological activity of proteins involved in inammation response, coagulation, cancer, and viral infection pathways.
Unlike N-linked glycosylation, the O-linked pathway in plants
is not as well described as in mammalian systems; although
monosaccharides are added to proline, hydroxyproline, and
serine in plants, mammalian-like additions (e.g., GlcNac) have
just recently been described (Gomord et al., 2010). In biopharming, O-glycosylation has primarily been used to stabilize
proteins to increase their shelf life by adding an O-glycosylation consensus sequence to the C-terminus of the protein
(Webster and Thomas, 2012).
Hydroxylation of proline on proteins is a PTM that
affects stability in some proteins; collagen is an example. The
hydroxyproline modication has been characterized in plants
at only low levels; consequently, a humanization approach has
been used to recapitulate this modication in plants. Coexpression of collagen and recombinant prolyl 4-hydroxylase in
transgenic maize seeds has been shown to produce effective
levels of hydroxyproline-stabilized collagen (Xu et al., 2011).
This modication has been used more to improve stability and
shelf life of the protein rather than address its immunological
effect (Webster and Thomas, 2012).
The addition of lipid molecules onto proteins (e.g., palmitoylation and myristoylation) is a PTM that has been considered in PMP design. Lipidation serves primarily to target the
protein on the plasma membrane or other intracellular lipid
location and also has been shown to have roles in signal
transduction. Correct subcellular targeting of PMPs that require lipidation is important; lipidation of the OspA vaccine
against Lyme disease or the Nef12 protein that addresses the
immune response to HIV indicates that chloroplast targeting is
a key to developing efcacious proteins (Webster and Thomas,
2012).
Production System
Production refers to the method of propagating, growing, or
producing plant, organs, or cells from which the PMP will be
puried. To a great extent, the host organism and expression
strategy will dictate the production method. For example, expression of a recombinant protein in seeds requires eld
production of stably transformed whole plants. Leaf expression can be achieved in eld or protected culture and be
the product of stable, transient, or plastid transformation
methods. Because the production method has signicant implications for cost, scale-up, and risk management, it needs to
be factored early in the process. The regulatory framework for
genetically modied organism crops is presented elsewhere
in this volume, and regulatory considerations for PMP are
discussed in the Section Regulatory Considerations; hence,
they will not be addressed in this section. Where production
method as it factors into the key decisions for PMP production
will be reviewed.
There are essentially ve options for PMP production.
These are: growth of whole stably transformed plants in open
elds; growth of whole stably or transiently transformed plants
in a greenhouse; growth of whole stably or transiently transformed plants in an articially lit growth chamber; production
of lower or aquatic plants in a semiclosed system; and production of plant cells in a sterile, closed bioreactor (Table 3).
Growth in open elds theoretically allows innite scale-up,
limited only by the amount of seed produced to establish the
crop. Indeed, perennial crops, such as alfalfa, can even allow
multiyear production. Field production provides the greatest
exibility for production platforms, as it encompasses the
126
Biotechnology: Pharming
Table 3
Production system
Type of plant
Advantages/challenges
Example
Closed system
Protalix
Biotherapeutics
Carrot cell culture
Taliglucerase alfa
Semiclosed system
Greenhouse
Field
CO2 control
Automatable
Expensive utilities
Transient expression possible
Tobacco, lettuce, tomatoes, alfalfa, etc.
Sun supplies energy
Supplemental light required to supplement
seasonal affects
Transient expression possible
Automatable
Inexpensive
Tobacco, lettuce, tomatoes, alfalfa, potatoes, bananas, Sun supplies energy
etc.
Containment difcult
No barrier to pests
Transmission through animals and birds
broadest number of host species and expression systems. Fieldbased production also does not require a capital-intensive
infrastructure. Nevertheless, there are signicant drawbacks
that have to date limited the number of PMPs produced
in open elds. As mentioned in the Section Transformation,
the development of stably transformed transgenic or transplastomic crop lines for commercial production requires
many years and millions of dollars in development costs,
making this potentially the highest cost production method.
In addition, regulatory agencies, such as the United States
Department of Agriculture (USDA), impose more stringent
regulations than what is required for transgenic plants expressing nontherapeutic proteins. The primary difference for
PMPs over the so-called input traits for genetically engineered
crops entails the level of containment required when a crop
expressing an output trait, such as PMP, is in the eld. For
example, elds are subject to multiple inspections, the eld
must be surrounded by a 50-foot fallow zone, isolation distance from similar crops is strictly enforced with windpollinated crops at a larger distance than self-pollinated crops,
and equipment must be dedicated to the eld trial for the
entire eld season and then cleaned using the USDA-approved
Standard Operating Procedures. No crop can be planted on the
plot the following year, so that volunteers can be destroyed.
These requirements increase production costs over other
types of transgenic crops (Breyer, 2009). For a list of crops
for which eld trial permits have been obtained and case
studies for eld release of PMP, see Breyer et al. (2012). A
recent survey of farmers perceptions of biopharming showed
that the greater the number and cost of production changes,
the fewer the farmers were willing to adopt the technology,
even if prots increased (Hayes and Kostandini, 2013). An
Biolex/synthon
Lemna
Interferon alpha 2b
Fraunhofer
Nicotiana
Flu HA protein
Medicago
Nicotiana
Flu virus-like
particles
Prodigene
Corn
Trypsin
evolving, but yet not nalized, process for GMP for eld-based
production increases substantially the uncertainties of eld
production.
Growth in enclosed or protected environments, such as
greenhouses and growth chambers, has been widely adopted
for PMP, including vaccines, monoclonal antibodies (MABs),
and therapeutic proteins, for a variety of reasons, such as
providing physical containment and connement. Scale-up
is limited by facility size, whereas production can continue
year-round with multiple production runs possible annually.
Potato and a number of leafy crops, such as tobacco, alfalfa,
lettuce, and spinach, are examples of plants that can be grown
successfully in contained facilities. All can be stably transformed and for lettuce and tobacco, plastid transformation
systems have been developed. For a stably transformed line,
a master stock of transgenic seed (or asexually propagated
tubers in the case of potato) is produced that is planted
to initiate a run. Maximum exibility is achieved when
transient expression is used as the expression system. Although
transient expression systems exist for multiple plant species,
N. benthamiana is used almost exclusively for commercial scale
transient production, having the most well-developed system,
including multiple vectors (Hellens et al., 2005) and silencing
suppressors (Voinnet et al., 2003).
Plant cell culture techniques have been in existence since
the 1950s and have been utilized successfully to synthesize a
wide variety of natural compounds with therapeutic value,
including paclitaxel (Taxol). Recombinant therapeutic protein
was produced in tobacco cells in 1990, and since then, a
number of antibodies, enzymes, hormones, and growth factors
have been produced (Hellwig et al., 2004; Paul and Ma, 2011).
Plant cell cultures combine the advantages of whole plant
Biotechnology: Pharming
Purication
Biotherapeutics are typically administered by injection,
although oral administration of plant-produced vaccines has
been suggested and studied. In the case of injection, the
product typically is of a higher purity than a product that is
administered orally. Removal of host cell proteins, DNA,
vector (virus or Agrobacterium), and other plant-based compounds such as chlorophyll and nicotine during processing is
a necessity in injected products, whereas in an oral pharmaceutical, the presence of some of these compounds would be
fully acceptable.
Production of an injectable product requires an extensive
amount of purication. A purication process may be divided
into three general stages: product recovery, clarication, and
purication. Plant-based therapeutics use purication strategies common to other biologics (Li and Qiu, 2013). These
include chromatographic operations as well as multiple types
of ltration operations. These types of operations are well
documented in many reviews (Li and Qiu, 2013) and any
number of commercial suppliers of chromatography resins
and ltration media and equipment are willing to aid in development of these purication operations. An example of
techniques used in downstream purication of a plant-derived
vaccine is given in the Case Study at the end of this article.
However, plants, when used as hosts for protein production, present unique challenges to bioprocessing recovery
and clarication operations. Plants contain a large amount
of brous, solid material that is a barrier to recovery of
therapeutic molecules, especially protein. Thus, recovery operations for plant-based products often include a milling,
grinding, pressing, or digestion step that is more severe than
127
steps used in some microbial or mammalian cell culture operations. If the product of interest is prone to physical degradation, these operations may have a detrimental effect on
product quality. Elimination of these solids in the food and
beverage industry is often part of production processes and
thus methods of production may be adapted from these industries. However, the standards for equipment design and
cleaning are often more strict in the pharmaceutical industry as
compared with the food industry and thus specialized equipment may need to be designed.
Some plants contain low molecular weight compounds
that are subject to rapid oxidation and are capable of impacting coexisting proteins in the early-process stream. The
time required to separate these compounds from the target
protein and the methods used to prevent oxidation have a
major impact on product quality. Attention must be given
early in a plant-based process to a wide variety of compounds,
such as chlorophyll, phenolics, and alkaloids, that are not
present in microbial and mammalian cell-based processes.
Colored components, such as chlorophyll, are easily visible
as process residues in equipment used in plant-based processes
and present a challenge in removal from the process stream
as well as in equipment cleaning. The presence of pectins,
cellulose bers, and other viscous, slime-like residues are a
challenge to clean from processing equipment, such as centrifuges, lter housings, and mixing vessels. The selection of
proper cleaning agents is critical in validation of cleaning
operations in plant-based processes. The presence of these
viscous components in a process stream also creates challenges
in mixing, uid movement, and product recovery in the production process.
Production of an orally available biotherapeutic may require minimal or no purication. A transgenic plant that is
edible is in itself a potential product if the biotherapeutic can
survive the transport to the site of interaction (typically the
gut). However, use of a system such as cell culture or a transiently infected plant that is not typically part of the food
chain would require at least partial processing and formulation to make the product not distasteful to the patient. Removal of objectionable species in some production systems,
such as very high bioburden levels in Agrobacterium-inltrated
systems, may be required and would depend on the production system. Orally available biotherapeutic products may
be viewed as more akin to food than drugs from a safety
perspective; therefore, many process controls that exist in the
pharmaceutical industry would likely be relaxed and the
manufacturer could argue that compliance with the food
industrys regulations was sufcient. However, the burden of
proof of product stability, process reproducibility, and efcacy
would still fall on the manufacturer and adherence to pharmaceutical requirements in these areas would more likely apply.
Regulatory Considerations
The use of plants as the biofactories for making a proteinbased pharmaceutical requires a new level of consideration of
the risks associated with the plant and production process as
compared with those used for food or even medicinal smallmolecule products. Consideration and ranking of the risks will
128
Biotechnology: Pharming
Biotechnology: Pharming
129
Case Study
Case Study: Rapid Production of Vaccine in Plants to
Address Pandemic Threats
In 2010, Medicago was contacted by the Defense Advanced
Research Projects Agency (DARPA) to partner in a program
sponsored by the US government to prevent strategic surprise
from negatively impacting the US national security and create
strategic surprise for the US adversaries by maintaining the
technological superiority of the US military (DARPA Website).
Medicago was asked to demonstrate the potential of a plantbased biopharmaceutical vaccine to mitigate risks associated
with a pandemic threat because of the speed and exibility
with which a new vaccine could be produced by Medicago.
This request was also made because Medicago had clinical
experience with plant-based, highly immunogenic vaccines
that contained u hemagglutinin (HA) proteins in virus-like
particles. To accomplish the key milestones of the project,
Medicago had to build a facility, scale up, and transfer a vaccine production process in approximately 1 year and then
produce 10 000 000 doses of a u vaccine in 30 calendar days.
The following case study highlights the process used to produce the vaccine.
The production of the vaccine can be divided into three
main sections: (1) transient protein expression after Agrobacterium delivery to leaf tissue, (2) protein separation from
plant biomass via tissue digestion, and (3) protein purication via standard industrial ltration and chromatographic
techniques.
130
Biotechnology: Pharming
Figure 5 The pick and place robot used for plant arrangement for
greenhouse operations.
Production: Processing
Once inltrated, plants were placed in an environmentally
controlled chamber under strict conditions for temperature,
light intensity, and light exposure cycle for a specied period
of time to allow protein expression and VLP accumulation in
the leaves of the plant. After incubation, leaves of the plants
were harvested manually and placed on a conveyor. The biomass was transported via conveyor to a dicer and the leaves
were cut into small squares. Diced leaves were transported via
conveyor to a stainless steel, mechanically agitated digestion
Biotechnology: Pharming
Conclusions
The project was deemed successful because the facility construction was completed in approximately 1 year and the
production process was transferred and scaled up 30-fold.
After a series of development and engineering runs, the process
was demonstrated to be ready to support manufacturing
operations. At the conclusion of a 30-day manufacturing
131
References
Artsaenko, O., Kettig, B., Fiedler, U., Conrad, U., During, K., 1998. Potato tubers as
a biofactory for recombinant antibodies. Molecular Breeding 4, 313319.
Barbante, A., Irons, S., Hawes, C., et al., 2008. Anchorage to the cytosolic face of
the endoplasmic reticulum membrane: A new strategy to stabilize a cytosolic
recombinant antigen in plants. Plant Biotechnology Journal 6, 560575.
Barta, A., Sommergruber, K., Thompson, D., et al., 1986. The expression of a
nopoline synthase-human growth hormone chimaeric gene in transformed
tobacco and sunower callus tissue. Plant Molecular Biology 6, 347357.
Bortesi, L., Rademacher, T., Schiermeyer, A., et al., 2012. Development of an
optimized tetracycline-inducible expression system to increase the accumulation of
interleukin-10 in tobacco BY-2 suspension cells. BMC Biotechnology 12, 1240.
Boyhan, D., Daniell, H., 2011. Low-cost production of proinsulin in tobacco and
lettuce chloroplasts for injectable or oral delivery of functional insulin and
C-peptide. Plant Biotechnology Journal 9, 585598.
Breyer, D., Goossens, M., Herman, P., Sneyers, M., 2009. Biosafety considerations
associated with molecular farming in genetically modied plants. Journal of
Medicinal Plants Research 3, 825838.
Breyer, D., Schrijver, A., Goossens, M., Pauwels, K., Herman, P., 2012. Biosafety of
molecular farming in genetically modied plants. In: Wang, A., Ma, S. (Eds.),
Molecular Farming in Plants: Recent Advances and Future Prospects.
Netherlands: Springer, pp. 259274.
Castilho, A., Strasser, R., Stadlmann, J., et al., 2010. In planta protein sialylation
through overexpression of the respective mammalian pathway. Journal of
Biological Chemistry 285, 1592315930.
Chen, Q., He, J., Phoolcharoen, W., Mason, H.S., 2011. Geminiviral vectors based
on bean yellow dwarf virus for production of vaccine antigens and monoclonal
antibodies in plants. Human Vaccines 7, 331338.
Chiera, J., Bouchard, R., Dorsey, S., et al., 2007. Isolation of two highly active
soybean (Glycine max (L.) Merr.) promoters and their characterization using a
new automated image collection and analysis system. Plant Cell Reports 26,
15011509.
Curtiss, III, R., Cardineau, G.A., 1997. Oral immunization by transgenic plants. USA
Patent Application 457, 536563.
De Jaeger, G., Scheffer, S., Jacobs, A., et al., 2002.Boosting heterologous protein
production in transgenic dicotyledonous seeds using Phaseolus vulgaris
regulatory sequences. Nature Biotechnology 20, 12651268.
De Muynck, B., Navarre, C., Boutry, M., 2010. Production of antibodies in plants:
Status after twenty years. Plant Biotechnology Journal 8, 529563.
Desai, P.N., Shrivastava, N., Padh, H., 2010. Production of heterologous proteins
in plants: Strategies for optimal expression. Biotechnology Advances 28, 427435.
Fischer, R., Schillberg, S., Hellwig, S., Twyman, R.M., Drossard, J., 2012. GMP
issues for recombinant plant-derived pharmaceutical proteins. Biotechnology
Advances 30, 434439.
Fischer, R., Stoger, E., Schillberg, S., Christou, P., Twyman, R.M., 2004. Plant-based
production of biopharmaceuticals. Current Opinion in Plant Biology 7, 152158.
Gisby, M.F., Mellors, P., Madesis, P., et al., 2011. A synthetic gene increases
TGFb3 accumulation by 75-fold in tobacco chloroplasts enabling rapid
purication and folding into a biologically active molecule. Plant Biotechnology
Journal 9, 618628.
Gomord, V., Fitchette, A.-C., Menu-Bouaouiche, L., et al., 2010. Plant-specic
glycosylation patterns in the context of therapeutic protein production. Plant
Biotechnology Journal 8, 564587.
Goulet, C., Khalf, M., Sainsbury, F., D'aoust, M.A., Michaud, D., 2012. A protease
activity-depleted environment for heterologous proteins migrating towards the leaf
cell apoplast. Plant Biotechnology Journal 10, 8394.
132
Biotechnology: Pharming
Gustafsson, C., Govindarajan, S., Minshull, J., 2004. Codon bias and heterologous
protein expression. Trends in Biotechnology 22, 346353.
Hayes, M., Kostandini, G., 2013. Farmers perceptions of biopharming: Insights from
a tobacco biopharming survey. Southern Agricultural Economics Association
Annual Meeting, Orlando, FL, February 22013. Orlando, FL nep-agr: The NEP
report on Agricultural Economics. Available at: http://www.victoria.ac.nz/sef/
School of Economics and Finance of http://www.victoria.ac.nz/ Victoria
University of Wellington.
Hellens, R.P., Allan, A.C., Friel, E.N., et al., 2005. Transient expression vectors for
functional genomics,quantication of promoter activity and RNA silencing in
plants. Plant Methods 1, 113.
Hellwig, S., Drossard, J., Twyman, R.M., Fischer, R., 2004. Plant cell cultures
for the production of recombinant proteins. Nature Biotechnology 22, 14151422.
Hiatt, A., Caffferkey, R., Bowdish, K., 1989. Production of antibodies in transgenic
plants. Nature 342, 7678.
Huang, T.-K., Mcdonald, K.A., 2012. Bioreactor systems for in vitro production of
foreign proteins using plant cell cultures. Biotechnology Advances 30, 398409.
Knoll, A., Higgins, J.D., Seeliger, K., et al., 2012. The Fanconi anemia ortholog
FANCM ensures ordered homologous recombination in both somatic and meiotic
cells in Arabidopsis. Plant Cell 24, 14481464.
Lakshmi, P.S., Verma, D., Yang, X., Lloyd, B., Daniell, H., 2013. Low cost
tuberculosis vaccine antigens in capsules: Expression in chloroplasts, bioencapsulation, stability and functional evaluation in vitro. PLoS One 8, e54708.
Linard, D., Sourrouille, C., Gomord, V., Faye, L., 2007. Pharming and transgenic
plants. Biotechnology Annual Review 13, 115147.
Li, G., Brown, P.J.B., Tang, J.X., et al., 2011. Surface contact stimulates the just-intime deployment of bacterial adhesins. Molecular Microbiology 83, 4151.
Li, M., Qiu, Y.X., 2013. A review on current downstream bio-processing technology
of vaccine products. Vaccine 31, 12641267.
Lssl, A.G., Waheed, M.T., 2011. Chloroplast-derived vaccines against human
diseases: Achievements, challenges and scopes. Plant Biotechnology Journal 9,
527539.
Lotter-Stark, H.C.T., Rybicki, E.P., Chikwamba, R.K., 2012. Plant made anti-HIV
microbicides A eld of opportunity. Biotechnology Advances 30, 16141626.
Ma, J.K., Chikwamba, R., Sparrow, P., et al., 2005. Plant-derived pharmaceuticals
The road forward. Trends in Plant Science 10, 580585.
Ma, J.K., Drake, P.M.W., Christou, P., 2003. The production of recombinant
pharmaceutical proteins in plants. Nature Reviews Genetics 4, 794805.
Mason, H.S., Lam, D.M., Arntzen, C.J., 1992. Expression of hepatitis B surface
antigen in transgenic plants. Proceedings of the National Academy of Sciences
USA 89, 1174511749.
Maxmen, A., 2012. Drug-making plant blooms. Nature 485, 160.
Nagels, B., Weterings, K., Callewaert, N., Van Damme, E.J.M., 2012. Production of
plant made pharmaceuticals: From plant host to functional protein. Critical
Reviews in Plant Sciences 31, 148180.
Neutra, M.R., Kozlowski, P.A., 2006. Mucosal vaccines: The promise and the
challenge. Nature reviews Immunology 6, 149158.
Obembe, O.O., Popoola, J.O., Leelavathi, S., Reddy, S.V., 2011. Advances in plant
molecular farming. Biotechnology Advances 29, 210222.
Paul, M., Ma, J.K.C., 2011. Plant-made pharmaceuticals: Leading products and
production platforms. Biotechnology and Applied Biochemistry 58, 5867.
Rabindran, S., Stevenson, N., Roy, G., et al., 2009. Plant-produced human growth
hormone shows biological activity in a rat model. Biotechnology Progress 25,
530534.
Ramessar, K., Sabalza, M., Capell, T., Christou, P., 2008. Maize plants: An ideal
production platform for effective and safe molecular pharming. Plant Science
174, 409419.
Rawel, H.M., Kroll, J., Kulling, S., 2007. Effect of non-protein components on the
degradability of proteins. Biotechnology Advances 25, 611613.
Ruiz-May, E., Kim, S.J., Brandizzi, F., Rose, J.K.C., 2012. The secreted plant
N-glycoproteome and associated secretory pathways. Frontiers in Plant Science 3,
315.
Schillberg, S., Emans, N., Fischer, R., 2002. Antibody molecular farming in plants
and plant cells. Phytochemistry Reviews 1, 4554.
Schillberg, S., Twyman, R.M., Fischer, R., 2005. Opportunities for recombinant
antigen and antibody expression in transgenic plants Technology assessment.
Vaccine 23, 17641769.
Schillberg, S., Zimmermann, S., Voss, A., Fischer, R., 1999. Apoplastic and
cytosolic expression of full-size antibodies and antibody fragments in Nicotiana
tabacum. Transgenic Research 8, 255263.
Schnmann, P.D., Coia, G., Waterhouse, P., 2002. Biopharming the SimpliRED
HIV diagnostic reagent in barley, potato and tobacco. Molecular Breeding 9,
113121.
Sparrow, P.A.C., Irwin, J.A., Dale, P.J., Twyman, R.M., Ma, J.K.C., 2007. Pharmaplanta: Road testing the developing regulatory guidelines for plant-made
pharmaceuticals. Transgenic Research 16, 147161.
Sriraman, R., Bardor, M., Sack, M., et al., 2004. Recombinant anti-hCG
antibodies retained in the endoplasmic reticulum of transformed plants lack
core-xylose and core-alpha(1,3)-fucose residues. Plant Biotechnology Journal 2,
279287.
Stein, H., Wilensky, M., Tsafrir, Y., et al., 2009. Production of bioactive, posttranslationally modied, heterotrimeric, human recombinant type-I collagen in
transgenic tobacco. Biomacromolecules 10, 26402645.
Stoger, E., Sack, M., Fischer, R., Christou, P., 2002. Plantibodies: Applications,
advantages and bottlenecks. Current Opinion in Biotechnology 13, 161166.
Streateld, S.J., 2006. Mucosal immunization using recombinant plant-based oral
vaccine. Methods 38, 150157.
Thomas, D.R., Penney, C.A., Majumder, A., Walmsley, A.M., 2011. Evolution of
plant-made pharmaceuticals. International Journal of Molecular Sciences 12,
32203236.
Twyman, R.M., Schillberg, S., Fischer, R., 2013. Optimizing the yield of recombinant
pharmaceutical proteins in plants. Current Pharmaceutical Design 19,
54865494.
Van Dussen, L., Zimran, A., Akkerman, E.M., et al., 2012. Taliglucerase alfa leads to
favorable bone marrow responses in patients with type I Gaucher disease. Blood
Cells, Molecules & Diseases 50, 206211.
Vermij, P., 2006. USDA approve the rst plant-based vaccine. Nature Biotechnology
24, 233234.
Victoria, J.G., Wang, C., Jones, M.S., et al., 2010. Viral nucleic acids in liveattenuated vaccines: Detection of minority variants and an adventitious virus.
Journal of Virology 84, 60336040.
Vitale, A., Pedrazzini, E., 2005. Recombinant pharmaceuticals from plants:
The plant endomembrane system as bioreactor. Molecular Interventions 5,
216225.
Voinnet, O., Rivas, S., Mestre, P., Baulcombe, D., 2003. An enhanced transient
expression system in plants based on suppression of gene silencing by the p19
protein of tomato bushy stunt virus. Plant Journal 33, 949956.
Waheed, M.T., Thnes, N., Mller, M., et al., 2011. Plastid expression of a doublepentameric vaccine candidate containing human papillomavirus-16 L1 antigen
fused with LTB as adjuvant: Transplastomic plants show pleiotropic phenotypes.
Plant Biotechnology Journal 9, 651660.
Webster, D.E., Thomas, M.C., 2012. Post-translational modication of plant-made
foreign proteins; glycosylation and beyond. Biotechnology Advances 30,
410418.
Wirz, H., Sauer-Budge, A.F., Briggs, J., et al., 2012. Automated production of plantbased vaccines and pharmaceuticals. Journal of Laboratory Automation 17,
449457.
Xu, X., Gan, Q., Clough, R.C., et al., 2011. Hydroxylation of recombinant human
collagen type I alpha 1 in transgenic maize co-expressed with a recombinant
human prolyl 4-hydroxylase. BMC Biotechnology 11, 6981.
Yusibov, V., Streateld, S.J., Kushnir, N., 2011. Clinical development of plantproduced recombinant pharmaceuticals: Vaccines, antibodies and beyond. Human
Vaccines 7, 313321.
Relevant Websites
http://www.collplant.com/
CollPlant.
http://www.bio.org/articles/connement-plan-goes-extra-mile-safety
Connement Plan Goes the Extra Mile for Safety.
http://www.functionalglycomics.org/static/consortium/Nomenclature.shtml
Consortium of Functional Glycomics.
http://www.ime.fraunhofer.de/en/presse_medien/PharmaPlanta.html
Fraunhofer IME.
http://ibioinc.com/products/
iBiO, Inc.
http://www.labtimes.org/labtimes/issues/lt2012/lt04/lt_2012_04_38_40.pdf
Lab times.
http://www.planetbiotechnology.com
Planet Biotechnology Inc.
http://www.bio.org/articles/plant-made-pharmaceuticals-background-and-key-points
Plant-Made Pharmaceuticals Background and Key Points.
Biotechnology: Pharming
http://www.protalix.com/
Protalix Biotherapeutics.
http://www.aphis.usda.gov/wps/portal/aphis/ourfocus/biotechnology?
1dmy&urile=wcm%3apath%3a%2FAPHIS_Content_Library%2FSA_Our_Focus%
2FSA_Biotechnology%2FSA_Permits_Notications_And_Petitions
The Animal and Plant Health Inspection Service.
133
http://www.ema.europa.eu/docs/en_GB/document_library/Scientic_guideline/2009/
09/WC500002801.pdf
The European Medicines Agency.
http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/
GuidanceforIndustry/ucm055424.pdf
US Food and Drug Administration.
Glossary
Avirulence (Avr) factor A pathogen/pest effector
recognized either directly or indirectly by the corresponding
functional plant resistance (R) protein.
Effector A secreted protein or other molecule used by
plant-associated organisms to modulate plant metabolism,
suppress, activate, and reprogram plant defenses and
thereby enable successful colonization of plant tissues.
Host-induced gene silencing (HIGS) This technique is
used for silencing genes in plant-associated organisms. In
HIGS, silencing is triggered directly within the plant and
targets genes in plant pathogens or plant pests. Silencing
induces the production of short double-stranded RNA
(dsRNAs) in the host plant cells following one of the two
delivery methods: (1) microprojectile particle bombardment
of RNAi constructs into plant leaves or (2) stable plant
transformation with RNAi constructs. It is used primarily to
silence genes in obligate biotrophic species, which are not
transformable via stable transformation methods.
Leucine-rich repeat (LRR) A structural motif found in
many resistance (R) proteins that mediate effector-triggered
immunity and also in some pattern-recognition receptors
(PRRs). This type of motif contains leucines or other
hydrophobic amino acids at regular intervals over a stretch
of 23 or 24 amino acids. The LRR is reiterated numerous
times in most plant PRR and R proteins and can occur
extracellularly or intracellularly. The LRR forms a parallel
sheet structure within the protein. Within this structure, the
hydrophobic leucines are in the protein interior whereas the
other residues are surface exposed and form a surface
capable of interacting with other proteins. Different
interacting surfaces can be generated via single amino acid
changes, and this permits the evolution of specic
interactions. LRR motifs mediate proteinprotein and
receptorligand interactions in many organisms. The LRR
motifs in plant R proteins probably participate in effector
perception and PAMP perception.
Pathogen- or microbial-associated molecular patterns
(PAMPs/MAMPs) Molecules associated with groups of
Introduction
To fulll the future demands for food, feed, and ber of the
ever-growing human population, novel crop protection strategies are required to minimize potential losses to agricultural
crops from the myriads of pathogenic microbes and invertebrate pests that cause diseases and damage. These plantinfecting organisms include phytopathogenic bacteria, fungi,
oomycetes (water molds), viruses, insects, and nematodes. The
resulting biotic stresses cause major losses to crop yield and
product quality, and when severe disease epidemics occur this
can result in the complete loss of the harvest (Agrios, 2005).
134
doi:10.1016/B978-0-444-52512-3.00248-5
135
136
PTI
ETS
ETI
ETS
ETI
Variant
adapted
pathogen
Adapted
pathogen
Avr1
Disease
Avr2
Disease
ETS
fec
to
re r
cru
itm
e
Ef
Potential
pathogen
PAMPs
de
no
vo
ef
rec fecto
r ui
r
tm
en
t
Resistance
nt
Disease
ETS
R1
PRR
Defense
PTI
Nonhost
Defense
ETI
Variant plant genotype
R2
Defense
ETI
New variant
plant genotype
Figure 1 The zig-zag-zig model. The evolutionary arms race between pathogen and host is represented by the sequential activation of layers of
plant defense and by the acquisition of novel effectors, resulting in either disease resistance or disease susceptibility (disease). Phase 1: PAMP
recognition and PAMP-triggered immunity (PTI). Phase 2: The adapted pathogen evolves or acquires an effector (Avr1) that circumvents PAMP
recognition, resulting in effector-triggered susceptibility (ETS). Phase 3: A variant plant with the ability to express the resistance protein (R1) that is
capable of directly or indirectly detecting the presence of Avr1, resulting in effector-triggered immunity (ETI). Phase 4: A variant adapted pathogen
evolves or acquires an additional effector, Avr2, resulting in ETS. Phase 5: A new variant plant with the resistance protein (R2) capable of directly
or indirectly detecting Avr2, resulting in ETI.
137
138
139
140
Transgenic approach
P1
(Parent 1)
Resistant
P2
(Parent 2)
Susceptible
Isolate R genes
A
Resistant plant species A
B
Resistant plant species B
C
F1
resistant
Backcross
F1 to P2
25% P1
Six cycles of
backcrossing to P2
Backcross 7
introgressed
segment
containing
R gene
(a)
Transform into
advanced
breeding line
12.5% P1
6.25% P1
3.12% P1
1.65% P1
0.83% P1
0.42% P1
A, B, C
Multiple
resistance
in a single
transgenic
line
Susceptible
cultivar for
X improvement
Fewer backcrossing
generations required
before a useful new
line is identified
(b)
Figure 2 The traditional breeding approach is compared with plant transformation technology to introgress desirable genes into commercial crop
plants. (a) In a traditional breeding program, as much as 0.4% of the genome complement from each donor parent can reside in the seventh
backcross generation along with the R gene of interest (originally from parent 1). (b) By the transgene transformation approach, multiple R genes
from several initial sources are rst assembled into a single Ti plasmid. After T-DNA integration into the plant genome, these R genes cosegregate
in all subsequent breeding steps, greatly simplifying the subsequent backcrossing program for introducing multiple new traits into a cultivar. When
the transgenic transformation approach is used, the entire sequence of the introduced DNA is known, whereas in the traditional breeding program,
neither the total extent of the DNA introgressed nor its sequence identity is known. Reproduced from Hammond-Kosack, K.E., Jones, J.D.G., 2000.
Responses to plant pathogens. In: Buchanan, B.B., Gruissem, W., Jones, R.L. (Eds.), Biochemistry and Molecular Biology of Plants. Rockville, MD:
American Society of Plant Physiology, pp. 11021156, with permission from American Society of Plant Biologists.
141
142
(b)
8_A1
6_A1
10_A2
13_A2
Whole genome sequencing and in planta transcriptomics used to identify the 45 core RXLR Pi effectors
present in 3 isolates from lineage 13_A2 that are also expressed early during leaf infection.
All genes
398 in planta
induced Pi genes
3915
1123
683
157 110
39818
2237
RXLR effectors
104
14
0
19
4
891
06_3928A
(c)
45 induced core
Pi RXLR effectors
45
68
3544
79
20
20
T30-4
NL07434
Three different
13_A2 isolates
The conserved core effectors Avrblb1, Avrblb2, and Avrvnt1 are present in all 13_A2 isolates.
These are recognized when the corresponding R gene is expressed.
Rpi-blb1
Rpi-blb2
Rpi-vnt1.1
R gene present,
no disease
No R gene
full disease
(d)
T30-4
06_3928A
Stack R genes that recognize different conserved Pi effectors to confer durable resistance by plant
biotechnology or marker assisted selection.
Figure 3 Effector-guided R gene deployment based on the identication of core effectors that lack sequence polymorphism. The core effectorguided R gene strategy is currently being used in potato (S. tuberosum) to mitigate the impact of the 13_A2 lineage of the late blight pathogen,
Phytophthora infestans. This pathogen undergoes major population shifts in agricultural systems via the successive emergence and migration of
asexual lineages. (a) The aggressive lineage, termed 13_A2, in the European P. infestans population, is rapidly displacing the other older lineages.
(b) The method used to identify the core effector repertoire in the new aggressive lineage of P. infestans. (c) The 13_A2 isolates carry intact and
in planta induced Avrblb1, Avrblb2, and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding disease resistance
genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. This core effector-guided approach can also be used to exclude from the elite potato germplasm
improvement scheme any R genes already defeated because the cognate core effectors contain sequence polymorphisms that evade plant
recognition. (d) R gene stacking is achieved by the two methods described in Figures 2(b) and 4. Reproduced from Figures 4A, 7A, and 8B in
Cooke, D.E.L., Cano, L.M., Raffaele, S., et al., 2012. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen.
PLoS Pathogens 8 (10), e1002940.
broad-spectrum R genes is particularly worthwhile in geographical regions where many destructive pathogen and pest
species (i.e., diseasepest complexes) are prevalent.
Further isolation and characterization of R genes of this
type will ensure that the largest tool kit is available for plant
biotechnologists to exploit and engineer broader spectrum
disease resistance in crops in the future. In particular, analysis
of the ever increasing abundance of genome sequence information and transcriptome sequence information available for
crop species should reveal the R-gene sequences most similar
to those genes known to confer broad-spectrum resistance.
These can then be preferentially tested for function via plant
transformation.
143
144
(Boch and Bonus, 2010). To date, these are the only type of
bacterial effectors known to function in this way. This discovery led to the description of a new type of DNA-binding
protein and opened up the possibility of targeting specic
plant genes.
TALEs produced by the bacteria Xanthomonas oryzae pv.
oryzae (Xoo) contribute to virulence by transcriptionally activating specic rice S genes (Li et al., 2012). Molecular engineering has been used to create a wide array of TAL effector
nuclease (TALENs) fusion-proteins (Boch, 2011; Schornack
et al., 2013). TALENs contain the DNA recognition repeats of
native or customized Xoo TAL effectors and the DNA cleavage
domains of FokI nuclease. To engineer rice to be resistant to
Xanthomonas-incited bacterial blight, the promoter of the rice
susceptibility gene Os11N3 (also called OsSWEET14) was targeted for TALEN-based disruption. This gene encodes a
member of the SWEET sucrose-efux transporter family. Two
Xoo TAL effectors, AvrXa7 or PthXo3, activate this S gene and
divert plant sugars to the bacteria, whereas a third effector
PthXo1 targets a different S gene. The Os11N3 promoter
contains binding sites for the AvrXa7 or PthXo3 effectors near
the TATA box. The TALENs were designed to mutate DNA
required for the susceptibility function, but not the development function of Os11N3. Therefore, post transformation the
rice lines were rst screened by PCR for mutations in both TALeffector binding sites, but leaving the TATA box intact. This
modied Os11N3 gene was no longer inducible when the rice
plants were infected by Xoo strains that deliver either the
AvrXa7 or PthXo3 effectors into plant cells. The stable TALENmodied plants showed strong (though recessive) resistance to
infection by the AvrXa7- or PthXo3-dependent Xoo strains but
not the PthXo1-dependent pathogenic Xoo strain (Li et al.,
2012). So far, natural polymorphisms in the Os11N3 gene that
would confer disease resistance have not been identied in rice
germplasm. By using the TALENs to edit precisely a rice gene
required for Xoo susceptibility, desirable alleles conferring resistance can now be used in rice breeding programs.
In many successful plant breeding programs to control
fungi, bacteria, and viruses, recessively inherited disease-resistance genes are well known and well used. In these situations,
the lack of a susceptibility protein target or the production of a
nonfunctional protein variant is hypothesized to be the
underlying cause of these recessively inherited traits. One of the
best studied recessive r gene is mlo, which has functional
orthologs in barley, tomato, and Arabidopsis (Consonni et al.,
2006; Bai et al., 2008). The wild-type MLO allele codes for a
seven transmembrane-spanning protein that is required for
susceptibility to powdery mildew. A subset of the secreted
powdery mildew effectors, presumably successfully target MLO
to aid fungal infection of the plants epidermal cell layer. MLO
protein families are present in many other crop species, each
colonized by different adapted powdery mildew species. Interestingly, the virulence function of the P. syringae effector HopZ2
was found to target Arabidopsis MLO2, and plants harboring TDNA inserted into mlo2 alleles were found to exhibit resistance
to this unrelated pathogen (Lewis et al., 2012). Therefore, inactivation of the plant-susceptibility factor MLO in a range of
crop species, by using precise genome editing, should confer
resistance to different devastating powdery mildew species and
potentially other unrelated pathogens.
In Arabidopsis, genetic dissection of susceptibility to powdery and downy mildews has identied multiple S genes
whose impairment results in disease resistance. The Arabidopsis
S genes PMR4 and DMR1 encode a callose synthase and
homoserine kinase, respectively, and both genes have functional orthologs in tomato. Single-gene silencing in transgenic
tomato plants, using RNAi constructs resulted in resistance to
the powdery mildew fungus Oidium neolycopersici. However,
resistance to O. neolycopersici by DMR1 silencing was associated
with severely reduced plant growth whereas PMR4 silencing
was not (Huibers et al., 2013). Therefore, PMR4 is currently the
more suitable candidate gene for immediate deployment via
plant biotechnology. This highlights the fact that S proteins
have more than one function and are often important for plant
growth and development.
145
146
(i.e., expression of the PCD-inducing gene occurred in the absence of pathogen infection). As a consequence, engineering of
PCD in transgenic crops may reduce infection by biotrophic
pathogens or hemibiotrophic pathogens with a long latent infection phase, but favor infection by necrotrophic pathogens
that thrive on the induced dead plant tissue. This point is further illustrated by the results obtained using barley plants engineered to overexpress the cell death regulator BAX inhibitor-1
(BI-1), which inhibits plant defense responses (Babaeizad et al.,
2009). Transgenic barley plants overexpressing the BI-1 protein
grew normally and exhibited enhanced susceptibility to the
obligate biotrophic powdery mildew pathogen B. graminis f. sp.
hordei. The same barley seedlings overexpressing the BI-1 protein exhibited enhanced resistance to the hemibiotroph F. graminearum when compared with the T3 progeny which had not
inherited the transgene.
147
148
149
Plant defense
LB
pPl
Gene 1 - R
pP2
Gene 2 - anti-S
RB
Examples
PRR receptor from another
plant species
Effector guided R protein
deployment
Self-activated R* protein
Defense signaling protein
Figure 4 In the future, durable disease control could be achieved using a stacked R and anti-S transgene T-DNA cassette containing two
contrasting promoters and genes. The stacked R anti-S transgene T-DNA cassette approach combines the use of an effective resistance protein
or defense-signaling mechanism (R) with a pathogen or pest debilitation mechanism to minimize plant susceptibility (anti-S). The R and anti-S
genes are arranged in parallel and are expressed from two sequence unrelated promoters to ensure T-DNA cassette stability during the plant
transformation procedure. As the repertoire of tightly regulated pathogen- or pest-inducible plant promoters gradually increases, this would permit
the development of double-stacked R and anti-S transgene containing two genes for each type. Alternatively, if the emphasis was on preferentially
enhancing plant defense or debilitation of the pathogen, a triple-stacked R gene and one anti-S transgene, or vice versa could be engineered into a
single T-DNA cassette. Further stacking of the unique T-DNA cassettes could also be achieved through conventional plant breeding, by creating
hybrid plants or combining advanced elite pure lines. However, these multiple stacked R and anti-S T-DNA cassettes (i.e., 2 genes plus 2 genes)
achieved through breeding would be inherited as two distinct genetic loci. CRISPR/Cas9, clustered regularly interspaced short palindromic
repeats; LB and RB, the left and right borders of the T-DNA construct; PCD, programmed cell death; pP1 and pP2, two different tightly regulated
pathogen-inducible or pest-inducible promoters; R, resistance; S, susceptibility; TALENs, transcription activator-like effector nucleases; T-DNA,
transferred DNA.
rigorous eld testing and nally commercial release. In addition, many of the proposed single-gene transgenic disease
control solutions that failed to make the grade either in early
testing or later when tested under eld conditions have already
provided considerable useful and novel insight into the importance of other plant components and further information
on the ways in which pathogens can rapidly evolve to overcome plant defenses.
In a few instances, disease resistance has been engineered
using genes of animal origin. For example, one potentially
powerful approach is the overexpression of antibodies that
recognize microbe-specic cell surface components. Antibodies
that specically recognize a surface antigen of Fusarium species
were fused with an antimicrobial peptide. Expression of these
chimeric proteins in Arabidopsis or wheat conferred complete
immunity to fungal infection (Li et al., 2008; Safarnejad
et al., 2011). Although this approach provides highly efcient
crop protection, the application of this technology in agricultural crops that provide human nutrition may raise ethical
concerns.
Conventional plant breeding strategies targeted at delivering improved crop protection are now occurring at an
accelerated pace through the increased use of high-density
150
Acknowledgments
Rothamsted Research receives grant-aided support from the
Biotechnology and Biological Sciences Research Council
(BBSRC), UK. Kim E. Hammond-Kosack receives additional
support from within the BBSRC Institute Strategy Grants 20:20
wheat (BB/J/00426X/1), the National Capability PHI-base
grant (BB/J/004383/1), and from other BBSRC grants (BB/J/
004596/1, BB/1000488/1 and BB/K020056/1). KHK thanks
Lynda Castle, Professor John Lucas and Drs Jason Rudd, WingSham Lee, Kostya Kanyuka, Martin Urban, Neil Brown, and
Nelly Brewer for their helpful comments and suggestions on
the gures. The help of Dr Michael Hammond-Kosack in
proofreading the manuscript and assembling references is
highly appreciated.
References
Agrios, G.N., 2005. Plant Pathology. London: Academic Press.
Atkinson, H.J., Lilley, C.J., Urwin, P.E., 2012. Strategies for transgenic nematode
control in developed and developing world crops. Current Opinion in
Biotechnology 23, 251256.
Babaeizad, V., Imani, J., Kogel, K.H., Eichmann, R., Hckelhoven, R., 2009. Overexpression of the cell death regulator BAX inhibitor-1 in barley confers reduced
or enhanced susceptibility to distinct fungal pathogens. Theoretical Applied
Genetics 118, 455463.
Bai, Y., Pavan, S., Zheng, Z., et al., 2008. Naturally occurring broad-spectrum
powdery mildew resistance in a central American tomato accession is caused by
loss of Mlo function. Molecular PlantMicrobe Interactions 21, 3039.
Bellaore, S., Shen, Z., Rosso, M.-N., et al., 2008. Direct identication of the
Meloidogyne incognita secretome reveals proteins with host cell reprogramming
potential. PLoS Pathogens 4 (10), e100192.
Beale, M.H., Birkett, M.A., Bruce, T.J.A., et al., 2006. Aphid alarm pheromone
produced by transgenic plants affects aphid and parasitoid behavior. Proceedings
of the National Academy of Sciences of the USA 103, 1050910513.
Boch, J., 2011. TALEs of genome targeting. Nature Biotechnology 29, 135136.
Boch, J., Bonas, U., 2010. Xanthomonas AvrBs3 family-type III effectors: Discovery
and function. Annual Review of Phytopathology 48, 419436.
Bruce, T.J.A., Wadhams, L.J., Woodcock, C.M., 2005. Insect host location: A volatile
situation. Trends in Plant Science 10, 13601385.
Brueggeman, R., Rostoks, N., Kudrna, D., et al., 2002. The barley stem rust
resistance gene Rpg1 is a novel disease-resistance gene with homology to
receptor kinases. Proceedings of the National Academy of Sciences of the USA
99, 93289333.
Castel, S.E., Martienssen, R.A., 2013. RNA interference in the nucleus: Roles for
small RNAs in transcription, epigenetics and beyond. Nature Reviews Genetics
14, 100112.
Century, K., Reuber, T.L., Ratcliffe, O.J., 2008. Regulating the regulators: The future
prospects for transcription-factor-based agricultural biotechnology products. Plant
Physiology 147, 2029.
Cessna, S.G., Sears, V.E., Dickman, M.B., Low, P.S., 2000. Oxalic acid, a
pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of
the host plant. Plant Cell 12, 21912200.
Chan, Y.L., Yang, A.H., Chen, J.T., Yeh, K.W., Chan, M.T., 2010. Heterologous
expression of taro cystatin protects transgenic tomato against Meloidogyne
incognita infection by means of interfering sex determination and suppressing
gall formation. Plant Cell Reports 29, 231238.
Chen, M., Shelton, A., Ye, G.-Y., 2011. Insect-resistant genetically modied rice in
China: From research to commercialization. Annual Review of Entomology 56,
81101.
Cheng, A.-X., Xiang, C.-Y., Li, J.-X., et al., 2007. The rice (E)-b-caryophyllene
synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes.
Phytochemistry 68, 16321641.
Chern, M., Fitzgerald, H.A., Canlas, P.E., Navarre, D.A., Ronald, P.C., 2005.
Overexpression of a rice NPR1 homolog leads to constitutive activation of
defense response and hypersensitivity to light. Molecular PlantMicrobe
Interactions 18, 511520.
Chinchilla, D., Shan, L., He, P., de Vries, S.C., Kemmerling, B., 2009. One
for all; the receptor-associated kinase BAK1. Trends in Plant Science 14,
535541.
Chinchilla, D., Zipfel, C., Robatzek, S., et al., 2007. A agellin-induced complex of
the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497500.
Chisholm, S.T., Coaker, G., Day, B., Staskawicz, B.J., 2006. Host-microbe
interactions: Shaping the evolution of the plant immune response. Cell 124,
803814.
Collinge, D.B., Jrgensen, H.J.L., Lund, O.S., Lyngkjr, M.F., 2010. Engineering
pathogen resistance in crop plants: Current trends and future prospects. Annual
Review of Phytopathology 48, 269291.
Conrath, U., Beckers, G.J.M., Flors, V., et al., 2006. Priming: Getting ready for
battle. Molecular PlantMicrobe Interactions 19, 10621071.
Consonni, C., Humphry, M.E., Hartmann, H.A., et al., 2006. Conserved requirement
for a plant host cell protein in powdery mildew pathogenesis. Nature Genetics
38, 716720.
Cools, H.J., Fraaije, B.A., 2008. Are azole fungicides losing ground against Septoria
wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest
Management Science 64, 681684.
Dangl, J.L., Horvath, D.M., Staskawicz, B.J., 2013. Pivoting the plant immune
system from dissection to deployment. Science 341, 746751.
De Lorenzo, G., DOvidio, R., Cervone, F., 2001. The role of polygalacturonaseinhibiting proteins (PGIPS) in defense against pathogenic fungi. Annual Review
of Phytopathology 39, 313335.
Deslandes, L., Rivas, S., 2012. Catch me if you can: Bacterial effectors and plant
targets. Trends in Plant Sciences 17, 644654.
Dixelius, C., Fagerstrm, T., Sundstrm, J.F., 2012. European agricultural policy
goes down the tubers. Nature Biotechnology 30, 492493.
Dodds, P.N., Rathjen, J.P., 2010. Plant immunity: Towards an integrated view of
plantpathogen interactions. Nature Reviews Genetics 11, 539548.
Dong, X., Ji, R., Guo, X., et al., 2008. Expressing a gene encoding wheat oxalate
oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica
napus). Planta 228, 331340.
Dong, Y.H., Wang, L.H., Xu, J.L., et al., 2001. Quenching quorum-sensing-dependent
bacterial infection by an N-acyl homoserine lactonase. Nature 411, 813817.
Dong, Y.-H., Zhang, L.-H., 2005. Quorum-sensing and quorum-quenching enzymes.
Journal of Microbiology 43, 101109.
Dong, Y.H., Zhang, X.F., Xu, J.L., Zhang, L.H., 2004. Insecticidal Bacillus
thuringiensis silences Erwinia carotovora virulence by a new form of microbial
antagonism, signal interference. Applied and Environmental Microbiology 70,
954960.
Duncan, L., Moens, M., 2006. Migratory endoparasitic nematodes. In: Perry, R.N.,
Moens, M. (Eds.), Plant Nematology. Wallingford, Oxfordshire: CABI Publishing,
pp. 123152.
Farnham, G., Baulcombe, D.C., 2006. Articial evolution extends the spectrum of
viruses that are targeted by a disease-resistance gene from potato. Proceedings
of the National Academy of Sciences of the USA 103, 1882818833.
Fisher, M.C., Henk, D.A., Briggs, C.J., et al., 2012. Emerging fungal threats to
animal, plant and ecosystem health. Nature 484, 186194.
Fuller, V.L., Lilley, C.J., Urwin, P.E., 2008. Nematode resistance. New Phytologist
180, 2744.
Gaj, T., Gersbach, C.A., Barbas III, C.F., 2013. ZFN, TALEN, and CRISPR/Cas-based
methods for genome engineering. Trends in Biotechnology 31, 397405.
Gao, S., Yu, B., Yuan, L., et al., 2011b. Production of transgenic sweet potato plants
resistant to stem nematodes using oryzacystatin-I gene. Scientia Horticulturae
128, 408414.
Gao, S., Yu, B., Zhai, H., He, S., Liu, Q., 2011a. Enhanced stem nematode
resistance of transgenic sweet potato plants expressing oryzacystatin-I gene.
Agricultural Sciences in China 10, 519525.
Gawehns, F., Cornelissen, B.J.C., Takken, F.L.W., 2013. The potential of effectortarget genes in breeding for plant innate immunity. Microbial Biotechnology 6,
223229.
Godfrey, D., Bhlenius, H., Pedersen, C., et al., 2010. Powdery mildew fungal
effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 11, 317.
Gomez-Ariza, J., Campo, S., Rufat, M., et al., 2007. Sucrose-mediated priming of
plant defense responses and broad-spectrum disease resistance by
overexpression of the maize pathogenesis-related PRms protein in rice plants.
Molecular PlantMicrobe Interactions 20, 832842.
Gurr, S.J., Rushton, P.J., 2005. Engineering plants with increased disease resistance:
What are we going to express? Trends in Biotechnology 23, 275282.
Gust, A.A., Brunner, F., Nrnberger, T., 2010. Biotechnological concepts for
improving plant innate immunity. Current Opinion in Biotechnology 21, 204210.
Hain, R., Reif, H.J., Krause, E., et al., 1993. Disease resistance results from foreign
phytoalexin expression in a novel plant. Nature 361, 153156.
Hammond-Kosack, K.E., Jones, J.D.G., 2000. Responses to plant pathogens. In:
Buchanan, B.B., Gruissem, W., Jones, R.L. (Eds.), Biochemistry and Molecular
Biology of Plants. Rockville, MD: American Society of Plant Physiology,
pp. 11021156.
Hammond-Kosack, K.E., Parker, J.E., 2003. Deciphering plant-pathogen
communication: Fresh perspectives for molecular resistance breeding. Current
Opinions in Biotechnology 14, 177193.
151
Hogenhout, S.A., Van der Hoorn, R.A.L., Terauchi, R., Kamoun, S., 2009. Emerging
concepts in effector biology of plant-associated organisms. Molecular Plant
Microbe Interactions 22, 115122.
van der Hoorn, R.A.L., Kamoun, S., 2008. From guard to decoy: A new model for
perception of plant pathogen effectors. Plant Cell 20, 20092017.
Horvath, H., Rostoks, N., Brueggeman, R., et al., 2003. Genetically engineered stem
rust resistance in barley using the Rpg1 gene. Proceedings of the National
Academy of Sciences of the USA 100, 364369.
Hu, H., Xiong, L., Yang, Y., 2005. Rice SERK1 gene positively regulates somatic
embryogenesis of cultured cell and host defense response against fungal
infection. Planta 222, 107117.
Huang, G., Allen, R., Davis, E.L., Baum, T.J., Hussey, R.S., 2006. Engineering broad
root-knot resistance in transgenic plants by RNAi silencing of a conserved and
essential root-knot nematode parasitism gene. Proceedings of the National
Academy of Sciences of the USA 103, 1430214306.
Huibers, R.P., Loonen, A.E.H.M., Gao, D., et al., 2013. Powdery mildew resistance
in tomato by impairment of SlPMR4 and SlDMR1. PLoS One. e0067467.
Jinek, M., East, A., Cheng, A., et al., 2013. RNA programmed genome editing in
human cells. eLife 2, e00471.
Jones, J.D.G., Dangl, J.L., 2006. The plant immune system. Nature 444, 323329.
Jones, J.D.G., Witek, K., Verweij, W., et al., 2014. Elevating crop disease resistance
with cloned genes. Philosophical Transactions of the Royal Society B Series 369.
doi:10.1098/rstb.2013.0087.
Kale, S.D., Gu, B., Capelluto, D.G., et al., 2010. External lipid PI3P mediates entry
of eukaryotic pathogen effectors into plant and animal host cells. Cell 142,
284295.
Koch, A., Kumara, N., Weber, L., et al., 2013. Host-induced gene silencing of
cytochrome P450 lanosterol C14-demethylaseencoding genes confers strong
resistance to Fusarium species. Proceedings of the National Academy of Science
of the USA 110, 1932419329.
Kllner, T.G., Held, M., Lenk, C., et al., 2008. A maize (E)--caryophyllene synthase
implicated in indirect defense responses against herbivores is not expressed in
most American maize varieties. Plant Cell 2, 482494.
Krattinger, S.G., Lagudah, E.S., Spielmeyer, W., et al., 2009. A putative ABC
transporter confers durable resistance to multiple fungal pathogens in wheat.
Science 323, 13601363.
Lacombe, S., Rougon-Cardoso, A., Sherwood, E., et al., 2010. Interfamily transfer of
a plant pattern-recognition receptor confers broad-spectrum bacterial resistance.
Nature Biotechnology 28, 365369.
Leadbeater, A., 2011. The impact of the new European regulations on the
management of crop diseases. In: Dehne, H.W., Deising, H.B., Gisi, U., Kuck, K.
H., Russell, P.E., Lyr, H. (Eds.), DPG Spectrum Phytomedizin. Modern
Fungicides and Antifungal Compounds VI. Braunschweig: Deutsche
Phytomedizinische Gesellschaft, pp. 110.
Lee, W.-S., Hammond-Kosack, K.E., Kanyuka, K., 2012. Barley stripe mosaic virusmediated tools for investigating gene function in cereal plants and their
pathogens: VIGS, HIGS and VOX. Plant Physiology 160, 582590.
Lee, W.-S., Rudd, J.J., Hammond-Kosack, K.E., Kanyuka, K.K., 2014.
Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts
recognition through both CERK1 and CEBiP homologues in wheat. Molecular
PlantMicrobe Interactions 27, 236243.
Lewis, J.D., Wan, J., Ford, R., et al., 2012. Quantitative interactor screening with
next-generation sequencing (QIS-Seq) identies Arabidopsis thaliana MLO2 as a
target of the Pseudomonas syringae type III effector HopZ2. BMC Genomics 13, 8.
Li, D., Wang, L., Wang, M., et al., 2009. Engineering OsBAK1 gene as a molecular
tool to improve rice architecture for high yield. Plant Biotechnology Journal 7,
791806.
Li, H.-P., Zhang, J.-B., Shi, R.-P., et al., 2008. Engineering fusarium head blight
resistance in wheat by expression of a fusion protein containing a Fusariumspecic antibody and an antifungal peptide. Molecular PlantMicrobe
Interactions 21, 12421248.
Lilley, C.J., Wang, D., Atkinson, H.J., Urwin, P.E., 2011. Effective delivery of a
nematode-repellent peptide using a root-cap-specic promoter. Plant
Biotechnology Journal 9, 151161.
Li, T., Liu, B., Spalding, M.H., Weeks, D.P., Yang, B., 2012. High-efciency TALENbased gene editing produces disease-resistant rice. Nature Biotechnology 30,
390392.
Makandar, R., Essig, J.S., Schapaugh, M.A., Trick, H.N., Shah, J., 2006. Genetically
engineered resistance to Fusarium head blight in wheat by expression of
Arabidopsis NPR1. Molecular PlantMicrobe Interactions 19, 123129.
Mao, Y.-B., Cai, W.-J., Wang, J.-W., et al., 2007. Silencing a cotton bollworm P450
monooxygenase gene by plant-mediated RNAi impairs larval tolerance of
gossypol. Nature Biotechnology 25, 13071313.
152
Marcos, J.F., Munoz, A., Perez-Paya, E., Misra, S., Lopez-Garcia, B., 2008.
Identication and rational design of novel antimicrobial peptides for plant
protection. Annual Review of Phytopathology 46, 273301.
Mirlohi, A., Brueggeman, R., Drader, T., et al., 2008. Allele sequencing of the barley
stem rust resistance gene Rpg1 identies regions relevant to disease resistance.
Phytopathology 98, 910918.
Narasimhan, M., Bressan, R., Paino dUurzo, M., Jenkins, M., Mengiste, T., 2009.
Unexpected turns and twists in structure/function of PR-proteins that connect
energy metabolism and immunity. In: van Loon, L.C. (Ed.), Advances in
Botanical Research: Plant Innate Immunity. Amsterdam: Elsevier, pp. 474491.
Narusaka, M., Kubo, Y., Hatakeyama, K., et al., 2013. Interfamily transfer of dual
NB-LRR genes confers resistance to multiple pathogens. PLoS One 8, e55954.
Nombela, G., Williamson, V.M., Muiz, M., 2003. The root-knot nematode resistance
gene Mi-1.2 of tomato is responsible for resistance against the whitey Bemisia
tabaci. Molecular PlantMicrobe Interactions 16, 645649.
Nowara, D., Gaya, A., Lacombe, C., et al., 2010. Host-induced gene silencing in the
obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22, 31303141.
Oerke, E.-C., 2006. Crop losses to pests. Journal of Agricultural Science 144, 3143.
Oliva, R., Segretin, M.E., Rietman, H., et al., 2011. Understanding and exploiting late
blight resistance in the age of effectors. Annual Review of Phytopathology 49,
507531.
Oliver, R.P., Solomon, P.S., 2010. New developments in pathogenicity and virulence
of necrotrophs. Current Opinion in Plant Biology 13, 415419.
Panwar, V., McCallum, B., Bakkeren, G., 2013a. Endogenous silencing of Puccinia
triticina pathogenicity genes through in planta-expressed sequences leads to the
suppression of rust diseases on wheat. Plant Journal 73, 521532.
Panwar, V., McCallum, B., Bakkeren, G., 2013b. Host-induced gene silencing of
wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the
Barley stripe mosaic virus. Plant Molecular Biology 81, 595608.
Pavan, S., Jacobsen, E., Visser, R.G.F., Bai, Y., 2010. Loss of susceptibility as a
novel breeding strategy for durable and broad-spectrum resistance. Molecular
Breeding 25, 112.
Pickett, J., Aradottr, G., Birkett, M., et al., 2014. Delivering sustainable crop
protection systems via the seed: Exploiting natural constitutive and inducible
defence pathways. Philosophical Transactions of the Royal Society. 369.
doi:10.1098/rstb.2012.0281.
Rahnamaeian, M., Langen, G., Imani, J., et al., 2009. Insect peptide metchnikowin
confers on barley a selective capacity for resistance to fungal ascomycetes
pathogens. Journal of Experimental Botany 60, 41054114.
Raeffaele, S., Kamoun, S., 2012. Genome evolution in lamentous plant pathogens:
Why bigger can be better. Nature Review Microbiology 10, 417430.
Ravensdale, M., Bernoux, M., Ve, T., et al., 2012. Intramolecular interaction
inuences binding of the Flax L5 and L6 resistance proteins to their AvrL567
ligands. PLoS Pathogens 8, e1003004.
Ravensdale, M., Nemri, A., Thrall, P.H., Ellis, J.G., Dodds, P.N., 2011. Coevolutionary interactions between host resistance and pathogen effector genes in
ax rust disease. Molecular Plant Pathology 12, 93102.
Reymond, P., Weber, H., Damond, M., Farmer, E.E., 2000. Differential gene
expression in response to mechanical wounding and insect feeding in
Arabidopsis. Plant Cell 12, 707719.
Roderick, H., Tripathy, L., Babirey, A., et al., 2012. Generation of transgenic plantain
(Musa spp.) with resistance to plant pathogenic nematodes. Molecular Plant
Pathology 13, 842851.
Rushton, P.R., Reinstdler, A., Lipka, V., Lippok, B., Somssich, I.E., 2002. Synthetic
plant promoters containing dened regulatory elements provide novel insights
into pathogen- and wound-induced signalling. Plant Cell 14, 749762.
Saintenac, C., Zhang, W., Salcedo, A., et al., 2013. Identication of wheat gene Sr35
that confers resistance to Ug99 stem rust race group. Science 341, 783786.
Safarnejad, M.R., Jouzani, G.S., Tabatabaie, M., Twyman, R.M., Schillberg, S., 2011.
Antibody-mediated resistance against plant pathogens. Biotechnology Advances
29, 961971.
Schilmiller, A.L., Howe, G.A., 2005. Systemic signaling in the wound response.
Current Opinion in Plant Biology 8, 369377.
Schnee, C., Kllner, T.G., Held, M., et al., 2006. The products of a single maize
sesquiterpene synthase form a volatile defense signal that attracts natural
enemies of maize herbivores. Proceedings of the National Academy of Sciences
of the USA 103, 11291134.
Schornack, S., Moscou, M.J., Ward, E.R., Horvath, D.M., 2013. Engineering plant
disease resistance based on TAL effectors. Annual Review of Phytopathology 51,
383406.
Shah, D.M., Rommens, C.M.T., Beachy, R.N., 1995. Resistance to diseases and
insects in transgenic plants: Progress and applications to agriculture. Trends in
Biotechnology 13, 362368.
Shin, S., Mackintosh, C.A., Lewis, J., et al., 2008. Transgenic wheat expressing a
barley class II chitinase gene has enhanced resistance against Fusarium
graminearum. Journal of Experimental Botany 59, 23712378.
Song, J., Bradeen, J.M., Naess, S.K., et al., 2003. Gene RB cloned from Solanum
bulbocastanum confers broad spectrum resistance to potato late blight.
Proceedings of the National Academy of Sciences of the USA 100, 91289133.
Spoel, S.H., Dong, X., 2008. Making sense of hormone crosstalk during plant
immune responses. Cell Host & Microbe 3, 348351.
Spoel, S.H., Dong, X., 2012. How do plants achieve immunity? Defence without
specialized immune cells. Nature Reviews Immunology 12, 89100.
Strange, R.N., Scott, P.R., 2005. Plant disease: A threat to global food security.
Annual Review of Phytopathology 43, 83116.
Stuiver, M.H., Custers, J.H.H.V., 2001. Engineering disease resistance in plants.
Nature 411, 865868.
Tabashnik, B.E., Brvault, T., Carrire, Y., 2013. Insect resistance to Bt crops:
Lessons from the rst billion acres. Nature Biotechnology 31, 510521.
The International Aphid Genomics Consortium, 2010. Genome sequence of the pea
aphid Acyrthosiphon pisum. PLoS Biology 8, e1000313.
Thomzik, J.E., Stenzel, K., Stcker, R., et al., 1997. Synthesis of a grapevine
phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions
resistance against Phytophthora infestans. Physiological and Molecular Plant
Pathology 51, 265278.
Tonukaria, N.J., Scott-Craig, J.S., Walton, J.D., 2000. The Cochliobolus carbonum
SNF1 gene is required for cell walldegrading enzyme expression and virulence
on maize. Plant Cell 12, 237247.
Tyler, B.M., 2009. Entering and breaking: Virulence effector proteins of oomycete
plant pathogens. Cellular Microbiology 11, 1320.
Tyler, B.M., Kale, S.D., Antignani, V., et al., 2011. How oomycete and fungal
effectors enter plant and animal cells. In 26th Fungal Genetics Conference.
Fungal Genetics Reports, vol. 58 (Suppl.). pp. 41. Asilomar, CA, USA: Genetics
Society of America.
Vaeck, M., Reynaerts, A., Hfte, H., et al., 1987. Transgenic plants protected from
insect attack. Nature 328, 3337.
Valent, B., Khang, C.H., 2010. Recent advances in rice blast effector research.
Current Opinion in Plant Biology 13, 434441.
Ve, T., Williams, S.J., Catanzariti, A.M., et al., 2013. Structures of the ax-rust
effector AvrM reveal insights into the molecular basis of plant-cell entry and
effector-triggered immunity. Proceedings of the National Academy of Sciences of
USA 110, 1759417599.
Wang, W., Wen, Y., Berkey, R., Xiao, S., 2009. Specic targeting of the Arabidopsis
resistance protein RPW8.2 to the interfacial membrane encasing the fungal
haustorium renders broad-spectrum resistance to Powdery Mildew. Plant Cell 21,
28982913.
Winter, M.D., McPherson, M.J., Atkinson, H.J., 2002. Neuronal uptake of pesticides
disrupts chemosensory cells of nematodes. Parasitology 125, 561565.
de Wit, P.J.G.M., Mehrabi, R., van den Burg, H.A., Stergiopoulos, I., 2009. Fungal
effector proteins: past, present and future. Molecular Plant Pathology 10, 735747.
Yamamizo, C., Kuchimura, K., Kobayashi, A., et al., 2006. Rewiring mitogenactivated protein kinase cascade by positive feedback confers potato blight
resistance. Plant Physiology 140, 681692.
Zipfel, C., Robatzek, S., 2010. Pathogen-associated molecular pattern triggered
immunity: Veni, vidi. Plant Physiology 154, 551554.
Relevant Websites
http://passport.snu.ac.kr/?t=FSD
Bioinformatic Portal System.
http://www.bcpc.org
British Crop Production Council.
http://plants.ensembl.org
EnsemblPlants.
http://arthropodgenomes.org/wiki/Resources
Insect genome database.
http://niblrrs.ucdavis.edu/
NIBLRRS.
http://www.phi-base.org/
PathogenHost Interactions database (PHI-base).
http://www.phytopathdb.org/
PhytoPathdb.
http://prgdb.crg.eu/wiki/Main_Page
Plant Disease Resistance Gene-Wiki.
Introduction
Biotechnology is an excellent, contemporary technological
tool complementary to the currently established genetic improvement technologies such as selection, plant breeding, and
mutational genetics. Choosing biotechnology provides an
important tool for improving food productivity, quality, reducing input costs and it supports sustainable production.
Development of biotech crops (or genetically modied crops)
for agronomic improvements, reduced pesticides, disease tolerance, postharvest preservation, and improved nutritional
quality is one of the selected applications of biotechnology in
the agriculture and food sector. With the advent of molecular
biology and biotechnology, it became possible not only to
identify a desirable phenotypic trait but also to identify the
precise genetic material responsible for that genetic trait. Recombinant deoxyribonucleic acid (rDNA) and plant transformation techniques have made it possible to alter the
composition of individual plant components such as lipids,
carbohydrates, and proteins beyond what is possible through
traditional breeding practices. More than 16.7 million farmers
around the world use agricultural biotechnology to increase
yields, prevent damage from insects and pests, and to reduce
farming's impact on the environment. Biotechnology improves
crop insect resistance, enhances crop herbicide tolerance, and
facilitates the use of more environmentally sustainable farming practices. Biotechnology is also helping to feed the world
by (1) generating higher crop yields with fewer inputs,
(2) lowering volumes of agricultural chemicals required by
crops limiting the run-off of these products into the environment, (3) using biotech crops that need fewer applications of pesticides and that allow farmers to reduce tilling
farmland, (4) developing crops with enhanced nutrition proles that solve vitamin and nutrient deciencies, (5) producing
foods free of allergens and toxins such as mycotoxin, and
(6) improving food and crop oil content to help improve
cardiovascular health (BIO, 2011; Phipps and Park, 2002;
Mackey and Fuchs, 2001).
Plant biotechnology has been adopted at a higher rate than
any other agricultural practice in history. Since 1996, when the
rst commercial biotech crops were planted, biotechnology
has become the fastest technique ever adopted in agriculture.
In 2011, the global area of biotech crops increased by approximately 8% from 2010 to reach 160 million hectares, up
from 148 million hectares in 2010 as shown in Figure 1. This
is a 94-fold-hectare increase since 1996. In its annual study,
the International Service for the Acquisition of Agri-Biotech
Applications (ISAAA) found that in 2011, 16.7 million farmers
in a record 29 countries planted biotech crops, an increase of
1.3 million from the previous year. Approximately 90% of the
farmers were small-scale and resource-poor farmers from developing countries. Indeed, biotech crops are helping farmers
to be more productive and protable. Biotech crop hectares
continue to climb after 15 consecutive years of strong growth,
as global population soars to 7 billion. The crops also contribute to a greener environment (James, 2011).
Despite the various benets of biotech crops, the use of
modern biotechnology has become a highly controversial
issue in some regions where it has been applied. It has polarized modern society in terms of the potential benets and
risks of the adoption of crop biotechnologies and derived
products in food and agriculture systems. The terminology for
the application of biotechnology to food and agriculture has
been used in various forms, such as genetic modication
(GM), genetic engineering (GE), genetic manipulation, gene
technology, and rDNA technology. However, the collective
term genetically modied organisms (GMOs) is used frequently in regulatory documents and in scientic literature to
describe the deliberate introduction of DNA by human intervention into plants, animals, and microorganisms (IFST,
2008). This article covers only the safety and regulatory issues
related to plant products derived by modern biotechnology,
called biotech crops or genetically modied plants, not for
animal products or other organisms.
doi:10.1016/B978-0-444-52512-3.00229-1
153
154
180
Total hectares
160
Industrial
Developing
140
120
100
80
60
40
20
0
1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006
A record 16.7 million farmers, in 29 countries, planted 160 million hectares (395 million acres) in
2011, a sustained increase of 8% or 12 million hectares (30 million acres) over 2010.
Figure 1 Global area of biotech crops. Reproduced from James, C., 2011. Global Status of Commercialized Biotech/GM Crops: 2011 ISAAA Briefs
No. 43.
100
90
80
HT Soybeans
70
60
HT Cotton
50
Bt Cotton
40
Bt Corn
30
HT Corn
20
10
0
1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Figure 2 Adoption of biotech crops in the United States Data for each crop category includes stacked events. Reproduced from ERS, USDA,
2012.
155
100
90
Bt only
80
Stacked (Bt and HT)
Planted acres (%)
70
HT only
60
50
40
30
20
10
0
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
Figure 3 Adoption of biotech cotton in the United States. BT, bacillus thuringiensis and HT, herbicide-tolerant. Reproduced from ERS, USDA (2012).
180
160
Million hectares
140
159
Conventional
GM
120
100
100
80
60
40
30
31
20
0
82%
Cotton
75%
Soybean
32%
Maize
26%
Candle
Figure 4 Global adoption rates for principal biotech crops. Reproduced from Clive James, ISAAA (2012).
Global adoption of biotech crops also has become widespread despite the controversy about efcacy and safety in
some countries in the region. According to the ISAAA, global
planting acreage of biotech crops has increased so that biotech
crops covered 160 million hectares and planted by 15.4 million farmers in 29 countries in 2011 (Figure 1).
156
Table 1
Crop
Bt protein
Event name
Target pests
Corn
Cry1Ab
Cry1F
Cry1A.105 Cry2Ab2
Vip3Aa20
mCry3a
Cry34Ab1/Cry35Ab1
Cry3Bb1
Cotton
Cry1F
Cry1Ac
Cry1Ac Cry2Ab2
281-24-236 (Dow)
3006-210-23 (Dow)
MON 15985 (Monsanto)
Lepidopteran pests
Lepidopteran pests
Lepidopteran pests
Bt proteins in stacked event, which were developed by conventional crossing of the events listed above, are not listed in this table. Breeding stacks express the transgenes inherited
from parental lines.
Source: Reproduced from CropLife International, 2012a. Labeling of Biotech-Derived Products; CropLife International, 2012b. Plant Biotechnology Pipeline. Available at: http://www.
croplife.org/view_document.aspx?docId=3631 (accessed 27.08.12).
tolerance weeds in farmlands has been more frequently reported than before, may be due to the intense use of a specic
herbicide in biotech crop elds during the last decade. Emergence of herbicide-tolerant weeds and potential development of
Bt-resistant insect pests have encouraged developers to continue
developing new Bt genes and HT genes (Table 2). For example,
a soybean event expressing Cry1Ac to control lepidopteran pests
of soybean is at its late stage of global regulatory approvals
before commercialization. Additional herbicide tolerance traits
such as the tolerance to 2-, 4-D, and dicamba are also under
regulatory pipelines. New molecular mechanisms to control
insect pests are under development, such as RNA interference,
which provides a mode of action different from Bt proteins.
In addition to Bt and HT traits, other traits are also gaining
increasing importance because of market needs. For example, a
high-oleic acid soybean is in its early stage of market launch in
the US; some other crops are in the regulatory pipeline or are
in the late stages of product development, awaiting their optimized composition (Table 2). Developing biotech events
conferring tolerance to abiotic stress such as drought has been
one of the hot topics for key developers in the world. One such
product, a drought-tolerant biotech corn, is almost ready to be
launched in the market in the Americas.
As of today, most of the biotech crops currently on the
market have come from key players located in the US and the
European Union (EU). However, it is expected that many new
biotech events could be brought to market by developers in
other countries in the near future, including India, China, and
Latin American countries (Stein and Rodrguez-Cerezo, 2010).
In terms of crop types, application of agbiotech is increasing so
that more diverse biotech crops are anticipated to appear on
the market in the future (Figure 4), such as potato, rice,
sugarcane, wheat, and some vegetables (Figure 5). Another
phenomenon that will be observed after 2014 is the potential
of generics of biotech events, as the early patents on biotech
crops expire (Gruskin, 2012).
Table 2
157
Crop
Early development
Corn
Herbicide tolerance
Dicamba & Glufosinate (Monsanto)
FOPS (Monsanto)
Multiple mode (DuPont Pioneer)
Insect resistance
Corn borer III (Monsanto)
New modes of action coleopteran III (DuPont
Pioneer)
New modes of action lepidopteran III (DuPont
Pioneer)
Second generation corn rootworm (Syngenta)
Novel insect traits (Syngenta)
Nitrogen utilization
(Monsanto, BASF)
(DuPont Pioneer)
(Syngenta)
Stress tolerance
Drought tolerance II (DuPont Pioneer)
Second
generation
drought
tolerance
(Monsanto, BASF)
Crop composition
Improved corn feed (BASF)
Increased ethanol (Syngenta)
Insect resistance
Hemiptera/stink bug (DuPont Pioneer)
Lepidopteran (DuPont Pioneer)
Nematode resistance
Soybean cyst nematode (Syngenta)
Soybean cyst nematode (BASF, Monsanto)
Disease resistance
Asian soybean rust II (DuPont Pioneer)
(Syngenta)
Fungal resistance
(BASF)
Increased yield
Second generation (Monsanto, BASF)
Crop composition
Increased oil and improved feed efciency (DuPont
Pioneer)
Insect resistance
Lygus Control (Monsanto)
Stress tolerance
Drought tolerance (Monsanto, BASF)
Herbicide tolerance
Roundups hybridization system (Monsanto)
DHT: 2,4-D & FOP (Dow AgroSciences)
Insect resistance
Corn rootworm III (Monsanto)
Optimums Intrasect insect protection Agrisure Viptera (DuPont Pioneer)
Lepidopteran/Coleopteran DP 4114 (DuPont Pioneer)
Integrated corn rootworm & European corn borer refuge
Optimums AcreMax XTreme Insect Protection (DuPont Pioneer)
Stress tolerance
Drought (Syngenta)
First generation drought tolerance (Monsanto, BASF)
Increased yield
(Monsanto, BASF)
Soybean
Cotton
Canola
Rice
Herbicide tolerance
Dicamba (Monsanto)
Multiple mode (DuPont Pioneer)
Hydroxyphenylpyruvate deoxygenase (HPPD) inhibitors (Syngenta, Bayer
CropScience)
DHT: 2,4-D & FOP (Dow AgroSciences)
GlyTols HPPD LibertyLinks (Bayer CropScience, M.S.Technologies)
Imidazolinone (BASF, Embrapa/Brazil)
Insect resistance
Second generation insect-Protected (Monsanto)
Intacta RR2 PROs (Monsanto)
Increased yield
First generation (Monsanto, BASF)
Crop composition
Soymega SDA omega-3 (Monsanto-Solae)
Low saturated, zero trans-fat oil (Monsanto)
Herbicide tolerance
Dicamba and Glufosinate (Monsanto)
DHT (Dow AgroSciences)
Insect resistance/herbicide tolerance
GlyTols LibertyLinks TwinLink (Bayer CropScience)
Next generation IR GlyTols LibertyLinks (Bayer CropScience)
Insect resistance
Genuitys Bollgard III (Monsanto)
Herbicide tolerance
Herbicide tolerance
Dicamba tolerance (Monsanto)
Next-generation Genuitys Roundup Readys (Monsanto)
Increased yield
Glyphosate tolerance DP 73496 (DuPont Pioneer)
First generation (Monsanto, BASF)
LibertyLinks tolerance (DuPont Pioneer)
Crop composition
Glyphosate tolerance LibertyLinks tolerance (Bayer CropScience)
Healthy fatty acids (BASF)
Next-generation Genuitys Roundup Readys LibertyLinks (Bayer CropScience,
Oil quality (Bayer CropScience)
Monsanto)
Herbicide tolerance
Herbicide tolerance
(DuPont Pioneer)
LibertyLinks tolerance (Bayer CropScience)
Insect resistance
Crop composition
Dual Mode of Action Lepidopteran (DuPont Pioneer) Beta-carotene content increased Golden rice 1 (IRRI/Philippines)
(Bayer CropScience)
Beta-carotene content increased Golden rice 2 (IRRI/Philippines)
(Continued )
158
Table 2
Crop
Other
crops
Continued
Early development
Increased yield
(BASF, Bayer CropScience)
Alfalfa
Increased yield (Monsanto, Forage Genetics
International)
Sugar beet
Increased yield (BASF, KWS)
Sugarcane
Insect resistance Roundup Readys (Monsanto)
Increased yield (BASF, CTC)
Wheat
Herbicide tolerance (Monsanto)
Increased yield (BASF, Monsanto)
Alfalfa
Reduced lignin (Monsanto, Forage Genetics International)
Beans
Geminivirus resistance (Embrapa/Brazil)
Eggplant
Insect resistance Bt Brinjal (Maharashtra Hybrid Seeds Company)
Potatoes
Potato virus Y resistance (Tecnoplant/Argentina)
Late blight resistance (BASF)a
High amylopectin (BASF, Avebe)a
High amylopectin (BASF)a
27
24
Soybeans
Rapeseed
Rice
Other
Maize
Cotton
Potatoes
21
18
15
12
9
6
3
0
2008
2009
2010
2011
2012
2013
2014
2015
Figure 5 Projected number of events in biotech crops worldwide, by crop. Reproduced from Stein, A.J., Rodriguez-Cerezo, E., 2009. The global
pipeline of new GM crops: Implications of asynchronous approval for international trade. Technical Report EUR 23486 EN. Luxemburg: European
Communities.
Table 3
159
Some key international consultations addressing the safety assessment of biotech (B2006)
Year
Organization
Title
1986
1993
1994
WHO
1996
1996
1990
1990
1997
2000
2000
2001
2001
CAC
2002
2002
OECD
CAC
2002
WHO
2003
CAC
2003
OECD
2006
Strategies for assessing the safety of foods produced by biotechnology, a joint FAO/WHO
consultation. Geneva, Switzerland, 510 November 1990
Biotechnologies and food: assuring the safety of foods produced by genetic modication.
Regulatory Toxicology and Pharmacology, 12, S1S196
Health aspects of marker genes in genetically modied plants. Report of a WHO
Workshop. Copenhagen, Denmark, 2124 September 1993
Application of the principles of substantial equivalence to the safety evaluation of foods or
food components from plants derived by modern biotechnology. Report of a WHO
Workshop, Copenhagen, Denmark, 31 October4 November 1994
Biotechnology and food safety. Report of a Joint FAO/WHO Consultation, Rome, Italy, 30
September4 October 1996. FAO Food and Nutrition Paper No. 61
ILSI Allergy and Immunology Institute (AII) guidance for assessing the allergenic potential
of foods derived from biotechnology
Report of the OECD workshop on the toxicological and nutritional testing of novel foods
Report of a Joint FAO/WHO Expert Consultation on foods derived from biotechnology
Safety aspects of genetically modied foods of plant origin. WHO Headquarters, Geneva,
Switzerland, 29 May2 June 2000
First session of the Codex ad hoc Intergovernmental Task Force on foods derived from
biotechnology. Chiba, Japan, March 2000
Allergenicity of genetically modied foods, a joint FAO/WHO consultation on foods derived
from biotechnology. Rome, Italy, 2225 January 2001
Second session of the Codex ad hoc Intergovernmental Task Force on Foods Derived from
Biotechnology. Chiba, Japan, March 2001
Report of the OECD Workshop on the nutritional assessment of novel foods and feeds
Third session of the Codex ad hoc Intergovernmental Task Force on Foods Derived from
Biotechnology. Yokohama, Japan, March 2002
The stakeholders' meeting on WHO draft document WHO Modern food biotechnology,
human health and development: an evidence-based study. WHO, Geneva
Fourth session of the Codex ad hoc Intergovernmental Task Force on Foods Derived from
Biotechnology. Yokohama, Japan, March 2003
Report on the questionnaire on biomarkers, research on the safety of novel foods, and
feasibility of postmarket monitoring
FAO expert consultation on biosafety within a biosecurity framework: Contributing to
sustainable agriculture and food production. 28 February3 March 2006, Rome, Italy
Source: Reproduced from FAO, 2008. GM Food Safety Assessment Tool for Trainers. Rome: Food & Agriculture Organization of the United Nations.
160
Risk communication
Risk
characterization
Hazard
characterization
Risk
evaluation
Exposure
assessment
Option
assessment
Option
implementation
Risk management
Risk assessment
Hazard
identification
Monitoring
and review
Consumers,
industry, and other
interest parties
Figure 6 Risk analysis framework for the safety assessment of foods derived from biotech crops. Reproduced from FAO, 2008. GM Food Safety
Assessment Tool for Trainers. Rome: Food & Agriculture Organization of the United Nations.
161
Donor organism
Parent crop
History of use
origin, habitat
characteristics
Modification process
Hazard
Identification
Comparative analysis of GM plants and derived food and feed and conventional
counterpart(s)
Molecular, compositional, phenotypical, and agronomical analyses
Hazard characterization
Intended differences
New gene product(s)
Compositional alterations
In case of multiple
compositional
changes
Unintended differences?
Agronomical and
compositional alterations
Exposure assessment
Risk characterization
Conclusion on safety
Figure 7 Scheme for premarket safety and nutritional testing of biotech plant-derived food and feed. Reproduced from EFSA GMO Panel Working
Group on Animal Feeding Trials, 2008. Safety and nutritional assessment of GM plants and derived food and feed: The role of animal feeding trials.
Food and Chemical Toxicology 46 (Suppl. 1), S2S70.
162
Feedback
(2) Hazard
characterization
(3) Exposure
characterization
coordination of all food standards work undertaken by international governmental and nongovernmental organizations.
The Codex's objectives include consideration of standards,
guidelines, or other recommendations as appropriate for foods
derived from biotechnology or traits introduced into foods by
biotechnology on the basis of scientic evidence and risk analysis. Codex developed principles for the human health risk
analysis of GM foods. The principles include a science-based,
premarket risk assessment performed on a case-by-case basis,
and also an evaluation of both direct effects from the inserted
gene and unintended effects that may arise as a consequence of
insertion of the new gene. The standards set out by the Codex
have been used widely as the benchmark in international trade
disputes. Three standards relating to GM crops are (1) principles for the risk analysis of foods derived from modern
biotechnology (FAO/WHO Codex Alimentarius, 2003a,b),
(2) guidelines for the conduct of food safety assessment
of foods derived from rDNA plants (FAO/WHO Codex
Alimentarius, 2003a,b), and (3) working principles for risk
analysis for food safety for application by governments
(FAO/WHO, 2007).
163
Problem formulation
Conceptual model
(Predicted environmental
relationships and risk
hypotheses related to
assessment endpoints)
Assessment endpoints
(Valued entities that need
to be protected, and are
operationally defined)
Analysis plan
(Experimental plan to collect relevant data
including measures of exposure and effects)
Hazard
identification and
assessment
(effects testing or
consequences
assessment)
Exposure
assessment
(levels and
likelihood of
exposure)
Risk
characterization
Figure 9 Schematic of problem formulation in the context of the risk assessment process as proposed by the US Environmental Protection
Agency. Reproduced from Nickson, T.E., 2008. Planning environmental risk assessment for genetically modied crops: Problem formulation for
stress-tolerant crops. Plant Physiology 147 (2), 494502.
in 1986 called the Blue Book because its cover is blue. This
guidance book identied that the specic aims of rDNA techniques in agriculture are, to reduce vulnerability to environmental stress: to detect and control infectious agents in animals
and in the eld and postharvest; to reduce dependence on use
patterns of chemical pesticides; to decrease dependence on
chemical fertilizers and irrigation; and to increase the nutritional
qualities of seed, fruits, grains, and vegetables. The book also
says that rDNA techniques represent a development of conventional procedures. They permit precise alteration, construction, recombination, deletion and translocation of genes
that may give the recipient cells a desirable phenotype. Moreover, rDNA techniques allow genetic material to be transferred
into, and to express in, another organism which may be quite
unrated to the source of the transferred DNA (OECD, 1986).
The book has been used as a starting point for countries that
need to set up their own biosafety regulation on GM crops.
Producing the consensus documents on environmental and
food/feed biosafety is one of the OECD's main activities done by
the Working Group on the harmonization of regulatory oversight in biotechnology. The objectives of the OECD's working
group are (1) to protect the environment, (2) to promote harmonization, while (3) reducing unnecessary barriers to trade.
Working group focuses on the safety assessment of GM crops by
the development of consensus documents, information dissemination via BioTrack Online, and facilitating regulatory harmonization. Food/feed consensus documents on new crop
164
foods are not yet regulated. Countries where they have legislation in place focus primarily on assessment of risks for
consumer health. Countries that have provisions for GM foods
usually also regulate GMOs in general, taking into account
health and environmental risks, as well as control trade-related
issues such as potential testing and labeling systems. The GMO
regulatory systems that countries apply depend on the existing
national legislation, their legal systems, and the administrative
systems that are in place. UNEP-GEFs (United Nations Environment Program-Global Environment Facility) National
Biosafety Framework (NBF) project has been helping underdeveloped and developing countries to establish biosafety
regulations and a regulatory framework since early 2000. As of
May 2012, a total of 118 countries have completed the majority of development of their NBFs. Their drafts of the NBFs
are available online at UNEP (2008, 2012). Immediately after
the Asilomar conference, many countries introduced some
form of GMO regulation intended to ensure the safe use of the
technology. In the USA, for instance, the National Institutes of
Health (NIH) produced guidelines that applied to all organizations receiving funding from the USA government (NIH,
2002). These NIH guidelines remain the primary regulatory
system for assuring safety in the USA regarding transgenic organisms in containment. For the agricultural use of commercially released GMOs, the US government deliberately
chose to use existing agencies and not to change any laws. The
US Ofce of Science and Technology Policy Committee generated the Coordinated Framework for the regulation of biotechnology in 1986 to guide framework for GM regulation (US
Department of State, 1999). The USDA works with the Environment Protection Agency (EPA) and the Food and Drug
Administration (FDA) to regulate the use of GMOs.
that foods from plants produced through modern biotechnology are as safe as those from plants developed through
conventional breeding. Therefore, GM foods should be regulated the same as any other foods entering the market. Accordingly, the FDA evaluates the application of biotechnology
to food products on a case-by-case basis, as it does with any
other food. Under the Food, Drug and Cosmetic Act, the FDA
usually focuses on the products, the food, or food ingredients,
rather than on the plant development processes used in their
production, as the basis for regulation. The same holds true for
food and ingredients derived through biotechnology. The FDA
offers a series of testing procedures that enable food manufacturers to anticipate safety concerns and to consult with the
FDA as necessary for a regulatory review of new plant varieties
and products testing under development. The FDA review
process focuses on the areas, such as (1) safety and nutritional
value of the newly introduced proteins, (2) identity, composition, and nutritional value of modied carbohydrates,
fats, or oils, (3) concentration and bioavailability of nutrients
for which the food crop is consumed, and (4) potential for
allergens to be transferred from one food source to another. To
ensure safety, a variety of toxicological and other product
safety data are provided to the FDA for food products or ingredients produced through the use of new plant varieties. The
FDA requires GMO developers to notify the agency at least
4 months in advance of commercialization of any GM foods
or animal feed and supply the food safety authority with their
research data for review. In practice, biotech companies have
led notices of commercialization long before the 4-month
minimum. The FDA review includes a thorough safety assessment that compares every signicant parameter of the GM
plant with the traditional counterpart. If no changes are detected, the FDA concludes the GM crop to be substantially
equivalent to the conventional crop with respect to nutrition
and food safety (USGC and NCGA, 2005).
US Department of Agriculture
The USDA and the EPA are responsible for reviewing the
ecological effects of new plants developed through biotechnology. The Animal and Plant Health Inspection Service
(APHIS) within the USDA is the primary agency regulating the
safety testing of biotech plants that are not insect or disease
resistant. APHIS approval must be obtained before proceeding
to eld test or commercialize a biotech plant. To test a biotech
plant in the eld, GM crop developers must seek an environmental release permit from APHIS. Once testing is allowed,
APHIS and state agriculture ofcials can inspect the test eld
throughout the process to ensure that tests are conducted
safely. Before GM crops can be grown commercially, a petition
must be submitted to APHIS containing the scientic details
about the plant, results of eld tests, and any indirect effects
on other plants. This petition is published in the Federal
Register, providing the public time to comment. When the
USDA has determined that the product is safe for eld use, it is
approved for commercialization. There are also four points at
which USDA may advance or halt development of a biotech
plant product. These are (1) greenhouse approval, (2) eld
trial authorization, (3) authorization to transport seed, and
165
166
Applicant
Application
Member state
Transmission
of dossier
EFSA
Safety
dossier
Detection
method
Joint research center
Member states
Comments
EFSA scientific panel
Validation
Opinion
European commission
Standing committee on the food
chain animal health
Unfavorable
opinion
Council of
ministers
European
commission
Draft
decision
Favorable
opinion
Decision
Figure 10 EU approval procedure for GM food and feed. EFSA, European Food Safety Authority. Reproduced from Kleter G., Kuiper, H.A., 2006.
EU Regulatory Framework and Status of Genetically Modied Crops. EAAP Workshop. ERIKILT Institute of Food Safety, Wageningen.
the deliberate release of GMOs into the environment for research and development and for placing the GMO on the
market (European Commission, 2012a,b; EFSA Panel on
Genetically Modied Organisms, 2010). Any person seeking
approval to place a GMO on the market must submit a notication to the competent authority of the member state where
the product is to be placed on the market for the rst time. The
notication dossier must describe the risk analysis conducted,
show that the products comply with the relevant European
Community product legislation, and must describe the environmental risk assessment required by the Directive. The
notication also must include specic conditions of use and
handling and a proposal for labeling and packaging, which
should comprise at least the requirements stipulated in Annex
III of the Directive, as amended. On receipt of the notication,
the competent authority has 90 days to either forward the
notication dossier to the Commission with a favorable
opinion or inform the applicant that the proposed release does
not fulll the requirements of the Directive. After receiving a
notication dossier, the Commission immediately forwards it
to the competent authorities of all member states. If no objections are raised by the competent authorities of the member
states within 60 days of the Commission forwarding the notication dossier, then the competent authority that received
the notication shall issue a written consent to the applicant
and shall inform the other member states and the Commission of that consent. (Maurer and Harl, 1998). Besides the
above-mentioned several EU Directives on GMOs, there is a
Regulation (European Commission (EC)) 1829/2003 on
genetically modied food and feed in the EU to ensure a high
level of protection of human health and welfare, environment,
and consumer interests, while seeking functioning of the internal market. The Regulation is supplemented by Regulation
167
Canada
In Canada, special labeling is required for all foods where
safety concerns, such as allergenicity and compositional or
nutritional changes are identied. Labeling must indicate the
nature of the change and must be understandable, truthful,
and not misleading. Manufacturers can choose to label products to provide information regarding the presence or absence
of GM ingredients, so long as the information is factual and
neither misleading nor deceptive (ISAAA, 2004).
168
Japan
Japan's Ministry of Agriculture, Forestry, and Fisheries (MAFF)
is responsible for environmental safety approvals, feed safety
approvals, and biotech labeling for foods. On 1 April 2001,
MAFF established a labeling scheme that requires labeling for
biotech food products if the biotech DNA or protein can be
scientically detected in the nished foods. MAFF regulations
require labels for rDNA only if an ingredient is at least 5% of
the total weight of the product (ISAAA, 2004).
Korea
The Korea Food and Drug Administration is in charge of inspecting GMO labeling on processed foods that use GM corn,
soybean, or soybean sprout, or when these three goods are
among the top ve ingredients of a processed food product.
Minor ingredients are exempt from labeling requirements. The
threshold level of unintentional mixture of GMO to those
three ingredients is 3%. Korea's Ministry for Food, Agriculture,
Forestry and Fisheries also requires labeling for commodity
shipments of the three goods if the shipment is destined for
direct consumption and if it contains a biotech-enhanced
component of 3% or higher. Identity Preservation handling
certicate is required for no labeling. Revision of labeling is
Table 4
product
Gene discovery
Construct optimization
Commercial event production and selection
Introgression breeding and wide-area testing
Regulatory science
Registration and regulatory affairs
Total
Emerging Issues
AP of biotechnology-derived materials in commodity shipments of grains, oilseeds, and their processed products remains a signicant trading issue between the trading partners.
It is critical to enable global bulk commodity supply chains to
function effectively and efciently. The term low-level presence
(LLP) refers to a specic instance of AP. LLP is the adventitious
presence of biotechnology-derived plant material in imported
commodities that has completed a full safety assessment and
has been approved for use in food, feed, grain, and derived
products by the safety authority in one or more countries,
including the country of cultivation. Under current bulkhandling systems for grains, there are many opportunities for
crops to commingle during crop production, transportation,
conditioning, and storage. Although many countries have zero
tolerance for unapproved biotech products, LLP in GM crops is
currently unavoidable. There are four different cases of
Category
169
Cost ($ million)
31.0
28.3
13.6
28.01
17.9
17.2
136.0
Duration in months
46.7
32.8
34.0
42.0
47.0
65.5
268.0
Source: Reproduced from Phillips McDougall, 2011. The cost and time involved in the discovery, development and
authorization of a new plant biotechnology-derived trait. A Consultancy Study for CropLife International. Midlothian, UK:
Phillips McDougal.
170
Conclusion
Since the rst commercialization of GM crops in 1996, in
countries where GM crops are grown and widely consumed,
there have been no reports of them causing any signicant
environmental damage or human health problems such as
toxic, allergenic, or nutritionally deleterious reaction. It is due
to the fact that robust scientic tests on GM crops before
commercialization have been conducted and that the combination of testing by developers to meet regulatory requirements for safety clearance has been done. Extensive use around
the world over a longer period of time with large exposed
populations, and the absence of evidence of harm, does provide important proof of safety of GM crop. GM crops have
been tested for 30 years, grown commercially for 16 years, and
they have been proven safe and reliable as food and for the
environment. There have been no cases of GM crops causing
ecological harm or human health problems following 16 years
of their cultivation and commercialization. The recent report
from the EU that involved 25 years of research from 500 independent research groups concluded that GM crops are no
more dangerous than other crops and are as safe as crops
produced by conventional plant breeding. The EU, the Royal
Society, and the US National Academy of Sciences all conclude
that GM crops are safe and effective. If GM technology had not
been available to the 14 million farmers using the technology
in 2009, maintaining global production levels at the 2009
levels would have required additional plantings of 3.8 million
hectare of soybean, 5.6 million hectares of corn, 2.6 million
hectares of cotton, and 0.3 million hectares of canola. This
total area requirement is equivalent to approximately 7% of
the arable land in the US, or 24% of the arable land in Brazil
(Brookes et al., 2011). Furthermore, GM crops have reduced
pesticide use by 390 million kg. GM crops are not the problem, but part of the solution to sustainably feeding 9 billion
people. However, despite the fact that GM crops have many
advantages to solve world hunger and poverty, there also exist
groups who are less convinced, insisting that new technologies
have limitations always bringing uncertainties and generating
new gaps in knowledge. Strategies that could increase the efciency of biosafety regulation without burdening GM crop
developers with further unnecessary bureaucracy need to be
established. There is a clear need for scientic communities to
References
Biotechnology Industry Organization, 2011. Available at: http://www.bio.org/
(accessed 15.01.14).
Caswell, J.A., 2000. Labeling policy for GMOs: To each his own? Agbioforum 3 (1),
5157. Available at: http://www.agbioforum.org (accessed 15.01.14).
CBD, 2000. Cartagena Protocol on Biosafety to the Convention on Biological
Diversity, Text and Annexes. Montreal, QC: The Secretariat of the Convention on
Biological Diversity.
CBD, 2010. Status of Capacity Building Activities. Montreal: Secretariat for the
Convention on Biological Diversity. UNEP/CBD/BS/COP-MOP/5/4.
CropLife International, 2005. Compliance management of conned eld trials for
biotech-derived plants. CropLife International Workshop Manual.
CropLife International, 2011. What is the Cartagena Protocol on Biosafety? Available
at: http://www.croplife.org/ (accessed 03.05.14).
CropLife International, 2012a. Labeling of Biotech-Derived Products.
CropLife International, 2012b. Plant Biotechnology Pipeline. Available at: http://www.
croplife.org/view_document.aspx?docId=3631 (accessed 27.08.12).
EFSA, 2012. Available at: http://www.efsa.europa.eu/ (accessed 03.05.14).
EFSA Panel on Genetically Modied Organisms, 2010. Guidance on the environmental
risk assessment of genetically modied plants. EFSA Journal 8 (11), 1879.
EuropaBio, 2012. Undue delays in the EU approval of safe GM products. Status
update.
European Commission, 2012a. GMO Legislation on GMO Cultivation. Available at:
http://ec.europa.eu/food/plant/gmo/legislation/gm_food_animal_feed_en.htm
(accessed 03.05.14).
European Commission, 2012b. GMO Authorization: Experimental Release into the
Environment. Available at: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?
uri=CELEX:32001L0018:EN:NOT (accessed 03.05.14).
171
Falck-Zepeda, J., Yorobe, Jr., J., Husin, B.A., et al., 2012. Estimates and
implications of the costs of compliance with biosafety regulations in developing
countries. GM Crops & Food 3 (1), 5259.
FAO, 2008. GM Food Safety Assessment Tool for Trainers. Rome: Food &
Agriculture Organization of the United Nations.
FAO, 2010. Introduction to risk analysis-basic principles of risk assessment, risk
management and risk communication. Capacity building in agricultural
biotechnologies and biosafety. Regional training in GM risk analysis for Armenia,
Georgia and Moldova. Rome: FAO.
FAO/WHO, 2000. Safety aspects of genetically modied foods of plant origin. A
Joint FAO/WHO Consultation on Foods Derived from Biotechnology, Geneva,
Switzerland, 29 May2 June 2000. Available at: http://www.who.int/entity/
foodsafety/publications/biotech/en/ec_june2000_en.pdf (accessed 03.05.14).
FAO/WHO, 2006. Food safety risk analysis: A guide for national food safety
authorities. FAO Food and Nutrition Paper 87. Rome: FAO.
FAO/WHO, 2007. CODEX Alimentarius Working Principles for Risk Analysis for
Food Safety for Application by Governments, rst ed. Available at: www.
codexalimentarius.net/input/download/standards/10751/ (accessed 15.01.14).
FAO/WHO CODEX Alimentarius, 2003a. Guideline for the Conduct of Food Safety
Assessment of Foods Derived from Recombinant-DNA Plants. Available at: www.
codexalimentarius.net/input/download/standards/10021/ (accessed 15.01.14).
FAO/WHO CODEX Alimentarius, 2003b. Principles for the Risk Analysis of Foods
Derived from Modern Biotechnology. Available at: www.codexalimentarius.net/
input/download/standards/10007/ (accessed 15.01.14).
Fedoroff, N., 2011. Burdensome and unnecessary regulation. GM Crops & Food 2
(2), 8788.
Government of Canada, 2011. Public consultation document: Policy approaches for
managing the low-level presence of genetically modied crops imported into
Canada. Working Group on Low Level Presence.
Gruskin, D., 2012. Agbiotech 2.0. Nature Biotechnology 30 (3), 211214.
Hayes, K.R., 2004. Best Practice and Current Practice in Ecological Risk Assessment
for Genetically Modied Organisms. Hobart, Australia: Centre for Research on
Introduced Marine Pests, CSIRO Division of Marine Research.
IFST, 2008. Genetic modication and food. Institute of Food Science and
Technology Information Statement. Institute of Food Science & Technology
(IFST). Available at: http://www.ifst.org (accessed 15.01.14).
ISAAA, 2004. Pocket K No. 7: Labeling GM Foods: Requirements for Implementing
Labeling Policies. Ithaca, NY: ISAAA.
James, C., 2011. Global Status of Commercialized Biotech/GM Crops: 2011 ISAAA
Briefs No. 43. Ithaca, NY: ISAAA.
Kalaitzandonakes, N., Alston, J.M., Bradford, K.J., 2007. Compliance costs for
regulatory approval of new biotech crops. Nature Biotechnology 25 (5),
509511.
Kinderlerer J., 2008. The Cartagena Protocol on Biosafety. Collection of Biosafety
Reviews vol. 4 (2008): 1265. International Centre for Genetic Engineering and
Biotechnology (ICGEB).
KPMG Consulting, 2000. Project Report. Economic Impact Study: Potential Costs
of Mandatory Labeling of Food Products Derived from Biotechnology in
Canada.
Kuiper, H.A., Kleter, G.A., Noteborn, H.P., Kok, E.J., 2001. Assessment of the food
safety issues related to genetically modied foods. Plant Journal 27 (6),
503528.
Mackey, M.A., Fuchs, R.L., 2001. Plant biotechnology products with direct consumer
benets. In: Thomas, J.A., Fuchs, R.L. (Eds.), Biotechnology and Safety, third ed.
Orlando, FL: Academic Press, pp. 119137.
Maurer, M., Harl, N., 1998. Obtaining Approvals to Market GMOs in the European
Union. Available at: http://www.econ.iastate.edu/~harl/Maurer_Harl_GMO_paper.
html
McHughen, A., 2001. Predicted failure of mandatory labels for genetically modied
foods. SCOPE GM Food Controversy Forum.
Nickson, T., McKee, M., 2002. Ecological assessment of crops derived
through biotechnology. In: Thomas, J.A., Fuchs, R.L. (Eds.), Biotechnology
and Safety Assessment, third ed. Orlando, FL: Academic Press,
pp. 234251.
NIH, 2002. National Institutes of Health Guidelines for Research involving
recombinant DNA molecules. Bethesda, MD: National Institutes of Health.
OECD, 1986. Recombinant DNA Safety Considerations Organisation for Economic
Co-operation and Development EC-Sponsored Research on Safety of Genetically
Modied Organisms. Paris: OECD.
OECD, 1993. Safety Evaluation of Foods Derived by Modern Biotechnology:
Concepts and Principles. Paris: OECD.
OECD, 2012. ENV/JM/BIO(2011)6/REV1 2010, Working Group on the Harmonization of Regulatory Oversight in Biotechnology: Environmental Risk/Safety
172
Stein, A.J., Rodrguez-Cerezo, E., 2010. International trade and the global pipeline of
new GM crops. Nature Biotechnology 28 (1), 2325.
U.S. Department of State, 1999. Food Biotechnology in the United States: Science,
Regulation, and Issues. Available at: http://fpc.state.gov/6176.htm
UNEP, 2008. National Biosafety Frameworks webpage.
UNEP, 2012. Biosafety, National Biosafety Framework. Available at: http://www.unep.
org/biosafety/National%20Biosafety%20frameworks.aspx
United Nations, 1992. Agenda 21 of the United Nations Conference on Environment
and Development, Rio de Janeiro, Brazil, June 1992. New York, NY: United
Nations.
USGC and NCGA, 2005. Agriculture Biotechnology Reference Guidebook.
Washington, DC: U.S. Grains Council and National Corn Growers Association.
Wolt, J.D., et al., 2010. Problem formulation in the environmental risk assessment
for genetically modied plants. Transgenic Research 19 (3), 425436.
Breeding: Animals
GL Bennett, EJ Pollak, LA Kuehn, and WM Snelling, USDA, ARS, US Meat Animal Research Center, Clay Center, NE, USA
Published by Elsevier Inc.
Glossary
Deoxyribonucleic acid (DNA) sequence Ordered
sequence of the DNA nucleotides adenine (A), cytosine (C),
guanine (G), and thymine (T). An animal's genome is its
complete DNA sequence.
Effective population size Number of animals in an ideal
population that would result in the same genetic diversity as
an actual, usually much larger, population.
Genetic effects (additive, dominant, recessive, and
overdominant) These terms describe the phenotype of the
heterozygous genotype compared to the phenotypes of the
two homozygous genotypes. When the heterozygote is
equal to the average of homozygotes, equal to the smaller
homozygote, equal to the larger homozygote, or exceeds the
larger homozygote, then gene effects are called additive,
recessive, dominant, or overdominant, respectively.
Genetic evaluation A prediction of the genetic value of an
animal as a parent. Genetic predictions are used to predict
average phenotypic differences between progeny from
different parents.
Genotype A genotype describes which form of a particular
polymorphism an animal has. An animal with two copies of
doi:10.1016/B978-0-444-52512-3.00228-X
173
174
Breeding: Animals
Breeding: Animals
175
some of the uncommon traits point to possible future expansion of the denition and goals for livestock selection.
DNA Technologies
Electronics
Accurate information is paramount to successful selection
programs. Information vital to the genetic evaluation supporting these selection programs consists of individual animal
identication, pedigree information, and phenotypes. Estimates of the accuracy of the individual's predicted breeding
merit complement genetic evaluation results. This accuracy is
predicated on the assumptions of the model used to create the
predictions of merit being the correct model and on accurate
information being recorded. Electronic capture of animal
identication and phenotypes improves the integrity of the
information contained in the national datasets used for genetic
evaluations.
Electronic identication such as Radio Frequency Identication (RFID) equipment, ear tags and ear tag readers, allow
livestock producers to scan the identication of an individual
directly into a recording system; hence, eliminating the potential errors of human recording. Phenotypic information can
often be collected at the same time and hence automatically
collated with the identication of that individual. Misidentication or inaccurate association of phenotypes to individuals compromises the precision of the evaluation.
Accuracy is a statistical result based on the assumptions of a
correct model and errorless information, whereas precision is a
concept that relates to the validity of these assumptions.
In some cases, electronically collected data may also be
more accurate than the same data appraised by humans.
Electronic scales calibrated to obtain weights at stability can be
more accurate than the same weights recorded by the person
watching the scale. Instrument grading of carcasses for quality
measures (e.g., marbling score) is objective and more accurate
than visual appraisal for the same measurement.
Electronic transmission of information to central databases
expedites the process of data entry into the genetic evaluation
database. Previous methods depended on data being transcribed and mailed to central locations and nally entered
manually into the database with iterations of checks to validate the integrity of the information. Electronic transmission
of digital data allows for immediate submission, electronic
queries of the data to check for errors (e.g., data outside of
acceptable ranges), and direct database query of the information to ensure consistency of new data with data entered
previously into the database (e.g., sex of the individual).
Electronic searches of the database provided via the web allow
access to genetic evaluation information immediately on creation. Electronic distribution of les of evaluations directly to
the owners of the animals speeds up the process of selection.
Finally, highly computerized systems of data capture, validation, and synthesis lend support to more frequent genetic
evaluations that in turn provide more timely information for
selection decisions earlier in an animal's life. An example of
frequently run genetic evaluations is the American Angus
Application of DNA-based technologies for livestock improvement starts with on-farm collection of animal tissue
samples. Those samples are then transferred to a laboratory,
where DNA is extracted for genotyping and the genotypes are
interpreted to provide the livestock breeder with information
for selection and mating decisions. Any tissue containing DNA
is a possible sample. Blood and hair follicles are common
DNA sources for cattle. Ear notches and tips of tails are convenient to collect when processing piglets at birth. Sampling
systems must ensure cleanliness and avoid contamination
with foreign material and DNA from other animals. It is vital
that the system maintains identity of the sample so that DNAbased information corresponds to the animal that was sampled (e.g., creation of a DNA sample collection website). Some
systems use prelabeled sample containers and barcoded tissue
sampling ear tags. These types of systems use the same identication for sample and animal tag and can reduce labeling
errors to maintain consistency between animal and sample
identity.
Collection and processing of DNA samples must occur
before making decisions. One of the uses of DNA information
is identifying genetic defects. Decisions on a carrier animal
(one normal DNA copy and one mutated DNA copy) and its
parents can occur any time between birth and use as a
breeding animal. Information from animals sampled and
genotyped soon after birth allows quick use of information in
the parents. In purebred animals, breed associations often post
identities of carrier and related animals and indicate their
carrier status on pedigrees for a few mutations that are veried
and important to the breed. DNA sequencing of animals reveals many mutations at very low frequencies that could adversely affect animals if they had two copies of the mutated
DNA. Reporting and transmitting DNA mutation information
needs to evolve so that livestock breeders can consider many
more mutations.
Determination of parentage is a growing use of DNA testing. In many cases, the livestock producers know the mother at
birth but the sire might be any one of a group of sires. Results
of parentage from DNA tests returned to livestock producers
have different formats. Identication of the most likely parent
and its reliability is useful to livestock breeders.
Genetic evaluation systems based on phenotypes require
parentage. The parentprogeny connection allows progeny
phenotypes to contribute to genetic evaluation of parents and
also allows parent information to contribute to genetic
evaluation of the progeny. For breeding animals, parentage
information is critical for either avoiding inbreeding or creating inbred animals. Parentage determined from DNA samples collected soon after birth allow undelayed incorporation
of progeny phenotypes into genetic evaluations.
Livestock breeders receive results of early genetic tests based
on DNA several ways. Results can consist of actual DNA differences, predicted effects of DNA differences, and categories of
predicted effects. Current tests use many DNA differences and
176
Breeding: Animals
Reproductive Technologies
Reproductive technologies have a tremendous effect on the
rate of genetic change in domesticated livestock species. Primarily, most of these gains occur because of increases in the
number of progeny possible per individual. Examples of these
technologies are articial insemination (AI) and multiple
ovulation embryo transfer (MOET). However, adoption rates
of some other reproductive technologies are not only less than
AI but they also have the potential to increase rates of genetic
change.
Cattle producers have had commercial access to AI since
the 1940s, with the establishment of standard procedures and
organization of AI cooperatives (Foote, 2002). The use of
semen extenders, technology to freeze semen and maintain
viability, and the ability to divide a single ejaculate into
multiple inseminations has overall increased the utility of AI.
As of 2010, the percentage of US dairy cows bred by AI exceeds
60%. Other domesticated livestock species, especially swine
and poultry, also heavily use AI although the viability of frozen semen is less than it is in cattle. Difculty with depositing
semen through the cervix of ewes has limited the use of AI in
sheep though many large international ocks use laparoscopic
techniques.
Similar to AI, MOEt allows a female to produce more offspring than would be possible using natural service breeding
schemes. For this process, the female is superovulated (using a
follicle stimulating-like hormone) and then inseminated. Recovery of fertilized embryos occurs before implantation. These
embryos are placed in recipient females to produce calves from
the donor female. Cryogenically freezing these embryos adds
more options for using them. Shipping frozen embryos to
multiple locations or delaying their transfer is possible. In
general, cost decreases the use of MOET compared to AI. It is
also difcult to identify genetically superior females before
using MOET because females have few progeny to prove their
genetic merit.
For sex-limited traits, such as milk production, both AI and
MOET offer advantages to most of the components of the
breeder's equation. More progeny increases the accuracy of
selection for the parents. For example, dairy bulls have hundreds of daughters tested for milk production using AI. The
larger number of progeny increases selection intensity as fewer
sires (AI) or dams (MOET) are needed to produce the next
generation of breeding animals. MOET can decrease the generation interval because a bull and a cow are more likely to
produce progeny to replace themselves from their rst mating.
Not surprisingly, both of these advances have had their
greatest impact on livestock species with low prolicacy.
Breeding: Animals
Historically, national and international associations providing genetic evaluation services to their membership published annual or biannual evaluations. Constraints on more
frequent evaluations were data collection and reporting,
computing capacity to run the large evaluation programs, and
time needed to assemble the results in a publication form
(e.g., a sire summary). Interesting nuances peculiar to some
traits also challenged the incorporation of new information.
For example, producers record and report a dairy cow's
monthly performance or a hen's weekly egg count but the trait
of interest is total lactation production (the accumulation of
all monthly production records) or yearly egg production.
Yearling weight may be the trait of interest at weaning but at
the time of selection all that is available are correlated birth
and weaning weights. Lactation projection strategies based on
partial records (using available monthly records of a lactation
in progress to predict total production) and multiple trait
evaluations capturing information from correlated traits are
just two examples of strategies designed to improve the
timeliness of evaluations for these situations.
As electronic reporting of data became routine and organizations moved to electronic delivery of genetic evaluation
results along with or instead of publications, the timeliness of
evaluations improved. Web-based programs allow producers
to search and obtain genetic evaluation information online to
expedite this process (e.g., Angus sire search and Holstein
search websites). These searches allowed producers to identify
animals that meet specications in traits of interest quickly.
As computing capacity and electronic movement and access
to information improved, the opportunity to provide more
frequent evaluations became possible. For example, the
American Angus Association provides weekly runs of genetic
evaluations. Another strategy used is to provide interim
evaluations that evaluate information from a particular producer alone instead of running the entire national program at
the time the information is received. Updates of interim
evaluations occur when the national program runs.
Awareness and interest regarding the value of genetic information increased in the animal industries, and so did the
desire to record and report evaluations for many more traits.
For example, at the Angus sire search website breeders can
search the database of evaluations for eighteen individual
traits. Efcient selection based on individually considering this
plethora of traits is difcult. An alternative to considering individual traits is combining the information into indices designed to reect selection objectives. At the Angus sire search
website, one could search the database for animals that excel
in indices (expressed as dollar values) for predicted value at
weaning of calves, to feedlots, or the value at harvest of the
progeny of an animal considered for selection. The dollar
value prediction of calves at weaning is an index consisting of
4 of the 18 individual traits reported:
1. Birth weight inuences difculty during birth and calf
survival hence percent calf crop weaned;
2. Weaning weight inuences revenue;
3. Maternal milk inuences weaning weight hence
revenue; and
4. Mature cow size reect maintenance requirements and
hence expense.
177
178
Breeding: Animals
Breed Comparisons
Breeds and lines within breeds arose from different base
populations with different selection histories, effective sizes,
and are often not farmed or raised together. Unbiased estimates of trait differences are important for deciding how to use
breeds and lines. Governments, livestock organizations,
international aid organizations, and companies compare
breeds and lines for the benet and education of livestock
producers and for internal use and merchandising by companies. The number of breeds and lines compared and the
duration of comparisons vary considerably. Some organized
comparisons extended for more than 50 years.
Methods to compare breeds and lines depend on many
circumstances. The best approach samples the breeds so that
they represent the genetics that are available to livestock
Crossbreeding Systems
Breeding males and females of the same breed, called straight
breeding or pure breeding, is one way to use breeds and lines.
Breeding males of one breed with females of another breed is
crossbreeding. Many livestock production systems benet
from planned crossbreeding systems. The benet is derived
from two factors known as heterosis and complementarity.
Heterosis has a genetic basis and describes the difference in
performance between crossbred animals and the average of the
purebreds used to create the crossbred. Several causes of
heterosis are possible and not exclusive. Many studies of
heterosis in livestock point to dominance as the primary cause
but experiments designed to estimate heterosis often have
difculty separating dominance from other possible causes
such as epistasis, the effects derived from combinations of two
or more differences in DNA. Dominance occurs when DNA at
the same location on a chromosome is not identical among
animals and those with pairs of nonidentical DNA perform
differently from the average of those with identical pairs
Breeding: Animals
179
180
Breeding: Animals
similarly. A common contemporary grouping is herd-yearseason consisting of animals born in the same herd, year, and
season. Statistical analyses for genetic evaluations typically
adjust contemporary groups simultaneously.
Heritability
Heritability describes how much of the differences in phenotypes among animals treated similarly is due to genetics. It is
the most basic connection from phenotype to DNA and genetic evaluation. Heritability is the ratio of genetic variance
(VG) to phenotypic variance (VP) and ranges from 0 to 1.
High heritability values of 0.5 mean that on average half of the
differences among phenotypes of animals are genetic. Low
values of approximately 0.1 mean that most of the differences
are not genetic. Multiplying heritability times the differences
between each animal's phenotype and their average is a simple
genetic evaluation. The accuracy of these genetic evaluations is
the square root of heritability.
Several types of genetic variance exist. Additive genetic
variance predicts permanent and continued response to selection. Other types of genetic variance (dominance and epistatic) do not predict long-term, continuing selection
responses. Broad sense heritability describes the ratio of total
genetic variance to phenotypic variance as discussed above.
Narrow sense heritability describes the ratio of additive genetic
variance to phenotypic variance. Genetic evaluation calculations use estimates of additive genetic variances.
Using the average of several measurements of a phenotype
can substantially increase heritability. The variance of the average of N independent measurements is 1/N times the variance
of one measurement. A phenotype like wool weight is measured each year of a ewe's life. The variance of an average
phenotype (VPAV) is the sum of the genetic (VG) and permanent environment (VPE) variances, which are repeated each
year, and the residual variance (VE) that is independent from
one measurement to the next is divided by N: VPAV VG VPE VE/N. The heritability of an average is VG/VPAV. Table 1
shows how VG and VPE affect heritability of the average
phenotype. New technologies may make it easier to measure
traits repeatedly leading to higher accuracy genetic evaluations.
Pedigrees
Pedigrees describe genetic connections among animals. Pedigrees record the male (sire) and female (dam) parents of each
Table 1
The relative increases in heritability of an average of
repeated measurements from adding an additional measurement is
more when genetic variance (G) is lower, variance from permanent
environment (PE) is lower, residual variance (E) is greater, and there
are few measurements
Variances
Number of measurements
PE
10
10
30
30
15
5
15
5
75
85
55
65
0.10
0.10
0.30
0.30
0.016
0.17
0.41
0.44
0.23
0.28
0.51
0.59
0.29
0.39
0.58
0.70
Breeding: Animals
animal. Relationships like full-sibs (same sire and dam), halfsibs (same sire or same dam), grandparents (grandsire and
granddam), and irregular relationships become apparent from
accumulating and linking sire and dam relationships. Many
breed associations have a long history of recording sires and
dams of purebred livestock and creating pedigrees. Individual
breeders and companies also maintain private pedigrees for
their use internally. Figure 1 shows pedigree diagrams emphasizing ancestors or families.
Related animals share a portion of their DNA. Pairs of close
relatives (sire and a daughter; two full-sibs) share more DNA
than distant relatives (two animals with the same great
grandsire). The phenotype of any animal that shares DNA with
a genetically evaluated animal can contribute to that evaluation. The degree of contribution depends on how much DNA
they share and the number and relationships to other animals
with phenotypes. The coefcient of relationship (R) between
two animals in a noninbred population is the average amount
of shared DNA between them. Values of R for simple relationships are 0.5 for parent and progeny or full-sibs; 0.25 for
half-sibs; and 0.062 5 for animals sharing a single grandparent. Calculation of R usually considers only the paired
chromosomes and not the sex chromosomes but it is possible
to consider them separately.
Actual livestock populations have many complex relationships among animals. Calculating R in these populations depends on tabular methods and other algorithms that can
extend to very large populations and breeds. The result of these
calculations is a relationship matrix, an array of values showing an R value for every pair of animals. Table 2 shows a small
portion of a relationship matrix in a cattle herd with R values
from 0.016 to 0.520 for ve animals. Genetic evaluations now
use relationships among millions of animals by combining
Animal
Table 2
Animal Identity
98006a
118052
118158
118216
118227
98006
118052
118158
118216
118227
1.0b
0.037
0.520
0.157
0.065
0.037
1.0
0.037
0.016
0.028
0.520
0.037
1.0
0.157
0.065
0.157
0.016
0.157
1.0
0.115
0.065
0.028
0.065
0.115
1.0
Parents
Grandparents
Mastercraft
Hercules 66053
Seventy-one hestar
Hope 06154
Principal 26072
Hope 56032
Creek ranch 247
(a)
Hope 06092
Hope 36049
Half-sib
181
Hercules 66053
Hope 56032
Hercules 96060
Hope 06154
Full-sibs
(b)
Figure 1 Pedigree diagrams emphasizing (a) ancestors and (b) family structure.
Hercules 46095
Hope 06154
Half-sib
182
Breeding: Animals
Table 3
Accuracy of animal phenotype, daughter averages, and
full-sib averages for different heritabilities and effects of rearing fullsibs in the same litter
Relationship
Animal
Daughter average
Full-sib average
Number
Litter effect
Heritability
0.10
0.25
0.40
0.55
0.32
0.50
0.63
0.74
2
4
8
16
32
0.22
0.30
0.41
0.54
0.67
0.34
0.46
0.59
0.72
0.83
0.43
0.55
0.69
0.80
0.88
0.49
0.62
0.75
0.85
0.91
0.16
0.22
0.20
0.29
0.24
0.25
0.33
0.31
0.43
0.36
0.32
0.41
0.38
0.50
0.43
0.37
0.46
0.43
0.55
0.48
1
2
2
4
4
Any
0
0.2
0
0.2
Genetic Correlation
Phenotypic correlation is the term that describes animals with
high values for one phenotype also tending to have high (or
low) values for another phenotype. Correlations are positive
when high values occur together and negative when high
values in one trait occur with low values in another. Desirable
describes positive correlations of phenotypes selected in the
same direction and negative correlations of phenotypes
Breeding: Animals
values. BLUP methods are now widely used by livestock industries to predict breeding values.
Steady advances in the adaptation of BLUP techniques to
different situations encountered in livestock breeding made
this technique increasingly valuable. Advances in computational power, application of numerical analysis methods, and
efcient memory storage algorithms also contributed toward
its broad adoption. Initial applications of BLUP were restricted
to predicting breeding values among sires for a single trait but
this expanded to sires and maternal grandsires and then to
individual animals (Animal Model BLUP) for direct and maternal breeding values. Additional enhancements included
simultaneous prediction of multiple traits and prediction of
categorical traits like survival.
Parent
A
Linked markers
Chromosome pair
Progeny 1
Progeny 2
183
Progeny 3
Progeny 4
Progeny 5
Figure 2 Linked genetic markers on a section of paired chromosomes are often inherited together. Dashed lines show parental chromosome
source in progeny chromosomes. Progeny 3 shows mixed chromosomal sources resulting from a crossover in replicating the parental
chromosome.
184
Breeding: Animals
Overdominance
AA
Dominance
Incomplete dominance
AT
Additive
Incomplete recessive
TT
Recessive
(a)
CC
CG
GG
(b)
CC
CG
GG
Figure 3 Description of (a) allele G effect depends on average phenotypes of heterozygous (CG) and homozygous (CC an GG) genotypes, and
(b) an example of epistasis involving two polymorphisms in different locations.
disequilibrium form inherited groups of alleles. Three polymorphisms with two alleles for each could form eight combinations (AGT, AGC, ACT, TGT, ACC, TGC, TCT, and TCC)
but strong disequilibrium may result in only three or four
actually occurring (e.g., AGT, AGC, TGT, and TCC). When
similar haplotypes occur in different populations, then causal
polymorphisms linked to the haplotype should also be
similar.
Genetic marker tests derived in one population may not
work in another because causal polymorphisms and linkages
with the causal polymorphisms can differ in populations because the causal polymorphism in one population might be
absent in another population. The National Beef Cattle
Evaluation Consortium (NBCEC website) and the SmartGene
for Beef project (SmartGene website) conducted validation
tests of some genetic markers used in beef cattle and available
from commercial companies.
Many traits emphasized in commercially available genetic
marker tests are costly, difcult, or available too late in life to
evaluate accurately using phenotypes and pedigrees. These
include meat quality, disease resistance, fertility, and efciency. Selection based on genetic markers has the most potential for these traits. However, the same constraints also
affect the success of discovering associations of genetic markers
with these traits.
Genomic Selection
Beyond simply inherited mutations and traits affected by
a single gene or small set of interacting genes with large
effects are a myriad of complex diseases and traits inuenced
by genetics and environmental conditions. Recent genomic
technologies enabled development of panels with dozens to
hundreds of thousands of genetic markers for livestock species.
Genotyping costs for these panels are very economical and
open the door to different approaches for using genomic information. Other improvements in DNA sequencers have
made sequencing of many individual animals affordable.
Targeted sequencing of the 2% of the genome that codes for
proteins (exome) is another approach being used to access
DNA information across the whole genome. DNA sequence
information reveals some of the structure and types of genetic
polymorphisms as well as their genotypes across the genome.
Sequencing genomes and exomes and genotyping hundreds of thousands of individual animals are much more affordable now than just a few years ago; however, it is still not
Breeding: Animals
cost effective. A strategy proposed and adopted in some selection schemes is the prediction of missing genotypes through
a process called imputation. This process begins by identifying
key animals for DNA sequencing or genotyping with panels of
tens or hundreds of thousands of genetic markers. Identifying
key animals usually begins with sires of males considered for
selection, one of the four selection pathways, and then sires of
females considered for selection. Other animals descended
from key animals are genotyped with smaller panels of hundreds to several thousand genetic markers. Imputing genotypes
uses both linkage disequilibrium among the genetic markers
and pedigree to ll in all genotypes for animals genotyped
only with smaller panels.
Although genetic evaluation using performance and pedigree records has been effective for some traits, including
marker genotypes in genetic evaluations can increase accuracy
or allow earlier evaluations. If genetic markers accounted for
sufcient genetic variation in a trait, then the accuracy of
newborn animals could be similar to that of a parent having
several progeny measured for the trait. The terms genomic
selection and genome-wide selection describe selection based
on panels of many markers spread widely across the genome.
There are several approaches to implementing genomic selection, and supporting research is rapidly progressing.
One approach to genomic selection begins by genotyping a
large training population using imputation with a large panel
of genetic markers or from sequencing individual animals.
Phenotypes measured in the training population are then
associated with genotyped and imputed polymorphisms.
One way of applying results from the training population
to the population under selection is imputing the same set of
genetic markers in the selection population by genotyping a
combination of larger and smaller panels of genetic markers.
Alternatively, a smaller panel of genetic markers selected from
the most highly associated set of genetic markers in the
training population is genotyped in the selection population.
Geneticists use both small panels consisting of markers
selected based on association with a suite of production traits
and large, whole-genome panels having enough markers to
ensure unknown causal polymorphisms in the genome will be
associated with genotyped genetic markers to explain genetic
variation. Low-density panels can reduce costs of genotyping
either by direct use of their genetic markers or as a tool to
impute large panel genotypes in conjunction with large panel,
reference genotypes of inuential ancestors.
Another source of training information that works well in
dairy and beef cattle is the progeny averages of widely used
sires. These sires have hundreds to thousands of progeny
measured for some traits. Progeny averages approach half
of true genetic differences and eliminate much of the dam
and nongenetic variation. If there are enough widely used
sires, then genotyping only these sires can lead to good estimates of genetic marker effects. However, this method is
limited to traits measured in many progeny. Other important
traits that are difcult to measure need other types of training
populations.
One of the difculties of estimating genetic marker effects is
that there are often many more genetic markers than training
animals. This leads to spurious associations with the markers
and erroneous genomic predictions in other populations.
185
Research on statistical methods and other approaches is addressing this problem. Two approaches to limit or prioritize
genetic markers for use in genomic prediction include using
markers in or near genes that are part of relevant metabolic
pathways and using genetic markers with predicted severe effects on proteins.
After genotyping and measuring phenotypes in the training
population, a new animal's predicted genomic value for a trait
in the selection population is the sum of marker genotypes
multiplied by estimated effects of each marker for that trait.
Livestock breeders would use these genomic predictions for
selection when no other information is available on a trait.
Sometimes animals or their relatives will have both genomic,
phenotypic, and pedigree information for a trait. One approach to combine this information is an index weighting the
genomic values and the genetic evaluations based on phenotypes and pedigree. A second approach uses a standard twotrait and pedigree genetic evaluation treating the genomic
breeding values as genetically correlated traits. A desirable
byproduct of this approach is an estimate of the proportion of
genetic variation explained by the genomic predictions. High
proportions indicate that genomic predictions are working
well and are appropriate for the population.
Single-step methods simultaneously estimate genetic
marker effects and combine either or both genotypes and
phenotypes of animals to produce genotype-assisted genetic
evaluations. This method uses genomic relationships to replace pedigree relationships when animals have genotypes.
Pedigree relationships are expectations of proportions of
shared genome based on parentage but genomic relationships
measure similarity of genotypes to estimate sharing.
These approaches effectively increase accuracy of young
genotyped animals for routinely recorded traits within wellstudied breeds and breeding populations, extending the predictions across breeds remains a challenge. Although marker
effects estimated in a specic population can account for
much genetic variation within that population, applying those
effects to genotypes from an unrelated population seldom
explains enough variation in the unrelated population to have
a meaningful impact on breeding value accuracy. Meeting the
challenge of robust genomic predictions applicable across
livestock populations could enable meaningful genomic predictions for traits that are economically important but too
difcult and expensive to measure routinely.
References
Flock, D.K., Heil, G., 2002. A long-term analysis of time trends in the performance
prole of white-egg and brown-egg hybrid laying strains based on results of
ofcial German random sample tests from 1974/75 to 1997/99. Archiv fr
Gegelkunde 66, 120.
Foote, R.H., 2002. The history of articial insemination: Selected notes and notables.
Journal of Animal Science 80, 110.
186
Breeding: Animals
Gregory, K.E., Bennett, G.L., Van Vleck, L.D., Echternkamp, S.E., Cundiff, L.V., 1997.
Genetic and environmental parameters for ovulation rate, twinning rate, and
weight traits in a cattle population selected for twinning. Journal of Animal
Science 75, 12131222.
Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003a. Carcass composition and yield
of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler
diets. Growth, livability, and feed conversion of 1957 versus 2001 broilers when
fed representative 1957 and 2001 broiler diets. Poultry Science 82, 15091518.
Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003b. Growth, livability, and feed
conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001
broiler diets. Poultry Science 82, 15001508.
Hohenboken, W.D., 1999. Applications of sexed semen in cattle production.
Theriogenology 52, 14211433.
Ibeagha-Awemu, E.M., Kgwatalala, P., Ibeagha, A.E., Zhao, X., 2008. A critical
analysis of disease-associated DNA polymorphisms in the genes of cattle, goat,
sheep, and pig. Mammalian Genome 19, 226245.
Kashyap, T.S., Dickerson, G.E., Bennett, G.L., 1981. Effectiveness of progeny test
multiple-trait index selection for eld performance of strain-cross layers I.
Estimated responses. Poultry Science 60, 121.
MacNeil, M.D., 2009. Research contributions from seventy-ve years of breeding
Line 1 Hereford cattle at Miles City, Montana. Journal of Animal Science 87,
24892501.
McParland, S., Kearney, J.F., Rath, M., Berry, D.P., 2007. Inbreeding trends and
pedigree analysis of Irish dairy and beef cattle populations. Journal of Animal
Science 85, 322331.
Merks, J.W.M., 2000. One century of genetic changes in pigs and the future needs.
In: Hill, W.G., Bishop, S.C., McGuirk, B. et al. (Eds.), The Challenge of Genetic
Change in Animal Production. Occasional Publication No. 27. Edinburgh, UK:
British Society of Animal Science, pp. 819.
Morris, C.A., Towers, N.R., Wheeler, M., Wesselink, C., 1994. Selection for or
against facial eczema susceptibility in Romney sheep, as monitored by serum
concentrations of a liver enzyme. New Zealand Journal of Agricultural Research
38, 211219.
Seidel Jr., G.E., 2012. Sexing mammalian sperm Where do we go from here?
Journal of Reproduction and Development 58, 505509.
Van Vleck, L.D., 1999. Implications of cloning for breed improvement strategies: Are
traditional methods of animal improvement obsolete? Journal of Animal Science
77, 111121.
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J., Campbell, K.H.S., 1997. Viable
offspring derived from fetal and adult mammalian cells. Nature 365, 810813.
Relevant Websites
http://www.angus.org/Nce/SireEvaluationDefault.aspx
Angus Genetic Evaluation.
http://www.angus.org/Nce/SireSummarySearchCriteria.aspx
Angus Sire Search.
http://aipl.ars.usda.gov
Animal Improvement Programs Laboratory.
http://www.holsteinusa.com/pedigree_info/searchTheDatabase.html
Holstein Association, USA.
http://www.animalgenome.org/gbrowse/
National Animal Genome Research Program.
http://www.nbcec.org/research.html
NBCEC.
http://omia.angis.org.au/
Online Mendelian Inheritance in Animals.
http://agbu.une.edu.au/SmartGene%20Report11.pdf
SmartGene.
http://beef.unl.edu/learning/dnacollection.shtml
UNL Beef.
Glossary
Epistasis The dependence of one gene's effects on the state
of a different gene in the same organism.
Genomic selection The use of a large number of genetic
markers across the genome to predict breeding values of
plants that have not been grown and tested yet.
Germplasm The material representing the genetic diversity
available to a breeding program, often stored as seeds or
vegetative plant cuttings or maintained in living nurseries.
Linkage disequilibrium Alleles at different genes that
cooccur in individuals more often or less often than
doi:10.1016/B978-0-444-52512-3.00226-6
187
188
Level of genetic
variation among
plants within the
same variety
Pure-line cultivars
Uniform
Modern rice,
wheat, soybean;
older tomato
Highly heterozygous
F1 hybrid cultivars
Modern maize, tomato, some
rice, many modern vegetables
Clonally propagated cultivars
Fruit trees, potato, ornamentals
Synthetic cultivars
Landrace population
varieties of inbreeding
species
Rice, wheat,
legume seed
landraces
Variable
Landraces of
outbreeding species
Natural populations
Unimproved forest and
rangeland species
Figure 1 Classication of cultivar types according to genetic diversity among plants within a cultivar and heterozygosity within a plant.
189
190
(G2 A2 D2 ), then the total phenotypic variance is composed of these components plus environmental variance:
P2 G2 2 A2 D2 2
The proportion of that total phenotypic variance that is
heritable is the heritability (h2):
h2
A2
A2
2
P2
A D2 2
G2
2 2
2 A 2 D 2
P2
A D
the genotypic variation among and within lines at each generation is simply a function of the level of inbreeding. However, modeling the nonadditive components of inheritance
that contribute to variation among and within lines under
intermediate generations is quite complicated (Cockerham,
1983) and measuring those components is exceedingly difcult (Edwards and Lamkey, 2002). In such a case, the appropriate measure of heritability depends on which
generations are considered the selection units and which are
considered the response units. In the simplest case, a sample
of completely homozygous inbred lines from a cross can be
evaluated, and only the best lines selected. If those best lines
are then propagated as cultivars and considered the end
product of that breeding cycle, then the heritability in this
situation is a function of total genotypic variance among
completely homozygous lines (which includes twice as much
additive variance as in the outbred population, no dominance
variance, but possibly other higher-order genetic components
of variance). Thus, it is entirely appropriate in this situation to
use an estimator of heritability that does not match Lush's
narrow-sense heritability. In situations where the selected lines
are themselves intermated to form a new breeding population,
which itself may be inbred, the appropriate heritability estimator depends on the generation of the selected lines as well
as the generation of the progeny lines. For this reason, plant
breeders would do well to label clearly their estimates of
heritability in terms of the units of selection and the units of
response to which they apply (Holland et al., 2003).
191
G2
G2
2
GE
e
2
re
192
1600
CML254
1400
B73
1200
Oh603
1000
800
600
400
200
0
Long daylength
environments
Short daylength
environments
2
and their inbreeding level, GE
is the genotype-by-environment
interaction variance, 2 is the average within-environment
microenvironmental variance, e is the number of environments
used for evaluation, and r is the number of replications per
family per environment. This equation shows that the heritability, and consequently, the expected gain from selection, can
be often increased by increasing the number of testing environments e. If the breeder includes environments that are too
distinct, however, the genotype-by-environment variance component may increase and overwhelm the genetic variance
component, causing heritability to decrease. In such situations,
it pays to identify more homogenous subsets of environments
and split the breeding program to select for families that are
superior within regions, rather than to continue to search for
families that are superior across the whole range of macroenvironments (Ceccarelli, 1989; Simmonds, 1991).
Another component of the heritability equation that
the breeder can exercise some control over is the withinenvironment microenvironmental variation (also known as
the experimental error variation). As seen in the equation
above, the contribution of this component to the denominator
of heritability can be reduced by increasing either the number
of testing environments or the number of replications at each
environment. There is a nearly direct trade-off in resources
between increasing the number of replications evaluated and
the number of unique genotypes that can be tested. Fortunately, breeders can avail themselves of experimental designs
and statistical analysis methods that can help reduce the experimental error variance without requiring additional testing
resources. The major challenge to controlling experimental
error in breeding trials is the large number of genotypes to be
evaluated. With many genotypes to evaluate, the total physical
eld size required to plant all of them often become so
large that the microenvironments of plots can become quite
different across the testing eld. Most commonly, soil quality
may vary across the eld so much that comparing the yield of a
variety grown on one side of the eld to a variety grown on the
193
194
195
which individual genes with large effects have been identied directly or by tight linkage to markers (Collard and
Mackill, 2008; Francia et al., 2005; Ismail et al., 2013);
Numerous disease resistances and simply inherited fruit
quality characteristics regularly targeted with markers in
commercial tomato breeding programs (Foolad and
Panthee, 2012);
Disease-resistance genes, self-incompatibility, fruit quality
in several fruit crops of genus Prunus (Dirlewanger et al.,
2004);
Many (450) simply inherited disease resistance and grain
quality characteristics targeted by public wheat breeding
programs (Dubcovsky, 2004; Eagles et al., 2001; Gupta
et al., 2010; Miedaner and Korzun, 2012).
The experience with marker-assisted selection in wheat
breeding is particularly instructive, as this has been done almost entirely in the public sector across several countries.
Australia pioneered the practical application of marker-assisted
selection on a large-scale by creating centralized genotyping
facilities to support the applied breeding programs (Eagles
et al., 2001). The USA federal government followed suit by
establishing four regional small grains genotyping facilities to
conduct marker analysis for both public and private sector
breeders and by funding a coordinated multistate project to
make genotypic selection widely available to applied breeding
programs (Dubcovsky, 2004). By removing the burden of
marker development and genotyping from each individual
breeding program (which typically do not have sufcient resources to perform marker analyses on substantial proportions
of their breeding material), the centralized facilities have enabled the integration of marker-assisted selection into cultivar
development in small grains. The USA small grains markerassisted breeding project assisted in the release of at least
90 cultivars.
The wheat example also highlights the trend seen across the
examples of marker-assisted selection in other species: specic
markers have been most useful for selection when they identify alleles of relatively large effect. Major disease-resistance
genes are the most common example of this: the presence of a
particular disease-resistance allele can determine completely if
a plant is resistant to a particular race of pathogen. In addition
to the targeted gene having a major effect, markers are most
useful when they are diagnostic for a phenotypic effect across
most breeding crosses that are expected to segregate for the
phenotype (Collard and Mackill, 2008; Holland, 2004). Although there are special cases in which linkage relationships
between linked markers and causal variants tend to hold in
breeding programs, high resolution genetic analysis to identify
casual sequence variation that underlies desired phenotypes is
usually required to obtain a diagnostic marker (Holland,
2004).
Markers have proven particularly useful to backcross
breeding programs, where a panel of markers can be used to
select simultaneously for the desired allele from the donor
parent, against linked donor alleles (to reduce linkage drag),
and against donor alleles on other chromosomes (to reduce
the number of generations required to recover most of the
recurrent parent genome) (Chen et al., 2000; Collard and
Mackill, 2008; Frisch et al., 1998; Randhawa et al., 2009).
196
197
more markers than individuals in the test population! Standard regression techniques cannot be used for such overtted
models, so alternative statistical techniques must be used, such
as Bayesian analysis, ridge regression, or mixed models with
constrained marker variances (Bernardo and Yu, 2007; Meuwissen et al., 2001; Xu, 2003). The details of these analyses are
complex, but the key objective of genomic selection is to
predict the breeding value of lines in the study as well as lines
with genotype information but no phenotype information
using the prediction model (Lorenz et al., 2011). Unlike QTL
mapping, the prediction models do not attempt to accurately
estimate the effects of each genome region, instead they sacrice accuracy on individual marker effects by overtting the
markers, but increase the accuracy of breeding value prediction
based on the net value of markers. In this way, the optimal
amount of information about polygenic effects is extracted
from the set of lines with both genotypic and phenotypic information (the training data set), providing better predictions
for lines with only genotypic data (Heffner et al., 2009), which
could represent untested sib lines or progeny generated from
crosses among lines in the training data set. Genomic selection
models are not expected to provide accurate estimates of the
effects of specic genome regions on traits, however.
Bernardo and Yu's (2007) original proposal for implementing genomic selection was in the context of a commercial
maize breeding program, in which genomic recurrent selection
could be conducted for several cycles on seeds or seedlings in
offseason nurseries. Separate genomic selection models could
be created for each biparental cross family, which maximizes
the consistency of linkage relationships between markers and
causal genes over several cycles of selection. Even when
genomic marker predictions of phenotypes are less accurate
than direct phenotypic evaluations, genomic selection can
produce greater gains per unit of time by enabling additional
cycles of selection on individuals seeds or plants in offseason
nurseries (Heffner et al., 2011a, 2010; Lorenzana and Bernardo, 2009; Massman et al., 2013).
An alternative use of genomic selection is the development
of prediction models encompassing lines derived from many
different parental combinations rather than just one cross
(Crossa et al., 2010; Heffner et al., 2010; Zhong et al., 2009).
Cross-validation and simulation studies suggest that this could
work (Crossa et al., 2010; Heffner et al., 2011b; Riedelsheimer
et al., 2012), but that there are difculties with combining
information across very diverse germplasm sets (Lorenz et al.,
2012; Zhong et al., 2009). Windhausen et al. (2012) demonstrated that genomic prediction models created by combining
diverse maize breeding pools had good accuracy for prediction
of germplasm in those same pools, but the prediction accuracy
fell to approximately zero when the models were applied to
newly created biparental populations. Simply, the training
data set used to create the genomic selection model must have
a close genetic relationship to the breeding population to
which it is derived. Exactly how close this relationship must be
is still a matter of investigation. The availability of such largescale prediction models is likely most useful for well-resourced
commercial breeding programs, where the ability to generate
and genotype new progeny lines outstrips the ability to conduct high-quality phenotypic evaluations of yield and other
complex traits. In this way, the breeding potential of progeny
198
lines that have never been planted in a eld could be predicted, and lines with superior predicted values could be retrieved from storage for future phenotypic evaluations. This
approach emphasizes the expenditure of precious phenotypic
testing resources for materials that have the best chance of
being cultivars or cultivar parents.
Marker-assisted selection and genomic selection are important components of modern breeding programs in many
crops. The balance between the use of resources on DNA
markers to select for specic gene alleles, genomic selection to
select for the polygenic background, and phenotypic evaluations will likely shift as research indicates the best application
of each evaluation method. The optimal balance likely will
vary among crops and even among different programs in the
same crop, as it will depend on the relative availability and
cost of genomics resources compared to eld testing.
To the extent that genetic dissections of important traits
succeed in identifying causal genes and sequence variants (via
association analysis, high resolution linkage mapping, or other
means), those alleles can be targeted for selection and for incorporation across distinct germplasm groups. This form of
direct allele selection (Sorrells and Wilson, 1997) should be
more effective at predicting the value of alleles across diverse
germplasm than genomic selection models, which are highly
dependent on the genetic context in which they are dened.
These different selection methods could be combined by
identifying a subset of the most important genes and targeting
them for direct allele selection, predicting the breeding value
of some portion of the remaining background polygenic
variation with a genomic selection model, and relying on extensive phenotypic evaluations of a selected subset of lines to
make nal decisions on cultivar releases. Note that highquality phenotypic evaluations underlie all three of these aspects of modern breeding.
References
Allard, R.W., 1960. Principles of Plant Breeding. New York: Wiley.
Allard, R.W., 1999. Principles of Plant Breeding, second ed. New York: John Wiley
and Sons.
Beavis, W.D., 1998. QTL analyses: Power, precision, and accuracy. In: Paterson, A.
H. (Ed.), Molecular Dissection of Complex Traits. Boca Raton, FL: CRC Press,
pp. 145162.
Bernardo, R., 1996. Best linear unbiased prediction of maize single-cross
performance. Crop Science 36, 5056.
Bernardo, R., 2008. Molecular markers and selection for complex traits in plants:
Learning from the last 20 years. Crop Science 48, 16491664.
Bernardo, R., Yu, J., 2007. Prospects for genomewide selection for quantitative traits
in maize. Crop Science 47, 10821090.
Blanc, G., Charcosset, A., Mangin, B., Gallais, A., Moreau, L., 2006. Connected
populations for detecting quantitative trait loci and testing for epistasis: An
application in maize. Theoretical and Applied Genetics 113, 206224.
Bonnett, D.G., Rebetzke, G.J., Spielmeyer, W., 2005. Strategies for efcient
implementation of molecular markers in wheat breeding. Molecular Breeding 15,
7585.
199
Huang, X., Zhao, Y., Wei, X., et al., 2012. Genome-wide association study of
owering time and grain yield traits in a worldwide collection of rice germplasm.
Nature Genetics 44, 3239.
Hung, H.-Y., Shannon, L.M., Tian, F., et al., 2012a. ZmCCT and the genetic basis of
day-length adaptation underlying the postdomestication spread of maize.
Proceedings of the National Academy of Sciences of the USA 109,
E1913E1921.
Hung, H.Y., Browne, C., Guill, K., et al., 2012b. The relationship between parental
genetic or phenotypic divergence and progeny variation in the maize nested
association mapping population. Heredity 108, 490499.
Ismail, A.M., Singh, U.S., Singh, S., Dar, M.H., Mackill, D.J., 2013. The
contribution of submergence-tolerant (sub1) rice varieties to food security i
n ood-prone rainfed lowland areas in Asia. Field Crops Research 152,
8393.
Janik, J., 2006. Origins of fruit culture and fruit breeding. In: Lamkey, K.R., Lee, M.
(Eds.), Plant breeding: The Arnel. R. Hallauer International Symposium. Ames,
IA: Blackwell. pp. 269282.
Jansky, S.H., Peloquin, S.J., 2006. Advantages of wild diploid Solanum species over
cultivated diploid relatives in potato breeding programs. Genetic Resources and
Crop Evolution 53, 669674.
Jiang, J., Friebe, B., Gill, B.S., 1993. Recent advances in alien gene transfer in
wheat. Euphytica 73, 199212.
Johannsen, W., 1903. Ueber erblichkeit in populationen und in reinen leinen. Jena:
Gustav Fischer.
Johannsen, W., 1911. The genotype conception of heredity. American Naturalist 45,
129159.
Koziel, M.G., Beland, G.L., Bowman, C., et al., 1993. Field performance of elite
transgenic maize plants expressing an insecticidal protein derived from Bacillus
thuringiensis. Biotechnology 11, 194200.
Kump, K.L., Bradbury, P.J., Buckler, E.S., et al., 2011. Genome-wide association
study of quantitative resistance to southern leaf blight in the maize nested
association mapping population. Nature Genetics 43, 163169.
Larsson, S.J., Lipka, A.E., Buckler, E.S., 2013. Lessons from dwarf8 on the
strengths and weaknesses of structured association mapping. PLoS Genetics 9,
e1003246.
Levings, C.S., Dudley, J.W., 1963. Evaluation of certain mating designs for
estimation of genetic variance in autotetraploid alfalfa. Crop Science 3, 532535.
Lewis, R.S., Kernodle, S.P., 2009. A method for accelerated trait conversion in plant
breeding. Theoretical and Applied Genetics 118, 14991508.
Li, J., Yuan, L., 2010. Hybrid Rice: Genetics, Breeding, and Seed Production Plant
Breeding Reviews. Oxford, UK: John Wiley & Sons, Inc. 15158.
Li, X., Zhu, C., Yeh, C.-T., et al., 2012. Genic and nongenic contributions to natural
variation of quantitative traits in maize. Genome Research 22, 24362444.
Lorenz, A.J., Chao, S.M., Asoro, F.G., et al., 2011. Genomic selection in plant
breeding: Knowledge and prospects. Advances in Agronomy 110, 77123.
Lorenz, A.J., Smith, K.P., Jannink, J.-L., 2012. Potential and optimization of
genomic selection for fusarium head blight resistance in six-row barley. Crop
Science 52, 16091621.
Lorenzana, R.E., Bernardo, R., 2009. Accuracy of genotypic value predictions for
marker-based selection in biparental plant populations. Theoretical and Applied
Genetics 120, 151161.
Lush, J.L., 1940. Intra-sire correlations or regressions of offspring on dam as a
method of estimating heritability of characteristics. Journal of Animal Science 33,
293301.
Lush, J.L., 1945. Animal Breeding Plans, third ed. Ames, IA: Collegiate Press.
Lynch, M., Walsh, B., 1998. Genetics and Analysis of Quantitative Traits.
Sunderland, MA: Sinauer Associates, Inc.
Massman, J.M., Jung, H.-J.G., Bernardo, R., 2013. Genomewide selection versus
marker-assisted recurrent selection to improve grain yield and stover-quality
traits for cellulosic ethanol in maize. Crop Science 53, 5866.
Melchinger, A.E., 1987. Expectation of means and variances of testcrosses produced
from F2 and backcross individuals and their selfed progenies. Heredity 59,
105115.
Melchinger, A.E., Utz, H.F., Schn, C.C., 1998. Quantitative trait locus (QTL)
mapping using different testers and independent population samples in maize
reveal low power of QTL detection and large bias in estimates of QTL effects.
Genetics 149, 383403.
Mendoza, H., Haynes, F., 1974. Genetic basis of heterosis for yield in the
autotetraploid potato. Theoretical and Applied Genetics 45, 2125.
Meuwissen, T.H.E., Hayes, B.J., Goddard, M.E., 2001. Prediction of total genetic
value using genome-wide dense marker maps. Genetics 157, 18191829.
Miedaner, T., Korzun, V., 2012. Marker-assisted selection for disease resistance in
wheat and barley breeding. Phytopathology 102, 560566.
200
Moreau, L., Charcosset, A., Hospital, F., Gallais, A., 1998. Marker-assisted selection
efciency in populations of nite size. Genetics 148, 13531365.
Morrell, P.L., Buckler, E.S., Ross-Ibarra, J., 2012. Crop genomics: Advances and
applications. Nature Review Genetics 13, 8596.
Morris, G.P., Ramu, P., Deshpande, S.P., et al., 2013. Population genomic and
genome-wide association studies of agroclimatic traits in sorghum. Proceedings
of the National Academy of Sciences of the USA 110, 453458.
Myles, S., Peiffer, J., Brown, P.J., et al., 2009. Association mapping: Critical
considerations shift from genotyping to experimental design. Plant Cell 21,
21942202.
Nyquist, W.E., 1991. Estimation of heritability and prediction of selection response
in plant populations. Critical Reviews in Plant Science 10, 235322.
Olukolu, B.A., Negeri, A., Dhawan, R., et al., 2013. A connected set of genes
associated with programmed cell death implicated in controlling the
hypersensitive response in maize. Genetics 193, 609620.
Ortiz, R., Dochez, C., Asiedu, R., Moonan, F., 2006. Breeding vegetatively
propagated crops. In: Lamkey, K.R., Lee, M. (Eds.), Plant breeding: The Arnel
Hallauer International Symposium. Ames, IA: Blackwell, pp. 251268.
Panter, D.M., Allen, F.L., 1995. Using best linear unbiased predictions to
enhance breeding for yield in soybean: I. Choosing parents. Crop Science 35,
397405.
Patterson, H.D., Williams, E.R., 1976. A new class of resolvable incomplete block
designs. Biometrika 63, 8392.
Perlak, F.J., Deaton, R.W., Armstrong, T.A., et al., 1990. Insect resistant cotton
plants. Biotechnology 8, 939943.
Piepho, H.-P., Mohring, J., Melchinger, A.E., Buchse, A., 2008. BLUP for
phenotypic selection in plant breeding and variety testing. Euphytica 161,
209228.
Qiao, C.G., Basford, K.E., DeLacy, I.H., Cooper, M., 2004. Advantage of single-trial
models for response to selection in wheat breeding multi-environment trials.
Theoretical and Applied Genetics 108, 12561264.
Randhawa, H.S., Mutti, J.S., Kidwell, K., et al., 2009. Rapid and targeted
introgression of genes into popular wheat cultivars using marker-assisted
background selection. PLoS One 4, e5752.
Richards, A.J., 1997. Plant Breeding Systems, second ed. UK: Chapman & Hall.
Riedelsheimer, C., Czedik-Eysenberg, A., Grieder, C., et al., 2012. Genomic and
metabolic prediction of complex heterotic traits in hybrid maize. Nature Genetics
44, 217220.
Rober, F., Gordillo, G., Geiger, H., 2005. In vivo haploid induction in maizeperformance of new inducers and signicance of doubled haploid lines in hybrid
breeding. Maydica 50, 275.
Robinson, G.K., 1991. That BLUP is a good thing: The estimation of random effects.
Statistical Science 6, 1551.
Ruiz Corral, J.A., Puga, N.D., Snchez Gonzalez, J.D.J., et al., 2008. Climatic
adaptation and ecological descriptors of 42 Mexican maize races. Crop Science
48, 15021512.
Schnell, F.W., 1983. Probleme der elternwahl-ein berblick. Arbeitstagung der
Arbeitsgemeinschaft der Saatzuchleiter in Gumpenstein 111.
Schn, C.C., Utz, H.F., Groh, S., et al., 2004. Quantitative trait locus mapping based
on resampling in a vast maize testcross experiment and its relevance to
quantitative genetics for complex traits. Genetics 167, 485498.
Sears, E.R., 1969. Wheat cytogenetics. Annual Review of Genetics 3, 451468.
Simmonds, N.W., 1991. Selection for local adaptation in a plant breeding
programme. Theoretical and Applied Genetics 82, 363367.
Simmonds, N.W., 1993. Introgression and incorporation. Strategies for the use of
crop genetic resources. Biological Reviews 68, 539562.
Smith, A.B., Cullis, B.R., Thompson, R., 2005. The analysis of crop cultivar
breeding and evaluation trials: An overview of current mixed model approaches.
Journal of Agricultural Science 143, 114.
Sorrells, M.E., Wilson, W.A., 1997. Direct classication and selection of superior
alleles for crop improvement. Crop Science 37, 691697.
Stebbins, G.L., 1974. Flowering Plants: Evolution Above the Species Level.
Cambridge, MA: Belknap Press.
Tanksley, S.D., McCouch, S.R., 1997. Seed banks and molecular maps: Unlocking
genetic potential from the wild. Science 277, 10631066.
Tester, M., Langridge, P., 2010. Breeding technologies to increase crop production
in a changing world. Science 327, 818822.
Tian, F., Bradbury, P.J., Brown, P.J., et al., 2011. Genome-wide association study of
leaf architecture in the maize nested association mapping population. Nature
Genetics 43, 159162.
Wallace, H.A., Brown, W.L., 1988. Corn and Its Early Fathers. Ames, IA: Iowa State
University Press Rev.
Wang, J., Chapman, S.C., Bonnett, D.G., Rebetzke, G.J., Crouch, J., 2007.
Application of population genetic theory and simulation models to efciently
pyramid multiple genes via marker-assisted selection. Crop Science 47,
582588.
Williams, E., Piepho, H.-P., Whitaker, D., 2011. Augmented p-rep designs.
Biometrical Journal 53, 1927.
Wilson, J.A., 1984. Hybrid Wheat Breeding and Commercial Seed Development
Plant Breeding Reviews. Hoboken, NJ, USA: John Wiley & Sons, Inc. 303319.
Wilson, L.M., Whitt, S.R., Ibaez, A.M., et al., 2004. Dissection of maize kernel
composition and starch production by candidate gene association. Plant Cell 16,
27192733.
Windhausen, V.S., Atlin, G.N., Hickey, J.M., et al., 2012. Effectiveness of genomic
prediction of maize hybrid performance in different breeding populations and
environments. G3: Genes: Genomes: Genetics 2, 14271436.
Wisser, R.J., Kolkman, J.M., Patzoldt, M.E., et al., 2011. Multivariate analysis of
maize disease resistances suggests a pleiotropic genetic basis and implicates a
GST gene. Proceedings of the National Academy of Sciences of the USA 108,
73397344.
Wolnger, R.D., Federer, W.T., Corderobrana, O., 1997. Recovering information in
augmented designs, using SAS PROC GLM and PROC MIXED. Agronomy
Journal 89, 856859.
Wu, K.-K., Ming, R., Moore, P.H., Paterson, A.H., 2006. Sugarcane genomics and
breeding. In: Lamkey, K.R., Lee, M. (Eds.), Plant Breeding: The Arnel R. Hallauer
International Symposium. USA: Blackwell Publishing, pp. 283292.
Xu, S., 2003. Estimating polygenic effects using markers of the entire genome.
Genetics 163, 789801.
Yan, J., Warburton, M., Crouch, J., 2011. Association mapping for enhancing maize
(Zea mays L.) genetic improvement. Crop Science 51, 433449.
Yan, J.B., Kandianis, C.B., Harjes, C.E., et al., 2010. Rare genetic variation at Zea
mays crtrb1 increases beta-carotene in maize grain. Nature Genetics 42,
322327.
Young, N.D., 1999. A cautiously optimistic vision for marker-assisted breeding.
Molecular Breeding 5, 505510.
Young, N.D., Tanksley, S.D., 1989. RFLP analysis of the size of chromosomal
segments retained around the Tm-2 locus of tomato during backcross breeding.
Theoretical and Applied Genetics 77, 353359.
Zhong, S., Dekkers, J.C.M., Fernando, R.L., Jannink, J.-L., 2009. Factors affecting
accuracy from genomic selection in populations derived from multiple inbred
lines: A barley case study. Genetics 182, 355364.
Zhu, C., Gore, M., Buckler, E.S., Yu, J., 2008. Status and prospects of association
mapping in plants. The Plant Genome 1, 520.
Relevant Websites
http://www.cgiar.org/
Consultative Group on International Agricultural Research, which organizes
research conducted at non-prot international research centers.
http://www.ars-grin.gov/
Germplasm collections of USDA, including searchable databases of seed
collections.
http://maswheat.ucdavis.edu
MASwheat collaborative project on marker-assisted selection in wheat, including
technical information on laboratory protocols and outreach and educational
materials for the general public.
http://www.extension.org/plant_breeding_genomics
On-line course materials and short tutorials on specic topics from extension
Foundation, a network of agricultural extension services of USA land-grant
universities.
http://www.plantbreeding.org/napb/
USA National Association of Plant Breeders, includes the plant breeding
newsletter.
C
Changing Structure and Organization of US Agriculture
WJ Armbruster, Farm Foundation, Darien, IL, USA
MC Ahearn, US Department of Agriculture Economic Research Service, Washington, DC, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Beginning farmer Farm operator of a farm on which all
operators have 10 years or less experience in operating
a farm.
Commodity specialization Total value of production
equaling at least 50% from one commodity or related group
of commodities determines a farms commodity
specialization, consistent with the North American Industry
Classication System. Farms that do not have a commodity
or livestock type composed of at least 50% of production
are classied as other crops or other livestock operations.
Contracting Many farmers market their production
through contracts in lieu of open market sales. These
farmers and their buyers agree to arrangements in the
contract signed before harvest (or before the completion
stage for livestock), specifying the terms under which
products are transferred from the farm.
Family farm There is no hard and fast denition of a
family farm in the United States, unlike the farm denition.
The United States Department of Agricultures Economic
Research Service (USDA ERS) denes a family farm as one
in which the majority of the business is owned by the
operator and individuals related to the operator by blood,
marriage, or adoption, including relatives who do not live in
the operator household. The share of US farms classied as
family farms has changed little since 1996, ranging from
97.1% to 98.3% of all farms.
Farm Any place from which US$1000 or more of
agricultural products are sold, or normally would have been
sold, during a year. A point system developed by the USDAs
National Agricultural Statistics Service is used to determine
when a farm normally would have sold US$1000 of
products, in the event they do not do so. This point system
Introduction
This article provides a brief description of general characteristics and changes in production agriculture over time. Key
inuences or drivers of change in structure and organization,
as well as other signicant drivers of change, are discussed.
Detailed measures of farm size and structure are presented and
doi:10.1016/B978-0-444-52512-3.00116-9
201
202
3 000
2 500
2 000
1 500
1 000
0 500
Output
Input
2011
2008
2005
2002
1999
1996
1993
1990
1987
1984
1981
1978
1975
1972
1969
1966
1963
1960
1957
1954
1951
1948
0 000
Figure 1 Indices of farm output, input, and total factor productivity, 19482011. US Department of Agriculture Economic Research Service,
2013a. Agricultural productivity. Available at: http://www.ers.usda.gov/topics/farm-economy/agricultural-productivity.aspx (accessed 07.07.13).
Technology adoption
Increasing size of farms tends to reduce cost of production
because of efciencies in machinery use, cost savings from
purchases of larger quantities of inputs at volume discounts,
Globalization of agriculture
The imports and exports of agricultural and food products tied
to globalization put a premium on efcient farm production
to hold down costs of exports and to keep lower cost imports
from replacing US production. Trade negotiations play
an important role in determining the implications of globalization for US domestic agricultural policy and products.
Progress in removing or reducing tariffs and import quotas
as barriers to trade have facilitated worldwide trade growth
in agricultural and food products. Trade negotiations also establish guidelines for the types of food safety or other requirements countries may impose on product quality
characteristics. It is critical that standards are not established
which are designed primarily to create a barrier to imports
from the United States or other countries, which could
offset productivity efciency as a key determinant of trade
ows. This is increasingly important amid concerns about
food security for the burgeoning world population of poor
consumers and a growing middle class demanding improved
diets.
Consumer preferences
Consumer food preferences and expectations are important
drivers of change in products sold by retailers. Whether they
are also major drivers of change in the size and structure of
farms depends on how they inuence new opportunities or
create challenges for producers. An important preference of
consumers is convenience, as more and more households rely
on two people in the workforce to provide adequate family
income. Food safety is an accompanying concern for consumers who rely on the convenience of food prepared by
others, such as packaged produce that has been handled in
large-volume processing facilities. Foodborne illnesses, especially occurring in fresh produce and in meats, have received
prominent attention in recent years and even partially eroded
203
Agricultural policy
There are a number of production-oriented agricultural policies that provide payment to major commodity producers to
support incomes. They include such programs as direct payments based on historical yields and acreage, countercyclical
payments, loan deciency payments, disaster assistance programs, or payments tied to conservation practices. Changes in
policies over time are surely connected to changes in farming
structure (Sumner et al., 2010), although clear causation is
difcult to establish. For example, empirical evidence suggests
that a share of agricultural program payments are capitalized
into the prices of land, but it is difcult to separately identify
how that might affect farm structure, apart from the key drivers
of structural change (see MacDonald et al. (2013) for a review
of recent literature).
Other agricultural policy measures may encourage or help
to maintain the number of smaller farms. Examples include
programs to foster farmers markets, facilitate purchase of local
foods by participants in food assistance programs, and provide
federal support for production process verication, which may
help smaller producers differentiate their products in the
market. However, smaller farms may need to seek out opportunities to collaborate with others to be able to compete
successfully in markets, even locally. Individually, they may
lack sufcient volume to move much beyond farm stand sales
or any local farmers markets.
204
Input costs
Input costs, which may be affected by factors outside the
control of agriculture, can also be important drivers of changing structure and size of farms. For example, the price of fuel,
fertilizer, and debt nancing are heavily inuenced by factors
outside of the agricultural sector. To the extent that their use
per unit of farm output varies across farm size, these factors
will have an impact on structure. And increases in farm size,
perhaps over a number of scattered parcels, may give the farm
operator more ability to capture volume discounts for products, transportation, and contracted production services.
However, input costs, which they are unable to inuence, may
put small farmers in a more challenging position in terms of
production efciency.
Risk management
As the size of a farm increases, risk management becomes an
evermore challenging element in determining its success or
failure. Diversication of production to provide alternative
sources of income is one element of risk management that has
long been the mainstay of farms from smaller through larger
operations. However, with the increasing specialization in a few
major commodities in many medium- and large-scale farms in
recent years, risk management must be carefully considered in
the decision-making processes. Crop insurance subsidized at
the federal level, and especially utilized by major eld crop
producers that tend to be larger than other farms, is one risk
management tool that has gained in popularity in recent years.
However, research has shown that due to risk-balancing tendencies on the part of a farmer, policies that decrease the variability of farm income could induce farmers to increase their
risks elsewhere, such as through increased nancial risk
(Featherstone et al., 1988). For example, increased nancial
leverage could provide incentives to increased concentration of
production. To what extent insurance will be a mainstay of
future farm programs remains to be seen, as policy constantly
evolves. Many anticipate increased reliance on insurance programs in the future, in part subsidized at the federal level, as
replacing much criticized direct subsidy programs for the major
agricultural commodities.
Tax policy
Tax policy involves a variety of provisions that impact how
rms and households organize their nances so as to minimize their tax burden and therefore can have indirect impacts
on farm structure. For example, tax policy affects the use of
capital in agriculture by the provisions associated with
expensing of capital acquisition in the calculation of taxable
income. The amount of capital costs that can be expensed,
rather than placed on a depreciation schedule, are limited,
depending on the tax year. For example, in 2000 US$20 000
could be expensed and in 2013 US$500 000 could be
expensed. These expensing provisions are especially useful for
large and expanding farms. In 2010, 83% of farms with sales
of US$500 000 or more made a capital investment, although
only 1% of these large farms had capital investments of US
$500 000 or more (Durst et al., 2013).
Tax policy may also inuence structural change by fostering growth in the number of small farms. Although small
farms earn little or nothing in cash income from farming, the
key to understand structural change and small farm survivability is to recognize the importance of the full range of returns to farming. Small farm households generally are full
owners of their farm land and farm land values have historically, and especially recently, risen rapidly, providing owners
with unrealized capital gains (Figure 2). However, farm land
owners generally receive a reduction in their local property
taxes because the land is valued for tax purposes for farm use
rather than market value, reducing their cost of investment
compared with the cost of owning other real estate.
The majority of farm families reside on their farm property,
and therefore many of the expenses associated with the
dwelling are included in farm business expenses. According to
data from the Internal Revenue Service, since 1980 the
aggregate net farm income reported by those that le Schedule
F forms (almost 90% of all farms) has been negative. Approximately three-quarters of all Schedule F lers have
negative net farm income (Durst et al., 2013). At the same
time that farm families may be experiencing rises in the value
of their farm land, paying property taxes based on the
lower farm use value and having the farm business cover
some residential expenses, families with off-farm income
benet from having farm losses that reduce taxes on their
nonfarm income. Moreover, many farm residents most likely
value the so-called psychic income that comes from a rural
lifestyle.
These additional returns to farming were most likely not
considered in 1986 when the US Ofce of Technology Assessment released a report that predicted by the year 2000
there would be 1.2 million farms in the United States. The
report stated:
The projected decline in the number of small farms is dramatic but
plausible, given the strong trend in this direction and the persistently
negative farm income in this class (U.S. Congress, 1986, p. 96).
205
Average U.S. farm real estate value, nominal and real (inflation adjusted), 19692011
2500
2000
1500
1000
500
0
1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 2002 2005 2008 2011
Note: The gross domestic product chain-type price index is used to convert NASS current-dollar
statistics to 2005=100 equivalents (Bureau of Economic Analysis, Dept. of Commerce).
Source: USDA-NASS. Available at: http://usda.mannlib.cornell.edu/MannUsda/view
DocumentInfo.do;jsessionid=F154BA78C7C50C021C8CA924EDB72FD5?documentID=1446
(accessed 29.04.14).
Figure 2 Average US farm real estate value, nominal and real (ination adjusted), 19692011.
206
Table 1
Farms: Number, land in farms, and average farm size, United States, 19852012
Year
Farms (number)
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2 292 530
2 249 820
2 212 960
2 200 940
2 174 520
2 145 820
2 116 760
2 107 840
2 201 590
2 197 690
2 196 400
2 190 500
2 190 510
2 192 330
2 187 280
2 166 780
2 148 630
2 135 360
2 126 860
2 112 970
2 098 690
2 088 790
2 204 950
2 200 100
2 200 210
2 192 000
2 181 630
2 170 000
1 012 073
1 005 333
998 923
994 423
990 723
986 850
981 736
978 503
968 845
965 935
962 515
958 675
956 010
952 080
948 460
945 080
942 070
940 300
936 750
932 260
927 940
925 790
921 460
919 910
919 890
918 840
917 000
914 000
441
447
451
452
456
460
464
464
440
440
438
438
436
434
434
436
438
440
440
441
442
443
418
418
418
419
420
421
Source: Reproduced from United States Department of Agriculture, National Agricultural Statistics Service, 2013. Quick Stats Data Base. Available at: http://www.nass.usda.gov/
Quick_Stats/ (accessed 29.04.14).
Table 2
Total farms
Point farmsb
US$10009999
US$10 00049 999
US$50 00099 999
US$100 000249 999
US$250 000499 999
US$500 000999 999
US$1 000 000 or more
1982
2007
Change
Farms (No.)
Distribution (Pct.)
Farms (No.)
Distribution (Pct.)
19822007
2 240 976
254 097
700 252
601 840
253 243
282 809
97 894
34 650
16 191
100.0
11.3
31.2
26.9
11.3
12.6
4.4
1.5
0.7
2 204 793
688 834
630 327
403 017
125 456
147 500
93 373
60 777
55 509
100.0
31.2
28.6
18.3
5.7
6.7
4.2
2.8
2.5
1.6
171.1
10.0
33.0
50.5
47.8
4.6
75.4
242.8
Table 3
207
All commodities
Meat animals
Dairy products
Poultry/eggs
Miscellaneous livestock
Food grains
Feed crops
Cotton
Tobacco
Oil crops
Vegetables
Fruits/nuts
All other crops
1985
1990
1995
US$1000
188 202 600
44 865 002
19 879 611
19 075 734
3 396 768
10 356 029
24 504 521
6 850 629
2 548 235
15 492 964
14 982 903
11 017 842
15 232 362
2000
2005
2010
Source: Reproduced from U.S. Department of Agriculture Economic Research Service, 2013b. Farm household well-being. Available at: http://www.ers.usda.gov/topics/farm-economy/
farm-household-well-being.aspx (accessed 07.07.13).
incorporated for sound business purposes. Although the Census of Agriculture asks farms that are organized as a corporation
whether or not they consider themselves to be a family corporation, this term does not have a clear denition nor is it a
recognized legal form of organization. Census of Agriculture
data for 1987, 1997, and 2007 (Table 5) shows that sole
proprietors continue to control the lions share of farm numbers, two-thirds of acres of farmland, and approximately half of
total farm sales. Partnerships are next in importance in number
of farms and acres and the third most important in farm sales.
Although the share of farms organized as partnerships has
declined somewhat over the period, the share of their sales has
increased. Family corporations control a small portion of farms
and gradually growing share of acres as well as sales. Other
farms, including nonfamily corporation farms, are a small
share of total numbers (under 2%), control approximately 8%
of farm acreage, and provide approximately 7% of farm sales.
Table 6 shows the number of farms and amount of farmland operated by the tenure status of farms, i.e., fully own all
acres, own part of the acres in the operation, and rent all acres
in the operation. More than two-thirds of farms fully own the
acreage farmed, but they account for less than 40% of acreage
farmed. The share of farms with full ownership increased more
from 1997 to 2007 than the share of acres they operated. This
is consistent with the increasing share of small farms in the
sector over this period, which are more likely than larger farms
to be full owners. The share of full tenant farms decreased
continuously during 19872007. The proportion of land operated by this group of farms has also decreased during that
time. Trends indicate that the experience since 1987 is likely to
be repeated as structure and size of farms continues to evolve,
although the recent historically high rates of increase in the
price of farm land may temper the future share of land owned
versus leased by large farms.
Farm Finances
Although small family farms (with gross sales of less than US
$250 000) produce a relatively small share (18%) of agricultures value of production, they controlled 51% of the
acreage used in agriculture in 2011 (Table 7) and 64% of farm
household assets in 2007 (Hoppe and Banker, 2010). The
acreage and assets controlled by the small-scale family farms
are down signicantly relative to 1990 when they accounted
for the vast majority, as reported by Lins (1994). This shift is
due to increasing numbers of large-scale family farms and their
increased ownership of the acreages farmed compared with the
situation in 1990.
On a cash basis, small farms as a group lose money
farming. The average small farm cannot generate enough net
farm income to support a family farm without outside income
sources. Perhaps not too surprising, as farm size increases so
too do average farm assets and debt. However, even the
smallest farms have large net worth. In 2011, the median net
1 469 952
775 000
2 107 377
1 231 400
204 716
29 090
Financial position
Favorable
Marginal income
Marginal solvency
Vulnerable
74
20
4
2
1 902 660
1 092 821
119 545
37 765
253 003
12
941
26
33
29
46
Cash grain
72
21
5
2
1 066 621
655 486
100 360
4 125
1 166 981
692 698
893 352
530 000
49 538
10 638
65 002
3
417
3
3
6
5
Soybean
67
29
2
2
689 577
382 739
30 685
550
720 262
401 250
620 939
350 000
10 497
968
490 840
23
245
13
7
31
23
60
32
5
3
1 218 242
402 682
126 498
1350
1 344 740
458 475
1 076 490
370 000
110 346
375
146 747
7
125
2
13
2
3
High-value crops
56
39
2
3
Percent
860 653
398 478
54 196
695
914 849
427 250
57
35
6
1
1 958 152
547 818
297 960
64 368
2 256 112
689 944
1 521 780
489 640
134 474
12 525
Dollars
10 799
1 131
714 733
328 400
18 042
1
301
1
6
1
1
Hogs
654 208
30
643
47
15
22
15
Beef cattle
Number of farms
Percent of farms
Farm size (mean operated acres)
Percent of acres
Percent of total value of production
Percent of farms receiving government payments
Percent of government payments
Item
Table 4
54
27
9
10
723 642
424 900
174 549
11 456
898 191
523 028
732 532
408 850
57 473
756
53 046
2
119
1
10
1
1
Poultry
78
12
7
2
1 713 365
953 591
397 588
100 026
2 110 953
1 193 482
1 307 180
760 000
186 755
60 300
53 734
2
386
2
12
4
3
Dairy
45
47
3
5
415 505
235 400
29 169
463
444 674
269 000
361 521
225 000
6399
5539
438 222
20
102
5
2
4
2
General livestock
60
34
3
3
910 727
399 995
81 082
825
991 810
433 394
761 808
342 170
34 324
1 250
2 172 843
100
415
100
100
100
100
All
208
Changing Structure and Organization of US Agriculture
71
55
8
13
23
31
25
4
41
33
22
58
6
11
19
31
34
57
2
81
17
0
7
41
23
30
61
2
6
17
36
38
33
8
38
37
17
7
34
21
38
58
3
12
18
41
27
59
18
17
25
40
9
44
25
22
60
3
10
20
29
37
45
2
25
62
11
7
30
42
21
52
8
21
30
31
10
63
4
59
26
11
11
47
24
18
56
4
10
29
31
25
65
12
27
57
4
24
47
19
11
51
11
17
30
31
12
98
27
59
8
6
11
40
25
24
56
4
12
26
33
25
34
7
25
48
20
Source: Reproduced from USDA Agricultural Resource Management Survey, 2011. Authors calculations based on ARMS data. ARMS is described at: http://www.ers.usda.gov/data-products/arms-farm-nancial-and-crop-production-practices.aspx
(accessed 29.04.14).
3
80
11
6
Farm location
Northeast
Midwest
South
West
9
42
25
25
58
4
10
21
33
32
46
7
37
42
15
210
Table 5
Share of farms, sales, and land, by legal organization,
19872007
Sole proprietor
Farms (%)
1987
1997
2007
Sales (%)
1987
1997
2007
Land (%)
1987
1997
2007
Partnership
Family corp.
Table 6
Number of farms and number of acres, by tenure of farm
operator, 19872007
1987
Other
No.
86.7
86.0
86.5
9.6
8.9
7.9
2.9
4.0
3.9
0.9
1.2
1.7
56.3
52.2
49.6
17.1
18.1
20.9
19.5
23.3
22.1
7.1
6.5
7.3
65.3
62.8
62.3
16.0
16.0
17.5
11.0
12.8
12.4
8.1
8.3
7.8
Off-Farm Income
A major motivation for the establishment of US agricultural
policies in the 1930s was the low incomes of farm families,
relative to nonfarm families the so-called farm problem
(Gardner, 1992). Low incomes among farm families are
largely a situation of the past, due in no small part to the
growth in off-farm income. In 1960, the ratio of farm to US
household income was 0.65, compared with 1.25 in 2011. In
the past two decades, the rate of increase in the average incomes of farm families has surpassed that of the average US
household (Figure 3).
One of the factors contributing to the reversal in the income gap between US and farm households is educational
attainment. Formal education is an especially important factor
not only in the nonfarm job market but also in todays highly
technical farming industry. In the early 1960s, only 4% of
principal farm operators had a 4-year college degree, compared
with 8% of the general US population. By 2011, the college
attainment levels were nearly comparable, 25% for principal
operators compared with 28% for the general population
(Table 8). Moreover, the US population now has a higher
share of the population that has not attained a high school
degree, compared with the farmer population (15% compared
to 9%). The closing educational attainment gap is even more
noteworthy when one considers that the farmer population
has a signicantly older age structure than the general US
population and the educational attainment is higher for
younger people in general.
The importance of off-farm income in maintaining the
large numbers of farms and acreage along with other assets
held by small- and medium-size family farms has been
understood for some time (Ahearn, 1986a, b). Without offfarm income sources to sustain family expenses, many of those
farmers would likely disappear, greatly reducing the number of
Farms
Full owner
Part owner
Tenant
Total
Acres
Full owner
Part owner
Tenant
Total
1997
%
No.
2007
%
No.
1 238 547
609 012
240 200
2 087 759
59
29
12
100
1 146 891
573 839
191 129
1 911 859
60
30
10
100
1 522 033
542 192
140 567
2 204 792
69
25
6
100
33
54
13
100
34
54
12
100
37
54
9
100
Table 7
211
Item
1 255 816
59
1 780 709
3 206 600
639 430
30
934 757
1 671 371
6 538
77 045
54 080
22 965
70 507
All
2 114 668
100
3 075 282
5 520 084
14 623
72 665
51 376
21 289
87 289
Percent
Mean farm income as a percent of total farm household income
9
10
76
4112
55 000
35 433
14 250
52 262
Total assets
Farm assets
Nonfarm assets
Total debt
Farm debt
Nonfarm debt
Total net worth
694 202
428 523
265 679
69 092
20 045
49 047
625 110
Total assets
Farm assets
Nonfarm assets
Total debt
Farm debt
Nonfarm debt
Total net worth
500 427
287 363
184 881
17 061
421
1 500
444 212
Farm income
Off-farm income
Earned income
Unearned income
Total income
1
14
89
17
2 250
53 424
32 500
12 500
57 050
1 131 522
856 589
274 933
120 213
69 387
50 827
1 011 309
672 500
412 300
178 500
34 300
800
250
597 767
100
100
384
74
26
256 434
35
20
9
84
16
320 229
43
50
31
91
9
164 574
22
75
60
78
22
741 237
100
35
100
31
50
19
61
33
6
92
7
0
46
41
13
10
65
25
8
67
24
5
70
25
9
66
25
(Continued )
212
Table 7
Continued
Item
83
17
90
10
90
10
All
86
14
Source: Reproduced from USDA Agricultural Resource Management Survey, 2011. Authors calculations based on ARMS. ARMS is described at: http://www.ers.usda.gov/dataproducts/arms-farm-nancial-and-crop-production-practices.aspx (accessed 29.04.14).
Dollars
Mean US household
60 000
40 000
Median US household
Median farm hosehold
20 000
0
1991
1993
1992
1995
1994
1997
1996
1999
1998
2001
2000
2003
2002
2005
2004
2007
2006
2009
2008
2011
2010
Table 8
Percent of persons by educational attainment, for farm and US population, selected years 19602011
Year
High school
1964
1979
1988
2000
2011
66
34
24
15
9
24
38
42
41
41
1960
1970
1980
1990
2000
2011
59
48
31
25
20
15
25
31
37
30
29
29
Some college
4
9
13
19
25
8
11
17
20
24
28
Source: Reproduced from USDA, Census and ARMS; U.S. Bureau of the Census. The 1964, 1979, and 1988 data for principal farm operators are Census of Ag available at: http://
www.agcensus.usda.gov/index.php. The principal farm operators data for 2000 and 2011 are authors calculations based on ARMS: http://www.ers.usda.gov/data-products/arms-farmnancial-and-crop-production-practices.aspx; and for the US population, the data are from the Census of Population and the Current Population Survey, years available at: http://www.
census.gov/hhes/socdemo/education/ (accessed 29.04.14).
Signicant Trends
A number of trends or issues facing agriculture are most likely
to impact the future structure and organization of the industry.
Some are derived from consumer demand for product characteristics and others are a matter of demographics, whereas
still others are policy driven.
213
214
Table 9
Item
Farm characteristics
Percent of family farms
14
33
40
12
100
43
46
11
255
67
27
6
276
85
14
1
125
83
16
1
179
73
23
4
200
47
27
20
29
27
14
47
33
27
40
20
12
29
100
27
15 651
52
49 686
318 534
7 095
76
84 036
359 236
6 195
75
101 615
428 491
1 304
76
105 909
511 997
1 902
72
89 015
400 273
Note: 1/ Calculation of farm income reects the expenses associated with reported depreciation.
Source: Economic Research Service, USDA, based on USDA Agricultural Resource Management Survey, 2011. Authors calculations based on ARMS. Description of ARMS available
at: http://www.ers.usda.gov/data-products/arms-farm-nancial-and-crop-production-practices.aspx (accessed 29.04.14).
of production from family farms (three-quarters) was produced on farms run by principal operators aged 3564 years
(USDA ERS, 2013b).
For more than two decades, the share of farms operated by
beginning farmers those operating farms on which all operators have 10 years or less experience operating a farm has
been in decline. Beginning farms and ranches account for 22%
of US family farms and ranches, and provide 10% of production on family farms. It is natural to assume that most
beginning farmers are relatively young. Indeed, when compared with the operators of more established farms, beginning
farmers do tend to be younger. The average age of the principal
operators of beginning farms in the US was 49 in 2011,
compared with 60 for established farms. However, only 14%
of beginning farmers were less than age of 35 years in 2011
and just more than half were greater than 50 years (Table 9).
Many of the older beginning farmers who come to farming late
in life operate very small farms and are more likely attracted to
the rural lifestyle that they are able to afford by working at
established careers off the farm. Although easily surpassing the
1% of principal farm operators who were less than 35 years of
age on established farms in 2011, the low share of young
beginning farmers helps to account for the decline in the share
of all farms operated by young farmers in recent decades
(Ahearn, 2013).
Younger beginning farmers tend to operate larger farms
than older operators of beginning farms. In 2011, 11% of
beginning operators less than age of 35 years had gross farm
sales of $250 000 or more, compared with 6% of those aged
3549 years and 1% of those aged 50 years and older. As a
result, young beginning farm households tend to earn more
income on their farm and less off farm than older beginning
farm households. Still, more than half of young beginning
215
Government Payments
Regulations
51
14
22
538
43
449
2 396
390
1 673
17
17
24
17
21
4
18
38
11
365 771
17
8 392
4 786
9 378
5 404
2 578
1 633
15
17
19
35
54
19
25
64
20
292 193
13
17 793
11 369
12 229
Dollars
13 639
7 902
2 961
7
24
12
15
70
20
10
77
17
100 454
5
26 347
19 032
12 992
19 687
13 155
3 331
6
26
10
12
69
26
8
75
20
79 997
4
54 745
41 608
20 727
36 332
23 851
6 255
5
30
13
7
57
31
5
66
24
52 891
2
10 512
8 899
7329
3 687
1 868
1 178
100
16
100
100
21
100
100
35
100
2 172 843
100
All
Source: Reproduced from USDA Agricultural Resource Management Survey, 2011. Authors calculations based on ARMS. ARMS is described at: http://www.ers.usda.gov/data-products/arms-farm-nancial-and-crop-production-practices.aspx (accessed
29.04.14).
2 631
815
3 256
15
5
1
34
20
9
1 281 537
59
oUS$10 000
Number of farms
Percent of farms
Item
Table 10
216
Changing Structure and Organization of US Agriculture
217
interesting dilemmas for long-standing US commodity programs, which in some cases have been challenged in the WTO
and under other trade agreements. Several of those cases have
been lost by the United States and farm programs had to be
adjusted or are still to be brought into alignment with the
decisions required or proposed remedies. In some instances,
the US programs have continued unabated and nes were
paid in lieu of changing the program. In others, adjustments
have been made that resulted in farmers being more exposed
to market price risks. To the extent that future negotiations or
dispute settlements eliminate farm program protections, the
need to manage risks may lead to greater consolidation of
production into larger units more capable of such risk
management.
Future Challenges
The preceding data, trends, and discussion suggest a number of
issues that will affect the future of agricultures structure,
protability, and role in the US and world economies. Some
issues are internal to the agricultural industry, whereas others
are driven by consumer interests and concerns, environmental
factors, and domestic and international trade policies. Managing the challenges of the several risks discussed below cuts
across the range of these issues.
Climate Change
To the extent that scientic expectations about climate change
leading to more variable and severe weather events are accurate,
weather risks faced by producers are more likely to be greater in
coming years. This will provide incentives for producers to
adapt crops they cultivate through adopting improved varieties
designed to better cope with weather events, such as prolonged
drought, excessive moisture, or extreme heat, or even to change
crops produced on their farms. Further, shifts in climatic zones
create the potential for costly pest problems from plant and
animal diseases, invasive weeds, insects, microbes, and fungi
that spread to new geographic areas.
Climate change, along with other challenges discussed here,
will put a premium on risk management at the producer level,
either through insurance programs or through other risk management strategies, such as futures market hedging and crop
diversication. These factors will continue to provide incentives
for growth in size of farming operations to spread the costs of
insurance, hedging, and crop diversication over larger acreages
and output.
Technology
Technology will most likely continue to evolve including
genomics and other branches of biotechnology that will most
likely have major implications for plant and animal breeding
and hence farm size increases are to be expected. New technologies typically are expensive, at least in the early stages
of implementation, and this creates an incentive for farmers
to spread the cost over larger acreages. Although some technologies are truly size neutral, such as genetically modied
218
Food Safety
Supply chains designed to deliver retail-level products with
characteristics that consumers desire have expanded signicantly as an organizational tool in the agricultural and food
industry in recent years. Further processing of most food
products, including even raw produce processed into more
convenient product forms ready for the table or food service
use, makes food safety a constant concern in the food supply
chain. To successfully compete for opportunities in the supply
chains, producers are required to adhere to strict food safety
guidelines incorporated into contracts within the supply chain
for products delivered to the next level. This facilitates traceability from the consumer back to the farm level of any
products that may cause foodborne illness outbreaks. Thus, it
may be expected that more use of HAACP-type programs will
be required of supply chain participants even at the farm level,
and the expense of such systems will be at least in part absorbed by the producers. This will provide further incentives
for growth in farm size to spread the costs involved over larger
amounts of product.
Concluding Comments
The future size and structure of US farms, number of farms and
farmers, and the relative economic prosperity of agriculture
will be determined by the factors identied above and others.
Similar changes are to be anticipated in most developed
countries and in those developing countries with large commercial farming sectors. The next few decades will most likely
see changes that have similar impacts to those experienced
over the past several decades. The exact nature of the changes,
the structural implications, and the opportunities created for
farmers to provide food, feed, ber, and fuel protably will be
determined by market forces, social systems, climatic conditions, environmental and other regulations, and agricultural
and trade policies, among other factors. It will be an exciting
time to be involved in the globally connected agricultural
sector.
Disclaimer
The views expressed here are the authors and do not necessarily represent the views of the USDA.
Globalization
Ongoing growth of emerging market and developing country
demand will create an opportunity for more US exports. It may
also open the door to more imports into the United States
from new production areas designed to serve expanding
markets. Globalization will continue to create challenges, as
witnessed by the current international debate on the acceptance of genetically modied agricultural products. But even
with increased globalization, domestic agricultural policy will
remain a major factor impacting farm size and structure in the
foreseeable future.
The extent to which the US producer thrives from developing market opportunities will depend at least in part on
trade negotiations and the implications for US domestic agricultural policy and products. It will be important that the
United States maintain strong food safety standards for any
References
Ahearn, M., 1986a. The nancial well-being of farm operators and their households.
Agricultural Economic Report No. 563. Washington, DC: USDA ERS.
Ahearn, M., 1986b. An income comparison of farm and nonfarm people. In: New
Dimensions in Rural Policy: Building Upon Our Heritage. Joint Economic
Committee of the U.S. Congress, 99th Congress, 2d Session, S. Washington,
DC: Government Printing Ofce, pp. 99153.
Ahearn, M., 2013. Beginning Farmers and Ranchers at a Glance. Economic Brief.
Washington, DC: USDA ERS.
Alston, J.M., Anderson, M.A., James, J.S., Pardey, P.G., 2010. Persistence Pays:
U.S. Agricultural Productivity Growth and the Benets from Public R&D
Spending. New York: Springer.
Durst, R., Williamson J., Farrigan, T., 2013. The potential impact of tax reform on
farm businesses and rural households. Economic Information Bulletin 107.
Washington, DC: USDA ERS.
Executive Ofce of the President, 2012. Report to the president on agricultural
preparedness and the agricultural research enterprise. Presidents Council of
219
Shields, D., 2010. Federal crop insurance: Background and issues. Congressional
Research Service, R-5700. Available at: http://adriansmith.house.gov/sites/
adriansmith.house.gov/les/CRS%20%20Crop%20Insurance.pdf (accessed
07.07.13).
Sumner, D.A., Alston, J.M., Glauber, J.W., 2010. Evolution of the economics of
agricultural policy. American Journal of Agricultural Economics 92 (2), 403423.
US Department of Agriculture Economic Research Service, 2013a. Agricultural
productivity. Available at: http://www.ers.usda.gov/topics/farm-economy/
agricultural-productivity.aspx (accessed 07.07.13).
US Department of Agriculture Economic Research Service, 2013b. Farm household
well-being. Available at: http://www.ers.usda.gov/topics/farm-economy/farmhousehold-well-being.aspx (accessed 07.07.13).
US Department of Agriculture Economic Research Service, 2013c. Farm sector
income and nances. Available at: http://www.ers.usda.gov/topics/farm-economy/
farm-sector-income-nances.aspx (accessed 07.07.13).
US Department of Agriculture National Agricultural Statistics Service, 2009. 2007
Census of Agriculture: United States Summary and State Data, vol. 1, part 51.
Washington, DC: USDA NASS.
United States Bureau of Labor Statistics, 2013. Quarterly Census of Employment and
Wages. Available at: http://www.bls.gov/cew/
United States Congress Ofce of Technology Assessment, 1986. Technology, Public
Policy, and The Changing Structure of American Agriculture. OTA-F285.
Washington, DC: Government Printing Ofce.
Relevant Websites
http://www.ers.usda.gov
US Department of Agriculture Economic Research Service.
http://www.nass.usda.gov
US Department of Agriculture National Agricultural Statistics Service.
Glossary
Adaptation Adjustment to changing conditions (including
climate change); can refer to adjustment during the lifetime
of an organism or system or to cross-generational genetic
changes.
Additionality The environmental impact, for example,
emission reduction, achieved in comparison to a business
as usual development pathway.
Agriculture, Forestry and Other Land Uses
(AFOLU) Intergovernmental Panel on Climate Change
guidelines for accounting of land-based greenhouse gas
emissions (successor to the land use, land-use change, and
forestry guidelines, but not yet formally accepted by United
Nations framework convention on climate change
(UNFCCC)).
Clean Development Mechanism Part of the Kyoto accord
of the UNFCCC
Introduction
Perspectives on agricultural mitigation have evolved from the
rst report of the Intergovernmental Panel on Climate Change
(IPCC) (Sauerbeck, 1993), through the second (Cole et al.,
1996; Paustian et al., 1997), third, and fourth (Metz et al.,
2007; Smith et al., 2008) to current discourse (Ericksen, 2008;
Beddington et al., 2012; Burney et al., 2010; Vermeulen et al.,
2012; Baker et al., 2012; Neufeldt et al., 2013). There has been
(1) a renement of numbers on current emissions and their
sources, with agriculture currently responsible for 11% of
global emissions (UNEP, 2013), (2) more integration in
scenario modeling than cross sectoral borders (Golub et al.,
2009), (3) responses to some of the accounting system
anomalies that allowed global emission displacement around
biofuels to be counted as emission reduction, (4) separate
efforts to deal with forestry emissions under the REDD
(efforts to reduce emissions from deforestation and forest
degradation) agenda that showed the challenges of a partial
approach in what is an integrated landscape (van Noordwijk
et al., 2013), and (5) a greater appreciation of action opportunities on the demand side of the equation. Part of the food
system industry is responding to consumer action and demand
for low-carbon-footprint products, whereas formal governance
systems and international negotiation arenas are slow to respond effectively. Current global greenhouse gas (GHG)
emission levels are already considerably higher than would be
allowed in 2020 in scenarios that keep global warming below
a 2 1C target (UNEP, 2013). Experiments with carbon markets
have captured the imagination beyond actual performance,
but there certainly are considerable opportunities to reduce net
GHG emissions while meeting rising global demands, compared to a business as usual extrapolation of past trends. The
challenge is how to provide economic incentives for clean
220
doi:10.1016/B978-0-444-52512-3.00002-4
miti forest. It has obtained a specic meaning in the international climate change discourse: it has become shorthand for
reducing the net emissions of GHGs to the atmosphere that are
seen as the primary drivers of global climate change, because
such climate change is considered a risk for humanity and the
future of planet Earth as known. Mitigation was dened as the
primary line of defense in the chain of events (Figure 1) that
caused a reduced quality of life due to the human activities that
induce an increase of atmospheric concentrations of GHGs. The
atmospheric concentration of GHG's, net result of emissions
and uptake by oceans and terrestrial systems, together with solar
irradiation, reection (albedo), and hydrological cycle shape
the climate system; the current rate of change will soon bring
us beyond the safe planetary boundaries of our coping range
(Rockstrom et al., 2009). This will lead to direct human vulnerability and to indirect effects on human welfare through
ecosystem changes. Adaptation is a second line of defense,
which reduces vulnerability in the face of exposure to change,
but which implies a failure of the UNFCCC to achieve its
primary target. Adaptation shifts the concept of what is dangerous, but does not reduce interference with the climate
system. Nor can it deal with the risks of run-away, positive
feedback loops such as changes in ocean current systems,
inducing further change once thresholds are crossed. One
does not know exactly where those thresholds are, so the
precautionary principle should be applied (Ramanathan and
Feng, 2008; Rockstrom et al., 2009). Early warning signs of real
change have been around for at least two decades (Smith et al.,
2009). Synergy between mitigation and adaptation is feasible
in land use (Verchot et al., 2007; Smith and Olesen, 2010).
Exogenous
variabiliy
Atmospheric concentrations of
short- and long-lived
greenhouse gasses
Human actions
Climate
systems
Impacts of actual
and predicted
climate change on
human and
ecosystems
Ot
effe her p
cts oten
o
t
sys n clim ial
tem
ate
s
Mitigation
Anthropogenic
GHG emissions
Atmosphere
Adaptation
Human quality of life
Vulnerability
221
1
222
responsibility for emissions embodied in trade among producers and consumers could, in their view, facilitate international agreement on global climate policy agreements
now hindered by concerns over the regional and historical
inequity of emissions. The emissions embodied in trade
concept also applies to agriculture and associated global
trade ows (Minang et al., 2010). For example, local nutrient
cycles became global nutrient ows (van Noordwijk, 1999),
with continued dependence on new inputs and associated
GHG emissions.
Footprint Accounting
In the face of the failure of the nation states to achieve convincing collective action at par with the challenge, a global
citizen-based approach has emerged with attention on the
footprint of all goods and services that they use for their
lifestyles and diets (Pandey et al., 2011; Peters, 2010). This
follows from a simple disaggregation of the citizen based accounting system:
f j EGHG,j f s m Ps Lm,s Fm
2
the ber supply systems with textile, paper, and other applications that also have fossil fuelbased alternatives. Jointly the
two are still the primary source of energy for a large share of the
rural population, with options to substitute rewood, charcoal,
and dried-manure by fossil fuel use. On the other side of the
spectrum, agriculture- and forestry-based biofuels resubstitute
for fossil fuel. Emission reduction in one sector can be
achieved by shifting product ows and associated emissions to
another sector, without decreasing the anthropogenic interference with the climate systems. The sectoral map of the world
has dotted lines as boundaries (Figure 2). Rigidity of concepts
such as an agriculture concept that does not allow overlap with
forestry, as in Food and Agriculture Organization databases, is
thus seriously challenged to deal with trees outside forest and
agroforestry as intermediate land use system (de Foresta et al.,
2013). Rigidity implies considerable cost to the rationality of
decisions based on them.
Multiple Perspectives
Compared to the discussions on Mitigation in Agriculture in
the rst IPCC report (Sauerbeck, 1993), the current discourse
(Beddington et al., 2012) has brought greater recognition for
the demand side, with attention to waste and lifestyle choices
of human diets. It also acknowledges that there are planetary
boundaries to ambitions for all to emulate the American
dream and diet. Thus the current debate encompasses multiple
aspects, accounting principles, and outstanding issues of
agriculture (Table 1).
There may be a general trend to move from an area-based
emissions per unit of agricultural land, to efciency/footprintbased concepts (emissions per unit end-user satisfaction with
goods and services), but these still have an area-based component in the calculation. Consequently, it requires productivity data. A concept of indirect land use change that has
emerged in the biofuel debate (Plevin et al., 2010) applies to
any new or existing crop and is a challenging one. To what
degree can a new use of a crop be held accountable for the
additional conversion of land into agriculture elsewhere in the
world? Will the new use have left some of the original demand
unmet? Is every parcel of land that once supplied a product for
a certain type of use bound to keep going that forever? With
such concepts we appear to be trapped in the rigidity of articial accounting concepts and need to go back to the basics of
the totality of anthropogenic interference with climate systems.
All this leads to a hot debate about the optimum level of
intensity of land use, in the face of the nonlinear relationship
between inputs, emissions, and yield per unit area (Dor et al.,
2011; Jackson et al., 2010, 2012; Matson et al., 2012). As intensication inuences various aspects of the accounting system, optimization from a GHG perspective can only be done
at national aggregated level. In terms of GHG accountability, a
focus on imports rather than local food production is a very
attractive choice at national level similar to the transfer of
high-emission industries to countries without emission reduction commitments. However, from an atmospheric impacts perspective, focus should be on reducing the total of net
GHG emissions directly or indirectly associated with the sum
total of global agricultural production.
Geological
eposits
Oceans
Waste
Wetlands
recycling
systems
Food supply
Ag. inputs
ply systems
energy sup-
Agricultural
land use
Renewable
Planetary
skin
Net
oceanic
C sink
N2O
and
CH4
Change in terrestrial
carbon stocks
Other
land uses
223
Climate
systems
Rural+Urban systems
Atmosphere
Figure 2 Agriculture as part of the anthropogenic GHG emissions: It relates not only to an important part of land use (interfacing with forests,
wetlands, and oceans as basis for food supply systems, as well as energy supply systems), but also with direct energy consumption for
agricultural inputs and transport, and with (missed opportunities) for waste recycling; ultimately agriculture responds to the shifts in demand, that
are based on human population size multiplied with the goods and services required for lifestyles and diets, modied by the footprints per unit
good and services.
224
Table 1
Perspective on agriculture
Accounting principle
Challenges
Livestock
Livestock is accountable for emissions both through the way
feed is produced with consequences for changes in C stocks
and N2O emissions and though methane emissions at the
animal level that depend on feed quality (IPCC, 2006; Herrero
et al., 2009, 2010). In the context of global land cover data, the
handling of the transition from grazed dry forest to wooded
savanna and to rangeland with trees is a challenge for consistency: with seminomadic and transhumance livestock systems being more easily accounted per head than per area
grazed. Deforestation in the humid forest zone of Latin
America has been historically dominated by extensive livestock
production, whereas in Africa Trypanomosiasis prevented similar livestock systems, whereas in Asia the regional supply/
demand situation did not make such conversion attractive.
Rice Paddies
Methane emissions by cultivated paddies or natural wetlands
is the net result of methane production in the anaerobic zones
of submerged soils by methanogens, and its oxidation into
CO2 by methanotrophs in the aerobic zones of wetland soils
and in upland soils (Le Mer and Roger, 2001). Net methane
emissions can be approximately 10 mg CH4 m2 h1, whereas
methane oxidation by aerobic upland soils (forests are most
active) is two orders of magnitude less. Submersion and organic matter addition increase methane emissions. Intermittent drainage and utilization of the sulfate forms of
N-fertilizers reduce CH4 emission (Le Mer and Roger, 2001).
Conversely, the methane oxidation potential of upland soils is
reduced by cultivation, especially by ammonium N-fertilizer
application.
Peatland Use
Globally, peatlands store more than half of total soil carbon.
Both in the northern temperate and tropical zones peatlands
are in agricultural use, with annual emissions per unit area that
are a factor 100 or more above those on mineral soils. Peatland emissions derive from the use of re in land clearing, the
increased decomposition due to drainage and fertilization.
Together these make the organic residues that took thousands
of years to accumulate disappear in one or a few decades.
225
Where natural and disturbed wetlands and peats emit methane, methane oxidizers become effective once the water
table is below 30 cm of the soil surface. Conversion of tropical
peatland for plantation crops such as oil palm has become a
major issue Agus et al. (2013).
226
227
Closing Remarks
There is a probability that current efforts to achieve mitigation
have actually made things worse. Franks and Hadingham
(2012) gave examples how a farm-focused effort at emission
reduction in selected countries can lead to increases rather
than decreases of global emissions. Henders and Ostwald
(2012) in their overview of leakage in a forest context, also
included relations with agricultural land use. Two decades of
international climate negotiations to effectively implement the
agreed framework convention, dealing with the additionality
and leakage issues, have made very little progress. There may
be some progress in bridging current debates on REDD and
Nationally Appropriate Mitigation Actions in developing
countries, but we are far from a Reducing Emissions from All
Land Uses ideal.
The dominant focus of the UNFCCC framing of the climate
problem on GHG emissions is under scrutiny, with consequences for the way mitigation is perceived, especially in the
land use sector. Firstly, there is growing recognition of the
Faustian choice that derives from the net effect of air pollution
on a global cooling, masking 50% of the committed GHG
warming from the Industrial Revolution (Unger, 2012).
Aligned with that view, is the enhanced visibility of global
climate change after industrial sulfur dioxide emissions were
reduced. Aggressive reduction of air pollutants, including ne
particulate matter from biomass burning that causes haze,
would increase climate warming (Jacobson, 2004; Lamarque
et al., 2010). Within the air pollutants, however, methane
through its effect on ozone decay (Fiore et al., 2008), is a
candidate for selective reductions in warming air pollutants,
which may provide a way to mitigate near-term warming by
complete pollution control until CO2 reductions take effect
(Unger, 2012). Worldwide implementation of current CH4
emission control technologies in waste management, agriculture, and the extraction and transport of fossil fuels by 2030
would lead to a reduction in anthropogenic CH4 emissions of
24% (relative to 2010 levels) and decrease the global mean
warming by an estimated central range of 0.20.4 1C relative
to a business-as-usual scenario (Unger, 2012).
228
Table 2
Accounting principle
Additionality
Leakage
Area-based (Annex-I
countries)
As international agreements
do not yet include the
land use sector, leakage
is not a big risk
Area-based (outside of
Annex-I countries)
Product-based (footprint
and efciency criteria)
Abbreviations: A/R-CDM, afforestation and reforestation as part of the clean development mechanism; REDD+, efforts to reduce emissions from deforestation and forest degradation;
VCS, voluntary carbon schemes.
References
Aertsens, J., De Nocker, L., Gobin, A., 2013. Valuing the carbon sequestration
potential for European agriculture. Land Use Policy 31 (2013), 584594.
Agus, F., Henson, I.E., Sahardjo, B.H., et al., 2013. Review of emission factors for
assessment of CO2 emission from land use change to oil palm in Southeast
Asia. In Killeen, T.J., Goon, J. (Eds.) Reports from the Technical Panels of the
Second Greenhouse Gas Working Group of the Roundtable for Sustainable Palm
Oil (RSPO). Kuala Lumpur: RSPO, pp. 727.
Baker, J.S., Murray, B.C., McCarl, B.A., Feng, S., Johansson, R., 2012. Implications
of alternative agricultural productivity growth assumptions on land management,
greenhouse gas emissions, and mitigation potential. American Journal of
Agricultural Economics. Available at: http://ajae.oxfordjournals.org/content/early/
2012/12/16/ajae.aas114.extract (accessed 05.12.13). doi:10.1093/ajae/aas114.
Bayala, J., Heng, L.K., van Noordwijk, M., Ouedraogo, S.J., 2008. Hydraulic
redistribution study in two native tree species of agroforestry parklands of West
African dry savanna. Acta Oecologica 34, 370378.
Beddington, J., Asaduzzaman, M., Clark, M., et al., 2012. Achieving Food Security
in the Face of Climate Change: Final Report from the Commission on
Sustainable Agriculture and Climate Change. Copenhagen: CGIAR Research
Program on Climate Change, Agriculture and Food Security (CCAFS). Available
at: http://ccafs.cgiar.org/commission/reports (accessed 05.12.13).
Burney, J.A., Davis, S.J., Lobell, D.B., 2010. Greenhouse gas mitigation by
agricultural intensication. Proceedings of the National Academy of Sciences of
the USA 107, 1205212057.
Cao, Q., Cui, Z., Chen, X., et al., 2012. Quantifying spatial variability of indigenous
nitrogen supply for precision nitrogen management in small scale farming.
Precision Agriculture 13 (1), 4561.
Cole, V., Cerri, C., Minami, K., et al., 1996. Agricultural options for mitigation of
greenhouse gas emissions. In: Watson, R.T., Zinyowera, M.C., Moss, R.H. (Eds.),
Climate Change 1995: Impacts, Adaptations and Mitigation of Climate Change.
Cambridge: Cambridge University Press, pp. 745771. Scientic-Technical
Analyses.
Crutzen, P.J., Mosier, A.R., Smith, K.A., Winiwarter, W., 2008. N2O release from
agro-biofuel production negates global warming reduction by replacing fossil
fuels. Atmospheric Chemistry and Physics 8, 389395.
Davis, S.C., Boddey, R.M., Alves, B.J.R., et al., 2013. Management swing potential
for bioenergy crops. GCB Bioenergy. doi:10.1111/gcbb.12042.
Davis, S.J., Caldeira, K., 2010. Consumption-based accounting of CO2 emissions.
Proceedings of the National Academy of Sciences of the USA 107 (12),
56875692.
Dor, T., Makowski, D., Malzieux, E., et al., 2011. Facing up to the paradigm of
ecological intensication in agronomy: Revisiting methods, concepts and
knowledge. European Journal of Agronomy 34 (4), 197210.
Ericksen, P.J., 2008. Conceptualizing food systems for global environmental change
research. Global Environmental Change: Human and Policy Dimensions 18,
234245.
Fiore, A.M., West, J.J., Horowitz, L.W., Naik, V., Schwarzkopf, M.D., 2008.
Characterizing the tropospheric ozone response to methane emission controls
and the benets to climate and air quality. Journal of Geophysical Research 113,
D08307. doi:10.1029/2007JD009162.
de Foresta, H., Somarriba, E., Temu, A., et al., 2013. Towards the assessment
of trees outside forests. Resources Assessment Working Paper 183.
Rome: FAO.
Franks, J.R., Hadingham, B., 2012. Reducing greenhouse gas emissions from
agriculture: Avoiding trivial solutions to a global problem. Land Use Policy 29,
727736.
Gebbers, R., Adamchuk, V.I., 2010. Precision agriculture and food security. Science
327 (5967), 828831.
Gibbs, H.K., Ruesch, A.S., Achard, F., et al., 2010. Tropical forests were the primary
sources of new agricultural land in the 1980s and 1990s. Proceedings of the
National Academy of Sciences of the USA 107, 1673216737.
Giller, K.E., Rowe, E.C., de Ridder, N., van Keulen, H., 2006. Resource use
dynamics and interactions in the tropics: Scaling up in space and time.
Agricultural Systems 88 (1), 827.
Golub, A., Hertel, T., Lee, H.L., Rose, S., Sohngen, B., 2009. The opportunity cost
of land use and the global potential for greenhouse gas mitigation in agriculture
and forestry. Resource and Energy Economics 31 (4), 299319.
Granier, C., Bessagnet, B., Bond, T., et al., 2011. Evolution of anthropogenic and
biomass burning emissions of air pollutants at global and regional scales during
the 19802010 period. Climatic Change 109, 163190.
Green, S.M., 2013. Ebullition of methane from rice paddies: The importance of
furthering understanding. Plant and Soil 370, I31I34.
Hairiah, K., Dewi, S., Agus, F., et al., 2011. Measuring carbon stocks across
land use systems: A manual. Bogor: World Agroforestry Centre ICRAF,
154 pp.
Henders, S., Ostwald, M., 2012. Forest carbon leakage quantication methods and
their suitability for assessing leakage in REDD. Forests 2012 (3), 3358.
doi:10.3390/f3010033.
Herrero, M., Thornton, P.K., Gerber, P., Reid, R.S., 2009. Livestock, livelihoods and
the environment: Understanding the trade-offs. Current Opinion in Environmental
Sustainability 1, 111120.
229
Herrero, M., Thornton, P.K., Notenbaert, A.M., et al., 2010. Smart investments in
sustainable food production: Revisiting mixed crop-livestock systems. Science
327 (5967), 822825.
Hillier, J., Brentrup, F., Wattenbach, M., et al., 2012. Which cropland greenhouse
gas mitigation options give the greatest benets in different world regions?
Climate and soil-specic predictions from integrated empirical models. Global
Change Biology 18 (6), 18801894.
Iiyama, M., Newman, D., Munster, C., et al., 2012. Productivity of Jatropha curcas
under smallholder farm conditions in Kenya agroforestry systems. Agroforestry
Systems 87 (4), 729746.
IPCC, 2006. 4: Agriculture, Forestry and Other Land Uses (AFOLU). 2006 IPCC
Guidelines for National Greenhouse Gas Inventories. Hayama: IPCC/IGES.
Jackson, L.E., van Noordwijk, M., Bengtsson, J., et al., 2010. Biodiversity and
agricultural sustainagility: From assessment to adaptive management. Current
Opinion in Environmental Sustainability 2, 8087.
Jackson, L.E., Pulleman, M.M., Brussaard, L., et al., 2012. Social-ecological and
regional adaptation of agrobiodiversity management across a global set of
research regions. Global Environmental Change 22, 623639.
Jacobson, M.Z., 2004. The short-term cooling but long-term global warming due to
biomass burning. Journal of Climate 17, 29092926.
Kahrl, F., Li, Y., Su, Y., et al., 2010. Greenhouse gas emissions from nitrogen
fertilizer use in China. Environmental Science and Policy 13, 688694.
Lamarque, J.F., Bond, T.C., Eyring, V., et al., 2010. Historical (18502000) gridded
anthropogenic and biomass burning emissions of reactive gases and aerosols:
Methodology and application. Atmospheric Chemistry and Physics 10,
70177039.
Lambin, E.F., 2012. Global Land Availability: Malthus Versus Ricardo. Global Food
Security. Available online 29 November 2012. Available at: http://www.
sciencedirect.com/science/article/pii/S2211912412000235 (accessed 29.04.14).
Le Mer, J., Roger, P., 2001. Production, oxidation, emission and consumption of
methane by soils: A review. European Journal of Soil Biology 37 (1), 2550.
Leakey, R.R.B., 2012. Living with the Trees of Life Towards the Transformation of
Tropical Agriculture. Wallingford: CABI, 200 pp.
Lusiana, B., van Noordwijk, M., Cadisch, G., 2012. Land sparing or sharing?
Exploring livestock fodder options in combination with land use zoning and
consequences for livelihoods and net carbon stocks using the FALLOW model.
Agriculture, Ecosystems and Environment 159, 145160.
Mahowald, N., Ward, D.S., Kloster, S., et al., 2011. Aerosol impacts on climate and
biogeochemistry. Annual Review of Environment and Resources 36, 4574.
Matson, P., Naylor, R., Ortiz-Monasterio, I., 2012. Looking for win-wins in intensive
agriculture. In: Matson, P. (Ed.), Seeds of Sustainability. Washington, DC: Island
Press/Center for Resource Economics, pp. 3145.
Mbow, C., Neufeldt, H., Van Noordwijk, M., et al., 2014. Agroforestry solutions to
address climate change and food security challenges in Africa. Current Opinion
in Environmental Sustainability 6, 6167.
Metz, B., Davidson, O.R., Bosch, P.R., Dave, R., Meyer, L.A., 2007. Climate change
2007: Mitigation of climate change. Contribution of Working Group III to the
Fourth Assessment Report of the Intergovernmental Panel on Climate Change.
Cambridge/New York, NY: Cambridge University Press.
Meyfroidt, P., Lambin, E.F., 2009. Forest transition in Vietnam and displacement of
deforestation abroad. Proceedings of the National Academy of Sciences of the
USA 106, 1613916144.
Meyfroidt, P., Lambin, E.F., 2011. Global forest transition: Prospects for an end to
deforestation. Annual Review of Environment and Resources 36, 343371.
van Middelaar, C.E., Cederberg, C., Vellinga, T.V., van der Werf, H.M., de Boer, I.J.,
2013. Exploring variability in methods and data sensitivity in carbon footprints of
feed ingredients. International Journal of Life Cycle Assessment 18, 768782.
Milne, E., Neufeldt, H., Rosenstock, T., et al., 2013. Methods for the quantication
of GHG emissions at the landscape level for developing countries in smallholder
contexts. Environmental Research Letters 8 (1), 015019.
Minang, P.A., van Noordwijk, M., Meyfroidt, P., Agus, F., Dewi, S., 2010. Emissions
Embodied in Trade (EET) and Land Use in Tropical Forest Margins. ASB Policy
Brief 17. Nairobi: ASB Partnership for the Tropical Forest Margins. Available at:
www.asb.cgiar.org (accessed 30.03.13).
Minasny, B., Sulaeman, Y., McBratney, A.B., 2011. Is soil carbon disappearing? The
dynamics of soil organic carbon in Java. Global Change Biology 17, 19171924.
Mosier, A., Kroeze, C., Nevison, C., et al., 1998. Closing the global N2O budget:
Nitrous oxide emissions through the agricultural nitrogen cycle. Nutrient Cycling
in Agroecosystems 52 (23), 225248.
Mulia, R., Widayati, A., Agung, P., Zulkarnain, M.T., 2013. Low carbon emission
development strategies for Jambi, Indonesia: Simulation and trade-off analysis
using the FALLOW model. Mitigation and Adaptation Strategies for Global
Change. doi:10.1007/s11027-013-9485-8.
230
Nelson, G.C., Rosegrant, M.W., Palazzo, A., et al., 2010. Food Security, Farming,
and Climate Change to 2050: Scenarios, Results, Policy Options. Washington,
DC: International Food Policy Research Institute.
Neufeldt, H., Adhya, T.K., Coulibaly, J.Y., Kissinger, G., Pan, G., 2013. Bridging the
gap I: Policies for reducing emissions from agriculture. UNEP, The Emissions
Gap Report 2013. Nairobi: UNEP, pp. 2328.
Van Noordwijk, M., 1999. Nutrient cycling in ecosystems versus nutrient budgets of
agricultural systems. In: Smaling, E.M.A., Oenema, O., Fresco, L.O. (Eds.),
Nutrient Disequilibria in Agro-Ecosystems: Concepts and Case Studies.
Wallingford: CAB International, pp. 126.
van Noordwijk, M., Agus, F., Dewi, S., et al., 2013. Reducing emissions from land
use in Indonesia: Motivation, policy instruments and expected funding streams.
Mitigation and Adaptation Strategies for Global Change. doi:10.1007/s11027013-9502-y.
van Noordwijk, M., Bayala, J., Hairiah, K., et al., 2014c. Agroforestry solutions for
buffering climate variability and adapting to change. In: Fuhrer, J., Gregory, P.J.
(Eds.), Climate Change Impact and Adaptation in Agricultural Systems.
Wallingford: CAB International.
Van Noordwijk, M., Cadisch, G., 2002. Access and excess problems in plant
nutrition. Plant and Soil 247, 2539.
van Noordwijk, M., Goverse, T., Ballabio, C., et al., 2014b. Soil Organic Carbon
Transition Curves: Reversal of Land Degradation through Management of Soil
Organic Matter for Multiple Benets. SCOPE Review of Multiple Benets of Soil
Organic Carbon. Wallingford: CAB International.
van Noordwijk, M., Hoang, M.H., Neufeldt, H., born, I., Yatich, T. (Eds.), 2011.
How Trees and People can Co-adapt to Climate Change: Reducing Vulnerability
through Multifunctional Agroforestry Landscapes. Nairobi: World Agroforestry
Centre (ICRAF).
van Noordwijk, M., Leimona, B., Jindal, R., et al., 2012. Efcient and fair incentives
for supporting landscape-level environmental services: Evolving practice and
paradigms of Payments for Ecosystem Services. Annual Review of Environment
and Resources 37, 389420.
Van Noordwijk, M., Lusiana, B., 2013. Re-assessing oxygen supply and air quality
(ROSAQ). In: van Noordwijk, M., Lusiana, B., Leimona, B., Dewi, S., Wulandari,
D. (Eds.), Negotiation-Support Toolkit for Learning Landscapes. Bogor: World
Agroforestry Centre (ICRAF) Southeast Asia Regional Program, pp. 153156.
van Noordwijk, M., Namirembe, S., Catacutan, D., Williamson, D., Gebrekirstos, A.,
2014a. Pricing rainbow, green, blue and grey water: Tree cover and geopolitics
of climatic teleconnections. Current Opinion in Environmental Sustainability 6,
4147.
Van Noordwijk, M., Wadman, W., 1992. Effects of spatial variability of nitrogen
supply on environmentally acceptable nitrogen fertilizer application rates to arable
crops. Netherlands Journal of Agricultural Science 40, 5172.
Pandey, D., Agrawal, M., Pandey, J.S., 2011. Carbon footprint: Current methods of
estimation. Environmental Monitoring and Assessment 178, 135160.
Partt, J., Barthel, M., Macnaughton, S., 2010. Food waste within food supply
chains: Quantication and potential for change to 2050. Philosophical
Transactions of the Royal Society B 365, 30653081.
Paustian, K., Andrn, O., Janzen, H.H., et al., 1997. Agricultural soils as a sink to
mitigate CO2 emissions. Soil Use and Management 13, 230244.
Peters, G.P., 2010. Carbon footprints and embodied carbon at multiple scales.
Current Opinion in Environmental Sustainability 2, 245250.
Peters, G.P., Minx, J.C., Weber, C.L., Edenhofer, O., 2011. Growth in emission
transfers via international trade from 1990 to 2008. Proceedings of the National
Academy of Sciences the USA 108, 89038908.
Pielke, R.A., Adegoke, J.O., Chase, T.N., et al., 2007. A new paradigm for assessing
the role of agriculture in the climate system and in climate change. Agricultural
and Forest Meteorology 142, 234254.
Plevin, R.J., Jones, A.D., Torn, M.S., Gibbs, H.K., 2010. Greenhouse gas emissions
from biofuels indirect land use change are uncertain but may be much greater
than previously estimated. Environmental Science and Technology 44,
80158021.
Powlson, D.S., Whitmore, A.P., Goulding, K.W.T., 2011. Soil carbon sequestration to
mitigate climate change: A critical re-examination to identify the true and the
false. European Journal of Soil Science 62, 4255.
Ramanathan, V., Feng, Y., 2008. On avoiding dangerous anthropogenic interference
with the climate system: Formidable challenges ahead. Proceedings of the
National Academy of Sciences of the USA 105, 1424514250.
Reay, D.S., Davidson, E.A., Smith, K.A., et al., 2012. Global agriculture and nitrous
oxide I. Nature Climate Change 2 (6), 410416.
Rizzo, A., Boano, F., Revelli, R., Ridol, L., 2013. Role of water ow in modeling
methane emissions from ooded paddy soils. Advances in Water Resources 52,
261274.
Rockstrom, J., Steffen, W., Noone, K., et al., 2009. A safe operating space for
humanity. Nature 461, 472475.
Rudel, T.K., Schneider, L., Uriarte, M., et al., 2009. Agricultural intensication and
changes in cultivated areas, 19702005. Proceedings of the National Academy
of Sciences of the USA 106, 2067520680.
Sauerbeck, D., 1993. CO2 emissions from agriculture: Sources and mitigation
potentials. Water, Air, and Soil Pollution 70, 381388.
Shindell, D., Kuylenstierna, J.C.I., Vignati, E., et al., 2012. Simultaneously mitigating
near-term climate change and improving human health and food security.
Science 335, 183189.
Smith, J.B., Schneider, S.H., Oppenheimer, M., et al., 2009. Assessing dangerous
climate change through an update of the Intergovernmental Panel on Climate
Change (IPCC) reasons for concern. Proceedings of the National Academy of
Sciences of the USA 106, 41334137.
Smith, P., Martino, D., Cai, Z., et al., 2008. Greenhouse gas mitigation in
agriculture. Philosophical Transactions of the Royal Society 363,
789813.
Smith, P., Olesen, J.E., 2010. Synergies between the mitigation of, and adaptation
to, climate change in agriculture. Journal of Agricultural Science 148 (5),
543552.
Stockmann, U., Adams, M.A., Crawford, J.W., et al., 2013. The knowns, known
unknowns and unknowns of sequestration of soil organic carbon. Agriculture,
Ecosystems and Environment 164, 8099.
Tata, H.L., van Noordwijk, M., Ruysschaert, D., et al., 2013. Will funding to reduce
emissions from deforestation and (forest) degradation (REDD ) stop conversion
of peat swamps to oil palm in orangutan habitat in Tripa in Aceh, Indonesia?
Mitigation and Adaptation Strategies for Global Change. doi:10.1007/s11027013-9524-5.
UNEP, 2013. The Emissions Gap Report 2013. Nairobi: UNEP.
UNFCCC, 1992. United Nations Framework Convention on Climate Change.
Available at: http://unfccc.int/resource/docs/convkp/conveng.pdf (accessed
30.03.13).
Unger, N., 2012. Global climate forcing by criteria air pollutants. Annual Review of
Energy and the Environment 37, 124.
Van Huis, A., 2013. Potential of insects as food and feed in assuring food security.
Annual Review of Entomology 58, 563583.
VandenBygaart, A.J., Angers, D.A., 2006. Towards accurate measurements of soil
organic carbon stock change in agroecosystems. Canadian Journal of Soil
Science 86, 465471.
Verchot, L.V., Hutabarat, L., Hairiah, K., van Noordwijk, M., 2006. Nitrogen
availability and soil N2O emissions following conversion of forests to coffee in
southern Sumatra. Global Biogeochemical Cycles 20, GB4008. doi:10.1029/
2005GB002469.
Verchot, L.V., Van Noordwijk, M., Kandji, S., et al., 2007. Climate change: Linking
adaptation and mitigation through agroforestry. Mitigation and Adaptation
Strategies for Global Change 12, 901918.
Vermeulen, S.J., Campbell, B.M., Ingram, J.S.I., 2012. Climate change and
food systems. Annual Review of Environment and Resources 37, 195222,
2012.
Wang, J., Zhang, X., Xiong, Z., et al., 2012. Methane emissions from a rice
agroecosystem in South China: Effects of water regime, straw incorporation and
nitrogen fertilizer. Nutrient Cycling in Agroecosystems 93 (1), 103112.
Wang, S., Wilkes, A., Zhang, Z., et al., 2011a. Management and land use change
effects on soil carbon in northern China's grasslands: A synthesis. Agriculture,
Ecosystems and Environment 142, 329340.
Wang, X., Cai, D., Hoogmoed, W.B., Oenema, O., 2011b. Regional distribution of
nitrogen fertilizer use and N-saving potential for improvement of food production
and nitrogen use efciency in China. Journal of the Science of Food and
Agriculture 91 (11), 20132023.
Watson, R.T., Noble, I., Bolin, B., et al., 2000. Land use, land-use change, and
forestry: A special report of the intergovernmental panel on climate change.
Cambridge: Cambridge University Press.
Williams, M., 2006. Deforesting the earth, from prehistory to global crisis: An
abridgement. Chicago, IL: The University of Chicago Press, 543 pp.
Xu, S., Shi, X., Zhao, Y., et al., 2011. Carbon sequestration potential of
recommended management practices for paddy soils of China, 19802050.
Geoderma 166, 206213.
Yunju, L., Kahrl, F., Jianjun, P., et al., 2012. Fertilizer use patterns in Yunnan
Province, China: Implications for agricultural and environmental policy.
Agricultural Systems 110, 7889.
Zhu, Z.L., Chen, D.L., 2002. Nitrogen fertilizer use in ChinaContributions to food
production, impacts on the environment and best management strategies.
Nutrient Cycling in Agroecosystems 63 (23), 117127.
Zomer, R.J., Trabucco, A., Coe, R., Place, F., 2009. Trees on farm: Analysis of
global extent and geographical patterns of agroforestry. Nairobi: World
Agroforestry Centre (ICRAF). ICRAF Working Paper 89.
Relevant Websites
http://www.asb.cgiar.org/
ASB (Alternatives to Shash and Burn Partnership for the Tropical Forest
Margins).
http://ccafs.cgiar.org/
CCAFS (Climate Change, Agriculture and Food Systems).
http://www.climatesmartagriculture.org/en/
Climate Smart Agriculture.
http://www.ecoagriculture.org/
Ecoagriculture.
231
http://www.es-partnership.org/esp
ESP (Ecosystem Services Partnership).
http://www.fao.org/climatechange/climatesmart/en/
FAO Climate Smart Agriculture.
http://www.cgiar.org/our-research/cgiar-research-programs/cgiar-research-programon-forests-trees-and-agroforestry/
FTA (Forests, trees and Agroforestry).
http://www.soilcarbon.org.uk/
Global Benets of Soil carbon (SCOPE).
http://www.scopenvironment.org/
SCOPE (Scientic Committee on Problems of the Environment).
http://www.unep.org/
UNEP.
Glossary
Disease management Methods to prevent and control
diseases and their effects on crops.
Emerging disease A disease that is increasing in incidence,
host or geographical range, or virulence and/or has been
newly discovered.
Environment The biotic and abiotic elements
surrounding an object or organism.
Epidemic Increased occurrence of disease in a population.
Host A living organism that is invaded or infected by a
parasite and from which the parasite obtains partial or total
nourishment.
Incidence The number of plants affected by a disease
within a population, commonly expressed as a percentage.
232
doi:10.1016/B978-0-444-52512-3.00004-8
233
(Staples, 2000). It is commonly suggested that as a consequence of this disease, Britain became a tea-drinking society
(Ainswort, 1969), although other social and economic factors
probably also played a role in this transition (Madden, 2013).
What is clear is that coffee production moved to other countries in South and Central America. A new epidemic was then
discovered during 1971 in Brazil, and from there the pathogen
spread over South and Central America in countries whose
economies depend on coffee production (Campbell and
Madden, 1990; Staples, 2000). The coffee rust epidemic of
2013 threatened the livelihoods of many smallholder farmers
in the Americas, amid speculation about the role of climate
change.
234
Canola diseases
Important recent epidemics in canola of Sclerotinia stem rot,
caused by Sclerotinia sclerotiorum, occurred in England in 1991
and in 2007. In 2007, 5.7% of plants were affected by the
disease, generating the worst epidemic since 1991 (Gladders
et al., 2008). It has been suggested that weather factors and
variation in inoculum were main factors in the development
of the epidemic. As a consequence, higher production of inoculum in the coming years was predicted (Gladders et al.,
2008). During 1991, disease levels were very high with incidence of 46% and an average of 5.5% of plants affected.
Weather factors were conducive for the disease in early May
and early June (Gladders et al., 1993).
(a)
235
(b)
Figure 1 Symptoms (pustules) of wheat stem rust, caused by the fungus Puccinia graminis f.sp. tritici, on a wheat stem (a) and leaf (b). Photo
by John Fredy Hernandez Nopsa.
Fungi
Fungi are an important group of plant pathogens that cause a
high proportion of plant diseases. Organisms in the kingdom
Fungi are eukaryotic, comprised of hyphae or yeast cells, and
reproduce by sexual or asexual spores (Figure 2) dispersed by
rain splash, wind, humans, animals, seed, and soil movement.
Fungal plant pathogens are distributed in all major phyla,
including Ascomycota, Basidiomycota, Zygomycota, Chytridiomycota, and Deuteromycota. Fungi can survive as
mycelium in a host or organic material tolerating wide temperature and moisture ranges (Agrios, 2005). They produce an
array of spores for dispersal (such as conidia and urediniospores) and also produce sexual and asexual structures for
survival (such as chlamydospores, sclerotia, zygospores, and
teliospores). Some fungi have complicated life cycles with
multiple spore types and different hosts (such as many rust
fungi), whereas others have simple life cycles. Fungi can utilize
direct penetration (e.g., Magnaporthe oryze) or natural openings
(stomata and lenticels) and wounds (e.g., Botrytis cinerea) to
gain access into the host. During the plant parasitic phase of
their life cycle, fungi can produce haustoria (feeding organs)
inside the host cell to draw nutrients (biotrophic fungi) or
produce enzymes that kill host cells ahead of mycelium development (necrotrophic fungi). This results in a variety of
symptoms, including leaf spots, blights, rots, wilts, etc. Some
fungi also produce toxins that may aid in plant colonization. These mycotoxins can be toxic to humans and animals,
such as deoxynivalenol and zearalenone produced by Fusarium
236
Oomycetes
Colloquially called water molds, oomycetes are classied
in the kingdom Chromista and are fungus-like eukaryotic
Viruses
(a)
(b)
(c)
Figure 4 Downy mildew on soybean. (a) Pale green to light yellow spots on the upper surface of soybean leaves and developed grayish mycelia
of the oomycete on the lower foliar surface of a soybean leaf; (b, c) determinate growth of sporangiophores showing unattached oval-shaped
sporangia (200 and 500 , respectively). Photo by Maria Valeria Avanzato.
237
Nematodes
Temperature
Nematodes, in the kingdom Animalia, are worm-like in appearance and generally soilborne (with exceptions such as
Aphelenchoides, a foliar nematode). Although numerous
saprophytic nematodes exist in soils, they differ from plant
pathogenic nematodes in that the latter have stylets that allow
feeding on plants. Nematodes hatch from eggs laid by females
either after mating with males or parthenogenetically. The
juveniles go through four molts, where in some species the
rst and second stages do not feed on plants. Soil moisture,
aeration, and temperatures greatly affect nematode survival
and movement. Plant pathogenic nematodes can be ecto- or
endoparasites depending on their feeding location in the root
and sedentary or migratory depending on their movement
during feeding. Nematode feeding on plants can cause
mechanical injury and alter cell physiology because of enzymes in their saliva. Consequent symptoms on plants include
yellowing, stunting, hyperplasia at feeding sites such as root
knots and root galls, root lesions, etc. Further, nematodes can
predispose plants to infection by other soilborne pathogens,
often producing wounds that facilitate pathogen entry. Diagnosis of nematode diseases relies on identifying the nematode
species based on morphology, by rst isolating nematodes
using soil isolation techniques, such as Baermann's funnel
method, sieving method, and centrifugation or sugar oatation methods (Agrios, 2005). Symptomatology and nucleic
acid-based detection techniques are also used.
Others
Other microorganisms such as protozoa, viroids, and algae also
cause serious plant diseases (Agrios, 2005). Some such examples include phloem necrosis of coffee (Phytomonas leptovasorum), coconut cadang-cadang disease (Coconut cadang-cadang
Pathogen
Disease
Host
Environment
238
Precipitation
Many plant pathogens, such as nonfastidious bacteria, nematodes, oomycetes, and certain fungi, rely on water for their
dispersal. Thus, precipitation patterns serve as drivers of these
epidemics and any alteration can change the prevalence and
spread of these diseases. In semiarid and arid regions of the
mid-latitudes, the incidence of non-vector-borne bacterial
diseases that have high moisture requirements are expected to
decline (Jones and Barbetti, 2012). Similarly, the Dothistroma
needle blight epidemic (caused by the fungus Mycosphaerella
pini) in North America may be moving north due to higher
temperatures and altered rainfall patterns (Woods et al., 2005).
In general, there is a correlation between the number of precipitation events per season and the number of infection cycles
for pathogens (Agrios, 2005). Vector-borne viral and bacterial
diseases can also be affected by changes in precipitation patterns. Long dry seasons, for example, can increase the number
of B. tabaci generations, consequently increasing the incidence
of begomoviruses (Jones and Barbetti, 2012). Similarly, increased soil moisture and temperature in temperate regions
may increase epidemics of fungi-transmitted viruses because
vector spores will be more easily dispersed. Thus, epidemics of
furoviruses and bymoviruses, such as Soil-borne wheat mosaic
virus and Wheat spindle streak mosaic virus, are expected to increase in Canada, Northern USA, Northern Europe, Northeast
Asia, and Southern South America (Jones and Barbetti, 2012).
However, in rain-fed elds of India and Africa, where reduced
Relative humidity
Many fungal pathogens require high relative humidity, and
associated surface moisture, for germination and dispersal of
their spores. Oomycetes (for most of their life cycle) and
bacteria need leaf surface moisture to aid with their movement
into natural openings and wounds. Powdery mildews are an
exception to this, causing maximum infection in low (50
70%) relative humidity environments (Agrios, 2005). Similarly, ight patterns and multiplication rates of insect vectors
can be adversely affected by high humidity. Plants become
more succulent and tender under high humidity scenarios,
making them more susceptible to contact-transmitted viruses
(Jones and Barbetti, 2012).
Wind
Wind drives plant disease epidemics by affecting dispersal of
pathogen propagules, increasing drying of host surfaces, and
increasing wounding of hosts. Certain spores of fungi (such as
urediniospores) and readily airborne insect vectors can be
dispersed around the globe by high intensity winds and
storms. Periodic increases in wind velocity, consequent to
climate change, however, can limit the dispersal of winged
aphid vectors and lower the incidence of the diseases they
transmit (Jones and Barbetti, 2012). The prevailing wind
direction can also determine the direction of spread of epidemics and disease outbreaks.
CO2
The CO2 concentration in the atmosphere affects the rate of
photosynthesis, especially in C3 plants, by altering internal
carbon dioxide concentrations (Ziska and Bunce, 1997). Thus,
elevated CO2 improves photosynthesis; increases plant size
attributes, such as leaf thickness, area, longevity, and number
of leaves; and also increases tillering, stem and root length,
and dry weight (Coakley et al., 1999). Such changes alter plant
architecture and density, creating more humid microclimates,
conducive for many fungal diseases. In addition to this,
changes in CO2 concentrations can alter secondary metabolite
pathways in plants, in turn altering the nutritive value of leaves
to disease vectors and affecting plant defense signaling. Higher
carbon:nitrogen ratios in these plants would also result in
slower decomposition of plant litter and greater survival of
pathogen resting structures (Coakley et al., 1999). Changes in
CO2 concentration can also affect hostpathogen interactions
in different pathosystems. In barley powdery mildew caused
by Blumeria graminis, an increase in CO2 results in a reduction
in the rate of primary penetration of the host, but increases the
growth rate of the pathogen once established (Coakley et al.,
1999). Such contrasting results are also seen in virus pathosystems where high CO2 is predicted to suppress pathogeninduced virus resistance but shown to increase resistance to
Potato virus Y in tobacco. Similarly, among bacterial pathogens,
soft rot of tomato caused by Pseudomonas marginalis was inhibited by higher CO2 concentrations, but incidence of bacterial wilt (R. solanacearum) on pepper increased (Jones and
Barbetti, 2012). Thus, the effects of CO2 on plant diseases are
pathosystem-specic, making generalizations difcult.
239
geographical areas. Under these new environmental conditions, factors that improve rates of reproduction and survival abilities (ability to oversummer and overwinter) will
affect pathogen tness. For example, predictions for the
generalist plant pathogen P. cinnamomi in Europe include
improved ability to persist under increased temperatures and
consequent range expansions (Bergot et al., 2004). In vectored pathogens, pathogen range expansions would also require increases in vector ranges. In temperate countries, insect
vectors are expected to have greater survival in warmer winters and faster reproduction with higher summer temperatures. In Europe, aphid-transmitted viral diseases, like potato
leaf roll and yellow dwarf in cereals, are predicted to increase
under higher temperatures (Jones and Barbetti, 2012). In
addition to responses to host and vector range shifts,
pathogens can be directly affected by climate change. Generalist viruses, less affected by temperature uctuations and
adapted to wider host ranges, are more likely to expand
under climate change scenarios (Jones and Barbetti, 2012).
Similarly, fungal, oomycete, and nematode pathogens that
depend on water for transport will more likely have reduced
expansion in tropical climates with lower predicted precipitation and more frequent droughts. In addition, extreme
weather events, like torrential rains, hurricanes, and storms,
can transport pathogens across large geographical distances
into new regions. A recent expansion of soybean rust (Phakopsora pachyrhizi) into North America occurred in November
2004, probably when the spores were introduced by hurricane Ivan.
240
the number of outbreaks could lead to greater use of pesticides, increasing the risk of pest resistance to pesticides. Additionally, faster crop growth may shorten the time between
applications, having direct effects on producers, economics,
environment, and food safety (Juroszek and von Tiedemann,
2011).
Additional Reading
There are a number of good recent reviews on the subject of
climate change and plant disease in addition to those cited
above (Chakraborty and Newton, 2011; Eastburn et al., 2011;
Gregory et al., 2009; Juroszek and von Tiedemann, 2011;
Luck et al., 2011; Newton et al., 2011; Pautasso et al., 2010,
2012; Savary et al., 2011b; Sutherst et al., 2011); this continues to be an active area for synthesis. Reviews have addressed soilborne pathogens, which are generally less studied
compared with foliar pathogens but have the potential for
particularly strong and potentially surprising responses to
climate change (Chakraborty et al., 2012; Garrett et al., 2012;
Pritchard, 2011). The effect of climate change on benecial
microbes also merits more attention (Compant et al., 2010).
As for forests, plantation production offer challenges because
of the long-lived nature of the perennial plant hosts (Ghini
et al., 2011).
The inclusion of plant disease and its management in
greenhouse gas budgets may support prioritization of management strategies (Carlton et al., 2012; Mahmuti et al., 2009).
The complexity of pathogenhostenvironment interactions is
an important problem for scenario analyses (Garrett et al.,
2011; Shaw and Osborne, 2011), and the need for better longterm data sets to validate scenario analyses is an ongoing issue,
with some intriguing exceptions (Bearchell et al., 2005; Jeger
and Pautasso, 2008). Work is ongoing to develop disease risk
assessments at the scales needed for effective prioritization
(Savary et al., 2011a; Sparks et al., 2011). The impact of variability in climate patterns, especially extreme events, is an
important challenge for scenario analysis for plant disease
(Garrett et al., 2013; Rosenzweig et al., 2001; Scherm, 2004;
Scherm and van Bruggen, 1994).
Acknowledgments
The authors appreciate support from the Australian Government's Cooperative Research Centres Program, the CGIAR
Consortium Research Program for Roots, Tubers and Bananas
241
References
Adger, W.N., Huq, S., Brown, K., Conway, D., Hulme, M., 2003. Adaptation to
climate change in the developing world. Progress in Development Studies 3 (3),
179195.
Agrios, G.N., 2005. Plant Pathology. Burlington, MA: Elsevier.
Ainswort, G.C., 1969. History of plant pathology in Great Britain. Annual Review of
Phytopathology 7, 1330.
Anderson, P.K., et al., 2004. Emerging infectious diseases of plants: Pathogen
pollution, climate change and agrotechnology drivers. Trends in Ecology &
Evolution 19 (10), 535544.
Ayliffe, M., Singh, R., Lagudah, E., 2008. Durable resistance to wheat stem rust
needed. Current Opinion in Plant Biology 11 (2), 187192.
Bearchell, S.J., Fraaije, B.A., Shaw, M.W., Fitt, B.D.L., 2005. Wheat archive links
long-term fungal pathogen population dynamics to air pollution. Proceedings of
the National Academy of Sciences of the USA 102 (15), 54385442.
Bergot, M., et al., 2004. Simulation of potential range expansion of oak disease
caused by Phytophthora cinnamomi under climate change. Global Change
Biology 10 (9), 15391552.
Boland, G.J., Melzer, M.S., Hopkin, A., Higgins, V., Nassuth, A., 2004. Climate
change and plant diseases in Ontario. Canadian Journal of Plant Pathology
Revue Canadienne De Phytopathologie 26 (3), 335350.
Buczacki, S.T., Harris, K.M., 1981. Pests, diseases and disorders of garden plants,
512 pp.
Burns, A., Gleadow, R., Cliff, J., Zacarias, A., Cavagnaro, T., 2010. Cassava: The
drought, war and famine crop in a changing world. Sustainability 2 (11),
35723607.
Campbell, C.L., Madden, L.V., 1990. Introduction to Plant Disease Epidemiology.
New York: John Willey & Sons.
Canto, T., Aranda, M.A., Fereres, A., 2009. Climate change effects on physiology
and population processes of hosts and vectors that inuence the spread of
hemipteran-borne plant viruses. Global Change Biology 15 (8), 18841894.
Carlton, R.R., West, J.S., Smith, P., Fitt, B.D.L., 2012. A comparison of GHG
emissions from UK eld crop production under selected arable systems with
reference to disease control. European Journal of Plant Pathology 133 (1),
333351.
242
Chakraborty, S., et al., 1998. Potential impact of climate change on plant diseases
of economic signicance to Australia. Australasian Plant Pathology 27 (1),
1535.
Chakraborty, S., Newton, A.C., 2011. Climate change, plant diseases and food
security: An overview. Plant Pathology 60 (1), 214.
Chakraborty, S., Pangga, I.B., Roper, M.M., 2012. Climate change and multitrophic
interactions in soil: The primacy of plants and functional domains. Global
Change Biology 18 (7), 21112125.
Chakraborty, S., Tiedemann, A.V., Teng, P.S., 2000. Climate change: Potential
impact on plant diseases. Environmental Pollution 108 (3), 317326.
Coakley, S.M., Scherm, H., Chakraborty, S., 1999. Climate change and plant disease
management. Annual Review of Phytopathology 37, 399426.
Compant, S., van der Heijden, M.G.A., Sessitsch, A., 2010. Climate change effects
on benecial plantmicroorganism interactions. FEMS Microbiology Ecology 73
(2), 197214.
Dixon, G.R., 2012. Climate change impact on crop growth and food production,
and plant pathogens. Canadian Journal of Plant Pathology 34 (3), 362379.
Dukes, J.S., et al., 2009. Responses of insect pests, pathogens, and invasive plant
species to climate change in the forests of northeastern North America: What can
we predict? Canadian Journal of Forest Research 39 (2), 231248.
Eastburn, D.M., McElrone, A.J., Bilgin, D.D., 2011. Inuence of atmospheric and
climatic change on plantpathogen interactions. Plant Pathology 60 (1), 5469.
FAO, 2013. Food and Agriculture Organization of the United Nations, FAOSTAT
Database (FAOSTAT, 2013). Available at: http://faostat3.fao.org/faostat-gateway/
go/to/home/E (accessed 31.05.13).
Fargette, D., et al., 2006. Molecular ecology and emergence of tropical plant viruses.
Annual Review of Phytopathology 44 (1), 235260.
Fletcher, J., 2011. Preparing for emerging and unknown threats in crops. In:
Eaglesham, A., Abel de Len, F., Hardy, R.W.F. (Eds.), Food Security: The
Intersection of Sustainability, Safety and Defense. Proceedings of the twenty-third
annual conference of the National Agricultural Biotechnology Council.
MinneapolisSt. Paul: NABC, pp. 149159. (NABC Report 23).
Francl, L., 2001. The disease triangle: A plant pathological paradigm revisited. The
Plant health instructor. APSnet. Available at: http://www.apsnet.org/edcenter/
instcomm/TeachingArticles/Pages/DiseaseTriangle.aspx (accessed 01.04.13).
Frankel, S.J., Hansen, E.M., 2011. Forest Phytophthora diseases in the Americas:
20072010. New Zealand Journal of Forestry Science 41 (Suppl), S159S167.
Fry, W.E., et al., 2013. The 2009 late blight pandemic in the eastern United States
causes and results. Plant Disease 97 (3), 296306.
Garbelotto, M., Pautasso, M., 2011. Impacts of exotic forest pathogens on
Mediterranean ecosystems: Four case studies. European Journal of Plant
Pathology 133 (1), 101116.
Garrett, K.A., Dendy, S.P., Frank, E.E., Rouse, M.N., Travers, S.E., 2006. Climate
change effects on plant disease: Genomes to ecosystems. Annual Review of
Phytopathology 44, 489509.
Garrett, K.A., et al., 2011. Complexity in climate-change impacts: An analytical
framework for effects mediated by plant disease. Plant Pathology 60 (1),
1530.
Garrett, K.A., et al., 2013. The effects of climate variability and the color of weather
time series on agricultural diseases and pests, and decision-making for their
management. Agricultural and Forest Meteorology 170, 216227.
Garrett, K.A., Jumpponen, A., Toomajian, C., Gomez-Montano, L., 2012. Climate
change and plant health: Designing research spillover from plant genomics for
understanding the role of microbial communities. Canadian Journal of Plant
Pathology 34, 349361.
Ghini, R., Bettiol, W., Hamada, E., 2011. Diseases in tropical and plantation crops
as affected by climate changes: Current knowledge and perspectives. Plant
Pathology 60 (1), 122132.
Gladders, P., Davies, J.M.L., Hardwick, N.V., 1993. Review of Sclerotinia epidemic
in winter oilseed rape in England and Wales 1991. Bulletin OILB/SROP 16, 9.
Gladders, P., Ginsburg, D., Smith, J.A., 2008. Sclerotinia in oilseed rape: A review
of the 2007 epidemic in England. Cambridge UK. Home-Grown Cereals
Authority.
Gregory, P.J., Johnson, S.N., Newton, A.C., Ingram, J.S.I., 2009. Integrating pests
and pathogens into the climate change/food security debate. Journal of
Experimental Botany 60 (10), 28272838.
Grunwald, N.J., et al., 2009. Standardizing the nomenclature for clonal lineages of
the sudden oak death pathogen, Phytophthora ramorum. Phytopathology 99 (7),
792795.
Hannukkala, A.O., Kaukoranta, T., Lehtinen, A., Rahkonen, A., 2007. Late-blight
epidemics on potato in Finland, 19332002; increased and earlier occurrence of
epidemics associated with climate change and lack of rotation. Plant Pathology
56 (1), 167176.
Hoffmann, U., 2011. Assuring food security in developing countries under the
challenges of climate change: Key trade and development issues of a
fundamental transformation of agriculture. United Nations Conference on Trade
and Development. Geneva: UNCTAD.
Islam, M.M., 2007. The great Bengal famine and the question of FAD yet again.
Modern Asian Studies 41 (02), 421440.
Jeger, M.J., Pautasso, M., 2008. Plant disease and global change The importance
of long-term data sets. New Phytologist 177 (1), 811.
Jones, R.A.C., Barbetti, M.J., 2012. Inuence of climate change on plant disease
infections and epidemics caused by viruses and bacteria. CAB Reviews:
Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 7.
Joshi, A.K., et al., 2011. Delivering rust resistant wheat to farmers: A step towards
increased food security. Euphytica 179 (1), 187196.
Juroszek, P., von Tiedemann, A., 2011. Potential strategies and future requirements
for plant disease management under a changing climate. Plant Pathology 60 (1),
100112.
Lake, J.A., Wade, R.N., 2009. Plantpathogen interactions and elevated CO2:
Morphological changes in favour of pathogens. Journal of Experimental Botany
60 (11), 31233131.
Luck, J., et al., 2011. Climate change and diseases of food crops. Plant Pathology
60 (1), 113121.
Madden, L.V., 2013. Spot of tea? Phytopathology News 47 (5), 5861.
Mahmuti, M., West, J.S., Watts, J., Gladders, P., Fitt, B.D.L., 2009. Controlling crop
disease contributes to both food security and climate change mitigation.
International Journal of Agricultural Sustainability 7 (3), 189202.
McDonald, B.A., Linde, C., 2002. Pathogen population genetics, evolutionary
potential, and durable resistance. Annual Review of Phytopathology 40,
349379.
Miraglia, M., et al., 2009. Climate change and food safety: An emerging issue with
special focus on Europe. Food and Chemical Toxicology: An International
Journal Published for the British Industrial Biological Research Association 47
(5), 10091021.
Mitzubuti, E.S.G., Fry, W.E., 2006. Potato late blight. In: Cooke, B.M., Jones, G.,
Kaye, B. (Eds.), The Epidemiology of Plant Diseases. Dordrecht, The Netherlands:
Springer, pp. 445471.
Newton, A.C., Johnson, S.N., Gregory, P.J., 2011. Implications of climate change for
diseases, crop yields and food security. Euphytica 179 (1), 318.
Nolla, J.A.B., Valiela, M.V.F., 1976. Contributions to the history of plant pathology
in South America, Central America, and Mexico. Annual Review of
Phytopathology 14 (1), 1129.
Otim-Nape, G.W., Thresh, J.M., 2006. The recient epidemic of Cassava mosaic virus
disease in Uganda. In: Cooke, B.M., Jones, G., Kaye, B. (Eds.), The
Epidemiology of Plant Diseases. Dordrecht, The Netherlands: Springer,
pp. 541549.
Padmanabhan, S.Y., 1973. The great Bengal famine. Annual Review of
Phytopathology 11, 1124.
Pautasso, M., et al., 2010. Plant health and global change Some implications for
landscape management. Biological Reviews 85 (4), 729755.
Pautasso, M., Doring, T.F., Garbelotto, M., Pellis, L., Jeger, M.J., 2012. Impacts of
climate change on plant diseases Opinions and trends. European Journal of
Plant Pathology 133 (1), 295313.
Pfender, W.F., Vollmer, S.S., 1999. Freezing temperature effect on survival of
Puccinia graminis subsp graminicola in Festuca arundinacea and Lolium
perenne. Plant Disease 83 (11), 10581062.
Porta Puglia, A., Vannacci, G., 2012. Fungal plant diseases in Europe and in the
Mediterranean basin. In: Lal, R. (Ed.), Encyclopedia of Life Support Systems
(EOLSS), Developed Under the Auspices of the UNESCO. Oxford, UK: Eolss
Publishers. Available at: http://www.eolss.net (accessed 31.05.13).
Pritchard, S.G., 2011. Soil organisms and global climate change. Plant Pathology 60
(1), 8299.
Rapilly, F., 2001. Plant pathogenic fungi: The rst identied pathogens in the history
of science. Comptes Rendus de l'Acadmie des Sciences - Series III Sciences
de la Vie 324 (10), 893898.
Ristaino, J.B., 2002. Tracking historic migrations of the Irish potato famine
pathogen, Phytophthora infestans. Microbes and Infection 4 (13), 13691377.
Rizzo, D.M., Garbelotto, M., Hansen, E.M., 2005. Phytophthora ramorum: Integrative
research and management of an emerging pathogen in California and Oregon
forests. Annual Review of Phytopathology 43, 309335.
Rosenzweig, C., Iglesias, A., Yang, X.B., Epstein, P.R., Chivian, E., 2001. Climate
change and extreme weather events; implications for food production, plant
diseases, and pests. Global Change & Human Health 2 (2), 90104.
Rossman, A.Y., 2008. The impact of invasive fungi on agricultural ecosystems in the
United States. Biological Invasions 11 (1), 97107.
Santer, M., 2009. Richard Bradley a unied, living agent theory of the cause of
infectious diseases of plants, animals, and humans in the rst decades of the
18th century. Perspectives in Biology and Medicine 52 (4), 566578.
Savary, S., et al., 2011a. Risk factors for crop health under global change and
agricultural shifts: A framework of analyses using rice in tropical and subtropical
Asia as a model. Phytopathology 101 (6), 696709.
Savary, S., et al., 2011b. International agricultural research tackling the effects of
global and climate changes on plant diseases in the developing world. Plant
Disease 95 (10), 12041216.
Scherm, H., 2004. Climate change: Can we predict the impacts on plant
pathology and pest management? Canadian Journal of Plant Pathology 26 (3),
267273.
Scherm, H., van Bruggen, A.H.C., 1994. Global warming and nonlinear growth: How
important are changes in average temperature? Phytopathology 84 (12),
13801384.
Shaw, M.W., Osborne, T.M., 2011. Geographic distribution of plant pathogens in
response to climate change. Plant Pathology 60 (1), 3143.
Shurtleff, M., Averre III, C., 1997. Glossary of Plant-Pathological Terms. St. Paul,
MN: APS Press.
Singh, R.P., et al., 2011. The emergence of Ug99 races of the stem rust fungus is a
threat to world wheat production. In: VanAlfen, N.K., Bruening, G., Leach, J.E.
(Eds.), Annual Review of Phytopathology, vol. 49. Palo Alto: Annual Reviews,
pp. 465481.
243
Sparks, A.H., Forbes, G.A., Hijmans, R.J., Garrett, K.A., 2011. A metamodeling
framework for extending the application domain of process-based ecological
models. Ecosphere 2 (8), Art90.
Staples, R.C., 2000. Research on the rust fungi during the twentieth century. Annual
Review of Phytopathology 38, 4969.
Sturrock, R., 2012. Climate change and forest diseases: Using today's knowledge to
address future challenges. Forest Systems 21 (2), 329336.
Sutherst, R.W., et al., 2011. Adapting to crop pest and pathogen risks under a
changing climate. Wiley Interdisciplinary Reviews: Climate Change 2 (2),
220237.
Webb, K.M., et al., 2010. A benet of high temperature: Increased effectiveness of a
rice bacterial blight disease resistance gene. New Phytol 185 (2), 568576.
Woods, A., Coates, K.D., Hamann, A., 2005. Is an unprecedented Dothistroma
needle blight epidemic related to climate change? BioScience 55 (9),
761769.
Yamamura, K., Kiritani, K., 1998. A simple method to estimate the potential increase
in the number of generations under global warming in temperate zones. Applied
Entomology and Zoology 33 (2), 289298.
Ziska, L.H., Bunce, J.A., 1997. Inuence of increasing carbon dioxide concentration
on the photosynthetic and growth stimulation of selected C4 crops and weeds.
Photosynthesis Research 54, 199208.
Glossary
Carbon footprint The total GHG emissions caused by an
activity or product.
Enteric methane (CH4) emissions Emissions of the
greenhouse gas, methane, from the animal's digestive tract
that result from microbial activity. Emissions are greater
from ruminant species compared to nonruminant species of
livestock.
Global warming potential (GWP) The potential
for greenhouse gases (GHG) to trap heat in the
Introduction
Anthropogenic (human-caused) climate change is both
impacting animal agricultural systems and inuenced by
those systems through emissions of greenhouse gases
(GHG). Concurrent with global climatic change, global
demand for animal agricultural products (e.g., meat, milk,
and eggs) is rising with the growing population and increasing per capita incomes in developing nations. The
world population is expected to surpass 9 billion by 2050
and demand for meat and dairy products are expected to
increase by 58% and 74%, respectively (Garg, 2012). Consequentially, understanding how our animal systems are
impacted by and contribute to climate change needs to be
discussed within the context of certain growing demand for
animal-derived products. Strategies to adapt and mitigate
the impacts of these systems on climate change will be an
interdisciplinary challenge that will require the cooperation
of farmers and ranchers, researchers, extension educators,
regulators, and policymakers. Advancements in animal
production to address climate change will be a combination
of extending current knowledge, innovative research, and
effective dissemination of research ndings.
The scientic consensus that human activity is contributing
to global climatic change among climate scientists is strong
(Oreskes, 2004), with several independent attempts to reconstruct global surface temperatures over the last several
thousand years leading to the same conclusion; there has been
a clear warming trend in the past century, which has occurred
at an unprecedented rate (Mann et al., 2008; Marcott et al.,
2013). The major cause for the warming trend is increasing
concentrations of GHG in the atmosphere, which has been
primarily driven by the combustion of fossil fuels since the
beginning of the Industrial Revolution. It has been known for
more than 100 years that carbon dioxide (CO2) inuences
temperature (Arrhenius, 1896), and along with methane
(CH4) and nitrous oxide (N2O) forms the major GHG emissions that result from animal systems. However, CO2, CH4,
and N2O do not all contribute to warming temperatures
244
doi:10.1016/B978-0-444-52512-3.00006-1
245
Consumer/retail
Feed production
Animals
Enteric fermentation
Transportation
Fossil fuel combustion
Electricity use
Processing
Refrigerants
Electricity use
Wastewater emissions
Figure 1 Example of the phases of production and greenhouse gases (GHG) emission sources that would be accounted for in an Life Cycle
Assessment (LCA) of beefs GHG emissions or carbon footprint. Methodologies and sources considered often vary from industry to industry and
analysis to analysis, which can lead to challenges when attempting to compare across LCA.
Direct Sources
Enteric
Enteric CH4 emissions are one of the major sources of GHG
emissions from ruminants (e.g., cattle, goats, and sheep)
agriculture systems (Pitesky et al., 2009; Thoma et al., 2013).
The production of CH4 represents a loss of the gross energy
(GE) value of the animal's feed, which depending on the diet
and level of intake can be a loss of 212% of dietary GE for
ruminants (Johnson and Ward, 1996). Enteric CH4 emissions
from nonruminant animals do occur from hindgut fermentation processes, but are minor compared to ruminants, with
CH4 emissions typically representing less than 1% of dietary
GE for pigs and lower still for poultry (Christensen and
Thorbek, 1987; Jrgensen, 2007; Wang and Huang, 2005).
When a ruminant animal consumes feed (e.g., forages and
grains), the feed nutrients will undergo fermentation processes
resulting in the production of volatile fatty acids (VFA) that are
absorbed through the rumen wall and metabolized by the
animal, during this process, CO2 as well as hydrogen (H2) is
produced. Methane emissions do not result directly from the
fermentation processes, but rather occur from methanogenesis
carried out by methanogenic archaea residing within the
rumen. The most prevalent substrates for methanogenesis in
the rumen are H2 and CO2 (Janssen and Kirs, 2008), with
methanogens reducing CO2 to CH4 with H2 summarized in
the following equation:
CO2 4H2 CH4 2H2 O
Other substrates used in methanogenesis include formate,
methanol, and acetate (Russell, 2002). With CO2 being
abundant in the rumen due to the continuous fermentation
processes, the pool of H2 available is one of primary determinants for the total yield of CH4 from rumen methanogenesis and many mathematical models predict rumen CH4
production by modeling the rumen H2 balance (Ellis et al.,
2008). For further detailed information, Janssen (2010) conducted an excellent in-depth review of the inuence of H2 on
rumen CH4 formation. The rumen partial pressure of H2 gas is
kept very low through the action of methanogens, which is
246
Eructation
CH4
H2 pool
Propionate
Acetate
butyrate
Methanogenesis
Biohydrogenation of
unsaturated fatty acids
Microbial growth
Figure 2 A simplied model of the rumen processes that determine enteric CH4 emissions from ruminant livestock species.
Nonenteric
The predominant nonenteric direct GHG emissions source
both from ruminant and nonruminant animal agriculture
systems (e.g., swine and poultry) is manure (i.e., urine and
feces mixed). Manure GHG emissions typically occur from
manure storage systems and land-applied manure. The primary GHG emissions from stored manure are CH4 and N2O.
Fresh manure (e.g., manure on the oor of animal housing
areas) results in little or no CH4 or N2O emissions (Shaw et al.,
2007; Sun et al., 2008). For land-applied manure, N2O is the
major GHG emitted (more discussion in the Sections Indirect
Fermentation=acetogenesisVFAs acetate
CH4
the animal's diet can impact the carbon (C) and nitrogen (N)
availability in the manure and the subsequent CH4 and N2O
emissions resulting from the manure (Klling et al., 2003).
Nitrous oxide emissions primarily occur from bacterial
denitrication processes; however, N2O emissions also occur
from nitrifying bacteria and ammonia oxidizing bacteria
(Bremner, 1997). The denitrication process reduces nitrate
(NO3) to dinitrogen gas (N2), which is environmentally benign and composes 78% of the Earth's atmosphere. One of the
intermediate products of the pathway is N2O, hence emissions
of N2O can result from denitrication. Most of the N in fresh
manure is in the form of organic N (in a carbon-containing
compound, like amino acids) or ammonium (NH4+). Thus,
very little NO3 is present for denitrication. However, if microbial nitrication processes occur, which require aerobic
conditions to oxidize NH4+ to NO3, the potential for N2O
emissions from the manure will greatly increase. Often, manure storage conditions do not allow for signicant enough
oxygen presence for nitrication to occur. Such storage systems
include anaerobic lagoons and anaerobic digesters, and consequently N2O emissions from these systems are typically low
(Chadwick et al., 2011). However, solid manure storage systems and compost bedded pack systems where manure is used
as a bedding source for animals and is periodically aerated can
allow for the necessary nitrication and denitrication microbial processes to occur that result in N2O emissions (Rotz,
2004).
For extensive animal systems (i.e., where animals are primarily housed outdoors) manure is unmanaged and distributed where animals defecate and urinate in the pasture or
rangeland. Emission factors for N2O emissions in g of N2ON
per kilogram of N excreted from urine and dung patches are
often higher than manure spread on croplands for fertilizer
due to the higher N concentration in the patches, which encourages N2O emissions (Mosier et al., 1998). Additionally,
N2O emission potential per unit of N excreted is higher
for urine patches compared with feces patches, as most N
in urine is excreted as urea (vs. organic N in feces), which
is typically rapidly hydrolyzed to NH4+ and then available
to undergo nitricationdenitrication processes (Oenema
et al., 1997).
Indirect Sources
Prefarm gate
Indirect prefarm gate emissions include GHG emissions released as a result of feed production for animals (e.g., N2O
emissions from cropland soils and CO2 emissions from fossil
fuel combustion in farm equipment) and on-farm electricity
use. Crop production that is destined for animal consumption
is typically fertilized either with animal manure or synthetic
fertilizer. Nitrous oxide emissions will occur from soil in
cropland from the same microbial processes as previously
discussed. In addition to the availability and form of N in the
soil, N2O emissions are inuenced by the amount of soil C,
soil moisture conditions, pH, and temperature (Smith et al.,
1998). Emissions of N2O will be higher with increasing soil C
availability, water content, temperature, and pH (Bouwman,
1996).
247
Methane emissions from soil used for livestock crop production are virtually nonexistent in well drained soils, and
CH4 uptake by soil can occur after tillage (Omonode et al.,
2007). Soil CO2 emissions can occur during the tillage of soil
as a result of aerobic decomposition of organic matter; however, plants typically assimilate more C through photosynthesis than C is released from plant and soil respiration
processes (Chianese et al., 2009). In assessments of animal
system GHG emissions, long-term C balances of croplands are
assumed to be zero as the C assimilated by plants or added to
the system (e.g., C from manure) will be equal to the C leaving
the cropland in the form of feed biomass and CO2e emissions
(Rotz et al., 2010). However, if previously tilled cropland is
shifted into permanent grasslands, there can be a net reduction
in CO2e emissions from an animal system due to C sequestration, as long as the grassland is not tilled in the future (Rotz
et al., 2009).
Indirect CO2 emissions occur from fossil fuel combustion
in farm equipment, and from electricity generation in power
plants that burn fossil fuels, such as coal. Although fossil fuel
combustion is not a large prefarm gate emission source for
animal systems, the total contribution of these sources to total
CO2e emissions per unit of product depends on the animal
agriculture sector considered. For example, a low input grass
nished beef system would likely have a lower proportion of
its total CO2e emissions per unit of product originating from
fossil fuel use than an intensively managed dairy farm, where
cattle are housed in mechanically ventilated barns and are
milked twice per day by a milking system using energy off the
electricity grid. Furthermore, the contribution of indirect prefarm gate emissions can vary within a sector of animal agriculture based on the management systems used and the
geographic location of the farm, which inuences climate and
the crops that can be grown. Rotz et al. (2010) used the
DairyGHG model to conduct a partial LCA (to the farm gate)
of ve simulated US dairies in Pennsylvania and California of
different herd sizes (ranging from 60 to 2000 cows) and
management strategies (grazing, conned, and drylot). Fuel
use on-farm for tractors and other farm equipments ranged
from 5.8% to 9.8% of the net CO2e emissions from the
simulated dairy farms. Secondary CO2e emissions were also
considered, which included the GHG emissions from the
production of fuel, electricity, fertilizer, machinery, pesticide,
and plastics used for feed production, for managing the animals, and manure management. The secondary emissions
were found to be 18.925% of net CO2e emissions of the ve
simulated dairies to the farm gate, which may be higher than
some estimates, as the authors included CO2 sequestration
from cropland (Rotz et al., 2010). The simulated 60 cow
grazing dairy in Pennsylvania had a lower proportion of its
total CO2e emissions per kilogram of energy-corrected milk
coming from on-farm fossil fuels and secondary sources
compared with the other systems, which would be expected
due to the lower inputs (e.g., less machinery use, electricity
use, etc.) of the system (Rotz et al., 2010).
Postfarm gate
The emissions that occur postfarm gate include emissions
from fossil fuel burning during transportation, refrigeration of
products (leakage of refrigerants that have high GWPs), and
248
Mitigation
Metrics for Mitigation of Greenhouse Gas Emissions from
Animal Systems
One faces a paradox of mitigating the CO2e emissions from
human activity, including animal systems while meeting the
nutritional and material needs of a growing world population
during climatic change and variability. Meeting these challenges will require a nuanced analysis and understanding of
the implications of policy changes, and dedicated efforts to
higher proportions of acetate and higher enteric CH4 emissions. Consequently, ruminants fed diets high in fermentable
carbohydrates (e.g., nishing beef cattle in feedlots fed a
7590% grain diet) produce lower CH4 emissions per unit
of feed intake compared to ruminants fed high forage diets
(e.g., grazing cattle and dairy cattle in connement systems fed
5060% forage diets). Aguerre et al. (2011) demonstrated the
impact of the forage-to-concentrate ratio on CH4 emissions
from dairy cattle fed diets from 47% upto 68% forage and
found a linear increase in CH4 emissions per cow per day and
per kilogram of dry matter intake with increasing dietary forage percentage.
However, simply decreasing forage consumption of all ruminants worldwide is not a viable, sustainable CO2e emission
mitigation solution for ruminant production systems. Diets
very high in fermentable carbohydrates can lead to rumen
acidosis resulting in health issues, such as liver abscesses and
laminitis (an inammation of the laminae of the hoof
that cause of lameness) (Brent, 1976; Kleen et al., 2003; Owens
et al., 1998). However, the efciency of gain (i.e., amount
of feed required for 1 kg of body weight gain) when feeding
diets high in fermentable carbohydrates has historically been
more economically protable than high forage diets for
ruminant meat animal systems during the nishing phase (the
last period of the animal's life before slaughter). Subsequently,
most beef cattle in North America are nished in feedlots
where they consume high grain diets (e.g., 7590% corn
or barley). However, in recent years due to sustained increases
in commodity prices, the protability of such feeding
systems has suffered. Furthermore, ruminants' ability to utilize
forages and byproducts (e.g., distiller's grains, cottonseed, citrus pulp, and almond hulls) is a form of valuable nutrient
recycling, particularly when considering cellulose (Oltjen
and Beckett, 1996). Cellulose is the most abundant organic
(carbon-containing) compound on Earth; however, it is
indigestible to humans and large-scale, commercial cellulosic
ethanol production for use in internal combustion engines
is yet to become a reality. Therefore, one of the primary ways
humans are able to capture the energy potential of the C
xed via photosynthetic processes of plants is through
ruminants and their symbiotic relationship with the microbial populations residing in their digestive tracts. In the context that agriculture at its core is about transforming nutrients
and natural resources of low value to humans to higher
value food and ber products, the ability of ruminants to use
low protein quality, high ber feedstuffs and convert them
into high quality protein cannot be discounted if we are to
meet growing human nutritional needs and should be
weighed against the impacts of enteric CH4 emissions from
ruminants.
Lipids included in the diets of cattle has been shown to
reduce enteric CH4 emissions per animal per day (Beauchemin
et al., 2009; Odongo et al., 2007), though some of the reduction can be attributed to decreases in intake and digestibility (Beauchemin and McGinn, 2006; Beauchemin et al.,
2007). Ruminant diets are typically low in fat (o5%) and
increasing dietary fat concentration above 56% of the diet
can negatively impact rumen fermentation and decrease feed
intake (Odongo et al., 2007). Lipids and more specically,
unsaturated fatty acids, can reduce CH4 emissions via two
249
250
Manure storage
Capturing and reducing GHG emissions through manure
storage design and manure treatment offers opportunities to
mitigate GHG emissions from animal systems. If manure is
stockpiled in solid form (415% dry matter) with little or no
management or treatment, the GHG emission potential from
the manure is high (Gilroyed et al., 2011). Manure treatments
can reduce GHG emissions, as well as address pathogen load
and odors from the manure, which are other areas of concern
for animal systems. For anaerobic manure lagoons where
manure is stored in a liquid form (o7% dry matter), adding a
cover to the lagoon can capture the GHG emitted. By aring
off the accumulated gas containing CH4, more of the total C
emissions are oxidized to CO2, which reduces the net CO2e
emissions from animal manure. Additionally, covers can allow
manure surface crusts to develop (by not being disturbed by
precipitation), which some research has suggested allow
methanotrophs (organisms that oxidize CH4 to CO2) to develop (Clemens et al., 2006; Petersen et al., 2005).
Anaerobic digestion of animal manure has increased in
popularity in recent years as a way for farmers to create an onfarm energy source through the production of biogas, which
consists of primarily CH4 (6070%) and CO2 (3040%)
(Cantrell et al., 2008). The biogas can then be further rened
for use in equipment or combusted to generate electricity that
can be used on-farm or put on the grid, which can offset fossil
fuel use in the animal system (Asgedom and Kebreab, 2011).
However, costs, both for construction and operation, can be a
prohibitive factor that can keep animal agricultural operations
from adopting anaerobic digestion of manure. For individual
operations, the costs can be difcult to overcome, though
through public policy efforts it is possible to increase anaerobic digestion capacity of animal manures. The European
Union has set a goal of 25% of its energy use to come from
renewable sources by 2020, which can encourage further development of anaerobic digestion of animal manure that is
already well underway in nations like Germany and Denmark
(Holm-Nielsen et al., 2009). In the US, there have been efforts
to have utility customers pay a premium for electricity generation, with the premium allowing dairies with anaerobic digesters to cover construction and operation costs (Wang et al.,
2011). An evaluation of the program found that grants to
Production efciency
After the discussion on ways to reduce GHG emissions via
reducing CO2e emissions per animal per day or from manure
per day, other opportunities exist to reduce CO2e emissions
per unit of product through production efciency. Production
efciency for animal systems can be dened as minimizing
the inputs (e.g., feed and fossil fuels) and undesirable outputs
(e.g., GHG emissions) required to produce a given quantity of
animal product (e.g., pork, beef, and milk) (Place and
Mitloehner, 2010). Capper and Bauman, 2013 conducted an
excellent review of the role productivity plays on the environmental sustainability that can be referenced for further
details. Improved production efciency can be achieved
through increasing productivity (e.g., milk yield and growth),
optimizing the productive lifetime of individual animals and
populations, and minimizing waste. Production efciency
should not come at the cost of animal health and well-being,
as reducing environmental impacts per unit of animal product
at the cost of shirking the social responsibility of humans
toward animals is not a sustainable solution. However, there is
often much overlap between enhancing animal health and
well-being and lowering CO2e emissions per unit of product.
Additionally, production efciency gains can be made within
all animal systems by a variety of methods, and therefore, can
be seen as a one-size-ts-all solution with a long list of
customizable answers depending on the operation, industry,
location, etc.
Further explanation of the potential of production efciency to mitigate CO2e emissions from animal systems per
unit of product can be gained through historical comparisons.
Capper et al. (2009) compared US dairy production in 1944
with the 2007 system and found a 63% reduction in the CO2e
emissions required to produce 1 billion kilogram of milk
for the 2007 system. A similar comparison of the 1977 US
beef production system to the 2007 system found a 16.3%
251
252
Food waste
Although there has been much discussion and analysis in recent years with regard to the potential climate impacts of
changing diets from those higher in animal product content to
those lower in animal product content (Garnett, 2011; Jones
and Kammen, 2011; Weber and Matthews, 2008), the actual
implementation of massive global dietary change seems unlikely, especially in the face of projected increasing worldwide
Conclusion
Animal agriculture systems face a challenge in the coming
decades to meet growing global demand for animal-derived
products with nite resources. Additionally, animal systems
must meet growing demand while adapting to climate change
and variability, which animal systems contribute to through
the emissions of GHG. The sources of GHG emissions from
the entire animal production chain (from the farm to the
consumer's plate) are varied and derived from microbiological,
chemical, and physical processes. Mitigating GHG emissions
can come from different strategies of animal feeding, animal
management, manure management, and increasing efciency
and reducing waste throughout the animal production chain.
Efciency improvements and reduction of food waste can
potentially address the challenges of meeting growing demand
and mitigating environmental impacts simultaneously. Ultimately, a concerted, multifaceted global effort that includes
farmers, researchers, and policymakers is required to create
tangible, positive change surrounding the issues of climate
change and animal systems.
See also: Air: Conned Animal Facilities and Air Quality Issues.
Air: Greenhouse Gases from Agriculture. Animal Welfare: Stress,
Global Issues, and Perspectives. Beef Cattle. Climate Change:
Agricultural Mitigation. Climate Change, Society, and Agriculture:
An Economic and Policy Perspective. Dairy Animals. Energy and
Greenhouse Gases Footprint of Food Processing. Food Security:
Postharvest Losses. Human Nutrition: Malnutrition and Diet. Swine
Diseases and Disorders
References
Aarnink, A.J.A., Verstegen, M.W.A., 2007. Nutrition, key factor to reduce
environmental load from pig production. Livestock Science 109, 194203.
Aguerre, M.J., Wattiaux, M.A., Powell, J.M., Broderick, G.A., Arndt, C., 2011. Effect
of forage-to-concentrate ratio in dairy cow diets on emission of methane, carbon
dioxide, and ammonia, lactation performance, and manure excretion. Journal of
Dairy Science 94, 30813093.
Angel, R., 2007. Metabolic disorders: Limitations to growth of and mineral
deposition into the broiler skeleton after hatch and potential implications for leg
problems. Journal of Applied Poultry Research 16, 138149.
Anil, S.S., Anil, L., Deen, J., 2009. Effect of lameness on sow longevity. Journal of
American Veterinary Medical Association 235, 734738.
Appuhamy, J.A.D.R.N., Strathe, A.B., Jayasundara, S., et al., 2013. Antimethanogenic effects of monensin in dairy and beef cattle: A meta-analysis.
Journal of Dairy Science 96, 51615173. Available at: http://www.
journalofdairyscience.org/article/S0022-0302(13)00424-4/abstract (accessed
16.04.14).
Arrhenius, S., 1896. XXXI. On the inuence of carbonic acid in the air upon
the temperature of the ground. Philosophical Magazine Series 5 41, 237276.
Asgedom, H., Kebreab, E., 2011. Benecial management practices and mitigation of
greenhouse gas emissions in the agriculture of the Canadian Prairie: A review.
Agronomy for Sustainable Development 31, 433451.
Barker, Z.E., Leach, K.A., Whay, H.R., Bell, N.J., Main, D.C., 2010. Assessment of
lameness prevalence and associated risk factors in dairy herds in England and
Wales. Journal of Dairy Science 93, 932941.
Beauchemin, K.A., Janzen, H., Little, S.M., McAllister, T.A., McGinn, S.M., 2010.
Life cycle assessment of greenhouse gas emissions from beef production in
western Canada: A case study. Agricultural Systems 103, 371379.
Beauchemin, K.A., McGinn, S.M., 2006. Methane emissions from beef cattle: Effects
of fumaric acid, essential oil, and canola oil. Journal of Animal Science 84,
14891496.
Beauchemin, K.A., McGinn, S.M., Benchaar, C., Holtshausen, L., 2009. Crushed
sunower, ax, or canola seeds in lactating dairy cow diets: Effects on methane
production, rumen fermentation, and milk production. Journal of Dairy Science
92, 21182127.
Beauchemin, K.A., McGinn, S.M., Martinez, T.F., McAllister, T.A., 2007. Use of
condensed tannin extract from quebracho trees to reduce methane emissions
from cattle. Journal of Animal Science 85, 19901996.
Beauchemin, K.A., McGinn, S.M., Petit, H.V., 2007. Methane abatement strategies
for cattle: Lipid supplementation of diets. Canadian Journal of Animal Science
87, 431440.
Bicalho, R.C., Vokey, F., Erb, H.N., Guard, C.L., 2007. Visual locomotion scoring in
the rst seventy days in milk: Impact on pregnancy and survival. Journal of
Dairy Science 90, 45864591.
Bicalho, R.C., Warnick, L.D., Guard, C.L., 2008. Strategies to analyze milk losses
caused by diseases with potential incidence throughout the lactation: A lameness
example. Journal of Dairy Science 91, 26532661.
Bouwman, A.F., 1996. Direct emission of nitrous oxide from agricultural soils.
Nutrient Cycling in Agroecosystems 46, 5370.
Bremner, J.M., 1997. Sources of nitrous oxide in soils. Nutrient Cycling in
Agroecosystems 49, 716.
Brent, B.E., 1976. Relationship of acidosis to other feedlot ailments. Journal of
Animal Science 43, 930935.
Calm, J.M., 2002. Emissions and environmental impacts from air-conditioning and
refrigeration systems. International Journal of Refrigeration 25, 293305.
Cantrell, K.B., Ducey, T., Ro, K.S., Hunt, P.G., 2008. Livestock waste-to-bioenergy
generation opportunities. Bioresource Technology 99, 79417953.
Capper, J.L., 2011a. The environmental impact of beef production in the United
States: 1977 compared with 2007. Journal of Animal Science 89, 42494261.
Capper, J.L., 2011b. Replacing rose-tinted spectacles with a high-powered
microscope: The historical versus modern carbon footprint of animal agriculture.
Animal Frontiers 1, 2632.
Capper, J.L., Bauman, D.E., 2013. The role of productivity in improving the
environmental sustainability of ruminant production systems. Annual Review of
Animal Biosciences 1, 469489.
Capper, J.L., Cady, R.A., Bauman, D.E., 2009. The environmental impact of dairy
production: 1944 compared with 2007. Journal of Animal Science 87,
21602167.
Chadwick, D., Sommer, S., Thorman, R., et al., 2011. Manure management:
Implications for greenhouse gas emissions. Animal Feed Science and Technology
166167, 514531.
253
Chianese, D.S., Rotz, C.A., Richard, T.L., 2009. Whole-farm greenhouse gas
emissions: A review with application to a Pennsylvania dairy farm. Applied
Engineering in Agriculture 25, 431442.
Christensen, K., Thorbek, G., 1987. Methane excretion in the growing pig. British
Journal of Nutrition 57, 355361.
Clemens, J., Trimborn, M., Weiland, P., Amon, B., 2006. Mitigation of greenhouse
gas emissions by anaerobic digestion of cattle slurry. Agriculture, Ecosystems &
Environment 112, 171177.
Costanza, R., 1980. Embodied energy and economic valuation. Science 210,
12191224.
Craine, J.M., Elmore, A.J., Olson, K.C., Tolleson, D., 2010. Climate change and
cattle nutritional stress. Global Change Biology 16, 29012911.
Cuellar, A.D., Webber, M.E., 2010. Wasted food, wasted energy: The embedded
energy in food waste in the United States. Environmental Science and
Technology 44, 64646469.
Dalal, R.C., Wang, W., Robertson, G.P., Parton, W.J., 2003. Nitrous oxide emission
from Australian agricultural lands and mitigation options: A review. Australian
Journal of Soil Research 41, 165195.
Di, H.J., Cameron, K.C., 2003. Mitigation of nitrous oxide emissions in sprayirrigated grazed grassland by treating the soil with dicyandiamide, a nitricaiton
inhibitor. Soil Use and Management 19, 284290.
Dorward, L.J., 2012. Where are the best opportunities for reducing greenhouse gas
emissions in the food system (including the food chain)? A comment. Food
Policy 37, 463466.
Dufeld, T.F., Merrill, J.K., Bagg, R.N., 2012. Meta-analysis of the effects of
monensin in beef cattle on feed efciency, body weight gain, and dry matter
intake. Journal of Animal Science 90, 45834592.
Dufeld, T.F., Rabiee, A.R., Lean, I.J., 2008. A meta-analysis of the impact of
monensin in lactating dairy cattle. Part 2. Production effects. Journal of Dairy
Science 91, 13471360.
Ellis, J.L., Dijkstra, J., Kebreab, E., et al., 2008. Aspects of rumen microbiology
central to mechanistic modelling of methane production in cattle. Journal of
Agricultural Science 146, 213233.
EPA, 2009. GreenChill Best Practices Guideline Commercial Refrigeration Retrots.
Washington, DC, USA: Environmental Protection Agency.
EPA, 2013. Municipal Solid Waste in the United States: 2011 Facts and Figures.
Washington, DC, USA: United States Environmental Protection Agency.
FAO, WFP, and IFAD, 2012. The State of Food Insecurity in the World 2012.
Economic Growth is Necessary But Not Sufcient to Accelerate Reduction of
Hunger and Malnutrition. Rome, Italy: FAO.
FDA, 2006, NADA Number: 095-735. Available at: http://www.accessdata.fda.gov/
scripts/AnimalDrugsAtFDA/report_details.cfm?dn=095-735 (accessed 30.06.13).
Finlay, B.J., Esteban, G., Clarke, K.J., et al., 1994. Some rumen ciliates have
endosymbiotic methanogens. FEMS Microbiology Letters 177, 157162.
Garg, M.R., 2012. Balanced feeding for improving livestock productivity Increase
in milk production and nutrient use efciency and decrease in methane emission.
In: Makkar, H.P.S. (Ed.), FAO Animal Production and Health Paper. Rome,
Italy: FAO, pp. 130. Available at: http://www.fao.org/docrep/016/i3014e/
i3014e00.pdf (accessed 17.04.14).
Garnett, T., 2011. Where are the best opportunities for reducing greenhouse gas
emissions in the food system (including the food chain)? Food Policy 36
(Suppl. 1), S23S32.
Gerber, P., Vellinga, T., Opio, C., Steinfeld, H., 2011. Productivity gains and
greenhouse gas emissions intensity in dairy systems. Livestock Science 139,
100108.
Gilroyed, B., Hao, X., Larney, F.J., McAllister, T.A., 2011. Greenhouse gas
emissions from cattle feedlot manure composting and anaerobic digestion
as a potential mitigation strategy. In: Guo, L., Gunasekara, A.S., McConnell, L.L.
(Eds.), Understanding Greenhouse Gas Emissions from Agricultural
Management 1072. Washington, DC: American Chemical Society, pp. 419441.
Grainger, C., Williams, R., Eckard, R.J., Hannah, M.C., 2010. A high dose of
monensin does not reduce methane emissions of dairy cows offered pasture
supplemented with grain. Journal of Dairy Science 93, 53005308.
Guan, H., Wittenberg, K.M., Ominski, K.H., Krause, D.O., 2006. Efcacy of
ionophores in cattle diets for mitigation of enteric methane. Journal of Animal
Science 84, 18961906.
Gustavsson, J., Cederberg, C., Sonesson, U., van Otterdijk, R., Meybeck, A., 2011.
Global Food Losses and Food Waste: Extent, Causes and Prevention. Rome,
Italy: Food and Agriculture Organization of the United Nations.
Hamilton, S.W., DePeters, E.J., McGarvey, J.A., Lathrop, J., Mitloehner, F.M., 2010.
Greenhouse gas, animal performance, and bacterial population structure
responses to dietary monensin fed to dairy cows. Journal of Environmental
Quality 39, 106114.
254
Hao, X., Chang, C., Larney, F.J., 2004. Carbon, nitrogen balances and greenhouse
gas emission during cattle feedlot manure composting. Journal of Environment
Quality 33, 3744.
Hao, X., Chang, C., Larney, F.J., Travis, G.R., 2001. Greenhouse gas emissions
during cattle feedlot manure composting. Journal of Environment Quality 30,
376386.
Hashimoto, A.G., Varel, V.H., Chen, Y.R., 1981. Ultimate methane yield from beef
cattle manure: Effect of temperature, ration constituents, antibiotics and manure
age. Agricultural Wastes 3, 241256.
Hassan, A.N., Nelson, B.K., 2012. Invited review: Anaerobic fermentation of dairy
food wastewater. Journal of Dairy Science 95, 61886203.
Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003. Growth, livability, and feed
conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001
broiler diets. Poultry Science 92, 15001508.
Hegarty, R.S., 1999. Reducing rumen methane emissions through elimination of
rumen protozoa. Autralian Journal of Agricultural Research 50, 13211327.
Holm-Nielsen, J.B., Al Seadi, T., Oleskowicz-Popiel, P., 2009. The future of
anaerobic digestion and biogas utilization. Bioresource Technology 100,
54785484.
Holtshausen, L., Chaves, A.V., Beauchemin, K.A., et al., 2009. Feeding saponincontaining Yucca schidigera and Quillaja saponaria to decrease enteric methane
production in dairy cows. Journal of Dairy Science 92, 28092821.
Husted, S., 1994. Seasonal variation in methane emission from stored slurry and
solid manures. Journal of Environment Quality 23, 585592.
Immig, I., 1996. The rumen and hindgut as source of ruminant methanogenesis.
Environmental Monitoring and Assessment 42, 5772.
Janssen, P.H., 2010. Inuence of hydrogen on rumen methane formation and
fermentation balances through microbial growth kinetics and fermentation
thermodynamics. Animal Feed Science and Technology 160, 122.
Janssen, P.H., Kirs, M., 2008. Structure of the archaeal community of the rumen.
Applied Environmental Microbiology 74, 36193625.
Johnson, K.A., Johnson, D.E., 1995. Methane emissions from cattle. Journal of
Animal Science 73, 24832492.
Johnson, D.E., Ward, G.M., 1996. Estimates of animal methane emissons.
Environmental Monitoring and Assessment 42, 133141.
Jones, C.M., Kammen, D.M., 2011. Quantifying carbon footprint reduction
opportunities for U.S. households and communities. Environmental Science &
Technology 45, 40884095.
Jrgensen, H., 2007. Methane emission by growing pigs and adult sows as
inuenced by fermentation. Livestock Science 109, 216219.
Kantor, L.S., Lipton, K., Manchester, A., Oliveira, V., 1997. Estimating and
addressing America's food losses. Food Reviews 20, 212.
von Keyserlingk, M.A., Barrientos, A., Ito, K., Galo, E., Weary, D.M., 2012.
Benchmarking cow comfort on North American freestall dairies: Lameness, leg
injuries, lying time, facility design, and management for high-producing Holstein
dairy cows. Journal of Dairy Science 95, 73997408.
Kleen, J.L., Hooijer, G.A., Rehage, J., Noordhuizen, J.P.T.M., 2003. Subacute
ruminal acidosis (SARA): A review. Journal of Veterinary Medicine Series A 50,
406414.
Krause, D.O., Nagaraja, T.G., Wright, A.D.G., Callaway, T.R., 2013. Board-invited
review: Rumen microbiology: Leading the way in microbial ecology. Journal of
Animal Science 91, 331341.
Klling, D.R., Menzi, H., Sutter, F., Lischer, P., Kreuzer, M., 2003. Ammonia,
nitrous oxide and methane emissions from differently stored dairy manure
derived from grass- and hay-based rations. Nutrient Cycling in Agroecosystems
65, 1322.
Le Treut, H., Somerville, R., Cubasch, U., et al., 2007. Historical overview of climate
change. In: Solomon, S., Qin, D., Manning, M., et al. (Eds.), Climate Change
2007: The Physical Science Basis. Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on Climate Change.
Cambridge, UK and New York, NY, USA: Cambridge University Press,
pp. 93128.
Ledgard, S.F., Lieffering, M., Coup, D., O'Brien, B., 2011. Carbon footprinting of
New Zealand lamb from the perspective of an exporting nation. Animal Frontiers
1, 4045.
Lonardi, J., Baumgartner, M., 2004. CO2 efciency in road freight transportation:
Status quo, measures and potential. Transportation Research Part D: Transport
and Environment 9, 451464.
Lin, H., Jiao, H.C., Buyse, J., Decuypere, E., 2006. Strategies for preventing heat
stress in poultry. World's Poultry Science Journal 62, 7185.
Lopez, S., McIntosh, F.M., Wallace, R.J., Newbold, C.J., 1999. Effect of adding
acetogenic bacteria on methane production by mixed rumen microorganisms.
Animal Feed Science and Technology 78, 19.
Mader, T.L., Frank, K.L., Harrington, J.A., Hahn, G.L., Nienaber, J.A., 2009. Potential
climate change effects on warm-season livestock production in the Great Plains.
Climatic Change 97, 529541.
Mann, M.E., Zhang, Z., Hughes, M.K., et al., 2008. Proxy-based reconstructions of
hemispheric and global surface temperature variations over the past two
millennia. Proceedings of the National Academy of Sciences 105,
1325213257.
Mao, H.-L., Wang, J.-K., Zhou, Y.-Y., Liu, J.-X., 2010. Effects of addition of tea
saponins and soybean oil on methane production, fermentation and microbial
population in the rumen of growing lambs. Livestock Science 129, 5662.
Marcott, S.A., Shakun, J.D., Clark, P.U., Mix, A.C., 2013. A reconstruction of
regional and global temperature for the past 11,300 years. Science 339,
11981201.
Mc Geough, E.J., Little, S.M., Janzen, H.H., et al., 2012. Life-cycle assessment of
greenhouse gas emissions from dairy production in Eastern Canada: A case
study. Journal of Dairy Science 95, 51645175.
Millar, N., Robertson, G.P., Grace, P.R., Gehl, R.J., Hoben, J.P., 2010. Nitrogen
fertilizer management for nitrous oxide (N2O) mitigation in intensive corn (Maize)
production: An emissions reduction protocol for US Midwest agriculture.
Mitigation and Adaptation Strategies for Global Change 15, 185204.
Mller, H.B., Sommer, S.G., Ahring, B.K., 2004. Methane productivity of manure,
straw and solid fractions of manure. Biomass and Bioenergy 26, 485495.
Morgavi, D.P., Jouany, J.P., Martin, C., 2008. Changes in methane emission and
rumen fermentation parameters induced by refaunation in sheep. Australian
Journal of Experimental Agriculture 48, 69.
Mosier, A., Kroeze, C., Nevinson, C., et al., 1998. Closing the global N2O budget:
Nitrous oxide emissions through the agricultural nitrogen cycle. Nutrient Cycling
in Agroecosystems 52, 225248.
Odongo, N.E., Bagg, R., Vessie, G., et al., 2007. Long-term effects of feeding
monensin on methane production in lactating dairy cows. Journal of Dairy
Science 90, 17811788.
Odongo, N.E., Or-Rashid, M.M., Kebreab, E., France, J., McBride, B.W., 2007. Effect
of supplementing myristic acid in dairy cow rations on ruminal methanogenesis
and fatty acid prole in milk. Journal of Dairy Science 90, 18511858.
Oenema, O., Velthof, G.L., Yamulki, S., Jarvis, S.C., 1997. Nitrous oxide emissions
from grazed grassland. Soil Use and Management 13, 288295.
Oltjen, J.W., Beckett, J.L., 1996. Role of ruminant livestock in sustainable
agricultural systems. Journal of Animal Science 74, 14061409.
Omonode, R.A., Vyn, T.J., Smith, D.R., Hegymegi, P., Gl, A., 2007. Soil carbon
dioxide and methane uxes from long-term tillage systems in continuous corn
and cornsoybean rotations. Soil and Tillage Research 95, 182195.
Oreskes, N., 2004. The scientic concensus on climate change. Science 306, 1686.
Owens, F.N., Secrist, D.S., Hill, W.J., Gill, D.R., 1998. Acidosis in cattle: A review.
Journal of Animal Science 76, 275286.
Park, K.-H., Thompson, A.G., Marinier, M., Clark, K., Wagner-Riddle, C., 2006.
Greenhouse gas emissions from stored liquid swine manure in a cold climate.
Atmospheric Environment 40, 618627.
Petersen, S.O., Amon, B., Gattinger, A., 2005. Methane oxidation in slurry storage
surface crusts. Journal of Environmental Quality 34, 455461.
Pitesky, M.E., Stackhouse, K.R., Mitloehner, F.M., 2009. Clearing the air. Advances
in Agronomy 103, 140.
Place, S.E., Mitloehner, F.M., 2010. Invited review: Contemporary environmental
issues: A review of the dairy industry's role in climate change and air quality
and the potential of mitigation through improved production efciency. Journal of
Dairy Science 93, 34073416.
Place, S.E., Mitloehner, F.M., 2012. Beef production in balance: Considerations for
life cycle analyses. Meat Science 92, 179181.
Rotz, C.A., 2004. Management to reduce nitrogen losses in animal production.
Journal of Animal Science 82, E119E137.
Rotz, C.A., Montes, F., Chianese, D.S., 2010. The carbon footprint of dairy
production systems through partial life cycle assessment. Journal of Dairy
Science 93, 12661282.
Rotz, C.A., Soder, K.J., Skinner, R.H., et al., 2009. Grazing can reduce the
environmental impact of dairy production systems. Forage and Grazinglands
doi:10.1094/fg-2009-0916-01-rs.
Russell, J.B., 2002. Rumen Microbiology and Its Role in Ruminant Nutrition. Ithaca,
NY: James B. Russell.
Russell, J.B., Houlihan, A.J., 2003. Ionophore resistance of ruminal bacteria and its
potential impact on human health. FEMS Microbiology Reviews 27, 6574.
Salminen, E., Rintala, J., 2002. Anaerobic digestion of organic solid poultry
slaughterhouse waste A review. Bioresource Technology 83, 1326.
Seinfeld, J.H., Pandis, S.N., 2006. Atmospheric Chemistry and Physics: From Air
Pollution to Climate Change. Hoboken, NJ: Wiley.
Shaw, S.L., Mitloehner, F.M., Jackson, W., et al., 2007. Volatile organic compound
emissions from dairy cows and their waste as measured by proton-transferreaction mass spectrometry. Environmental Science and Technology 41,
13101316.
Smith, K.A., Thomson, P.E., Clayton, H., McTaggart, I.P., Conen, F., 1998. Effects of
temperature, water content and nitrogen fertilisation on emissions of nitrous
oxide by soils. Atmospheric Environment 32, 33013309.
Solomon, S., Qin, D., Manning, M., et al., 2007. Technical summary. In: Solomon,
S., Qin, D., Manning, M., Chen, Z., Marquis, M., et al. (Eds.), Climate Change
2007: The Physical Science Basis. Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on Climate Change.
Cambridge, UK and New York, NY, USA: Cambridge University Press,
pp. 79131.
St-Pierre, N.R., Cobanov, B., Schnitkey, G., 2003. Economic losses from heat stress
by US livestock industries. Journal of Dairy Science 86, E52E77.
Steinfeld, H., Gerber, P., Wassenaar, T., et al., 2006. Livestock's Long Shadow:
Environmental Issues and Options. Rome, Italy: Food and Agriculture
Organization of the United Nations.
Sun, H., Trabue, S.L., Scoggin, K., et al., 2008. Alcohol, volatile fatty acid, phenol,
and methane emissions from dairy cows and fresh manure. Journal of
Environment Quality 37, 615622.
Thoma, G., Popp, J., Nutter, D., et al., 2013. Greenhouse gas emissions from milk
production and consumption in the United States: A cradle-to-grave life cycle
assessment circa 2008. International Dairy Journal 31, S3S14.
Walthall, C.L., Hateld, J., Backlund, P., et al., 2012. Climate Change and
Agriculture in the United States: Effects and Adaptation. Washington, DC: USDA.
Wang, S.-Y., Huang, D.-J., 2005. Assessment of greenhouse gas emissions from
poultry enteric fermentation. Asian-Australian Journal of Animal Science 18,
873878.
Wang, Q., Thompson, E., Parsons, R., Rogers, G., Dunn, D., 2011. Economic
feasibility of converting cow manure to electricity: A case study of the CVPS
Cow Power program in Vermont. Journal of Dairy Science 94, 49374949.
Weber, C.L., Matthews, H.S., 2008. Food-miles and the relative climate impacts of
food choices in the United States. Environmental Science & Technology 42,
35083513.
West, J.W., 2003. Effects of heat-stress on production in dairy cattle. Journal of
Dairy Science 86, 21312144.
255
Relevant Websites
http://www.extension.org/pages/60702/animal-agriculture-and-climate-change
Animal Agriculture and Climate Change.
http://www.ars.usda.gov/main/docs.htm?docid=17355
Dairy Greenhouse Gas Model from the Pasture Systems and Watershed
Management Research Unit in the Agriculture Research Service at the United
States Department of Agriculture (USDA-ARS).
http://www.fao.org/home/en/
Food and Agriculture Organization of the United Nations.
http://www.ipcc.ch/
Intergovernmental Panel on Climate Change.
http://climate.nasa.gov/
NASA Global Climate Change.
http://www.epa.gov/climatechange/
US Environmental Protection Agency Climate Change.
Glossary
Carbon dioxide Gas in the atmosphere consumed by
plants during photosynthesis.
Chilling hours The duration of temperature below a given
threshold required for plants to ower.
Direct effects Effects of climate on plants or animals, for
example, direct effect of temperature on plant growth.
Diseases Pathogens in the environment which cause a
reduction in growth or reduce the quality of the product.
Indirect effects Effects of climate on an organism which
affects the growth or productivity of the economic product,
for example, increase in disease pressure induced by climate
on a given plant.
Introduction
In the past 10 years, there has been renewed discussion about
the implications of climate change for agriculture. Increasing
evidence that our climate is changing and impacting agriculture is leading to understanding of the potential pressures
on our ability to ensure an adequate food supply for the
increasing human population. Rising carbon dioxide (CO2),
increasing temperatures, and more variable precipitation affect agricultural systems and no region of the world will be
exempt from these effects. Understanding these effects on
plants will help us develop cropping systems that are resilient
to climate stresses and identify adaptation strategies to cope
with climate change. Our goal in this article is to provide an
understanding of the implications of climate change on
cropping systems.
Climate has been changing and during the past 50 years
there has been an increase in CO2 concentration from 325 to
390 ppm with a projection of further increases to nearly
500 ppm by the middle of the twenty-rst century (IPCC,
2007a). During the twentieth century, global average air temperatures increased by approximately 0.74 C (0.560.92 C)
(IPCC, 2007a) with projections of further increases in surface
air temperatures of between 1.1 and 2.9 C by 2100 under
emission scenarios, which have adopted aggressive methods to
reduce CO2 emissions, and by up to 2.05.4 C under scenarios
with higher emission rates. For agricultural cropping systems,
trends in average temperature are not as important as the
diurnal range, and projections are for increasing minimum
temperatures more than maximum temperatures. Winter temperatures have increased more rapidly than summer temperatures, and nighttime minimum temperatures have warmed
more than daytime maximums. Across the US (and elsewhere),
record high temperatures are three times higher than the
number of record cold events (IPCC, 2007a; Meehl et al., 2009).
Meehl et al. (2007) summarized that on a global basis it is very
256
likely that heat waves will be more intense, more frequent, and
longer lasting in a future warmer climate. Cold episodes are
projected to decrease signicantly in a future warmer climate.
Almost everywhere, daily minimum temperatures are projected
to increase faster than daily maximum temperatures, leading to
a decrease in diurnal temperature range. Observations of
temperature have shown that 10 of the warmest 11 years have
occurred since 2001 (Hansen et al., 2012). Coupled with these
changes is the decrease in the number of frost days by 10% in
the eastern half of the US and an increase in the length of the
growing season by over 10 days (Karl et al., 2009). Temperatures are increasing and there are implications for plant growth
and also the rate at which plants transpire water because as
temperatures increase so does the saturated water vapor in the
air creating an atmosphere with an increased rate of water use
by crops.
Trends in precipitation are more difcult to assess; however, overall precipitation amounts and heavy precipitation
events have increased in most regions of the world; while
occurrences of drought has been increasing, particularly since
1970 (IPCC, 2007a; Allison et al., 2009). Karl and Knight
(1998) found that more than half of the observed increases in
total annual precipitation across the US between 1910 and
1996 were due to increases in frequency of large events (upper
10 percentile of measured daily values). Groisman et al.
(2005) examined records of measured daily rainfall data
across land areas of the world and found trends of increased
probability of extreme events for many regions outside of the
tropics.
In addition to temperature, precipitation, and CO2 changing, there is evidence that other components of the atmosphere changing as well. Solar radiation is one of the primary
factors affecting plant growth because plants capture sunlight
and convert this energy into sugars without which they would
not grow. The amount of solar radiation reaching the surface
of the earth is affected by cloud cover and the amount of
doi:10.1016/B978-0-444-52512-3.00003-6
6
World grain production
5
Yield (Mg ha1)
257
4
3
2
Wheat
Maize
Rice
1
0
1960
1970
1980
1990
2000
2010
Year
Figure 1 World grain production for wheat, maize, and rice since
1960 (www.fas.usda.gov).
Growth
response
Maximum
Broccoli
Moderate
Maize
Minimum
0
10
15
20
25
30
35
40
Temperature (C)
Figure 2 Idealized temperature response for plants showing the
maximum, minimum, and optimal temperatures for a warm-season
crop (maize) and a cool-season crop (broccoli) (Hateld et al., 2011).
258
Precipitation
Precipitation supplies water to the soil from which plants extract water. Precipitation is one of the most difcult climate
parameters to predict into the future; however, there is evidence that precipitation events will be more intense and there
may be shifts in its seasonality. Across the Midwest US, the
projection is for more precipitation to occur in the spring and
for a reduction in summer. These shifts have signicant
implications because Midwestern cropping patterns have developed to utilize the precipitation occurring during the
summer and any decline during that period reduces the
available soil water leading to a reduction in plant growth.
As the water supply in the soil is reduced, the plant is no
longer able to extract sufcient amounts of water and stomates
begin to close. As they close they no longer allow water to exit
(thereby reducing cooling benets), while also limiting the
amount of CO2 that enters from the atmosphere into the leaf.
Without CO2 being converted into sugars in the leaf, the plant
is no longer growing and productivity suffers.
Because the plant is dependent on the soil to supply the
water needed for plant growth, there is an important role for
soil in response to climate change. Soils absorb and hold water
because of their organic matter content and high-quality soils
with large amounts of organic matter store more water. Organic matter content in soils is replenished by adding organic
material and avoiding excessive tillage. These processes have
been recently reviewed by Hateld and Wright-Morton (2013)
in which they discussed how soils become marginal in their
functionality because of the loss of organic matter content and
erosion. Maintenance of the soil to increase water availability
can help reduce the impact of the increasing uncertainty in
precipitation. Soil management to decrease the potential for
erosion from the increased intensity of precipitation events
will be necessary to maintain crop cover either as growing
Carbon Dioxide
Carbon is one of the fundamental building blocks for all plant
compounds. Through the process of photosynthesis, CO2 is
converted into sugars which are ultimately converted into
proteins, starches, amino acids, etc. through a variety of
metabolic processes. Rising levels of CO2 in the atmosphere
has a positive effect on plant growth and development. Even
using conservative estimates, the current levels of approximately 390 ppm will increase at a faster rate than originally
expected to nearly 450500 ppm by 2050 (Karl et al., 2009).
To assess the effect of increasing CO2 on plant growth, enclosed chambers and free-air CO2 enrichment (FACE) studies
have been conducted in which plants have been exposed to
higher levels of CO2 typical of what may be expected in future
climates. These studies have shown a positive effect on plant
growth (Kimball, 1983, 2011) with increasing CO2 concentrations increasing growth by ~10% in plants such as maize
and sorghum, which already have the highly efcient C4
photosynthetic pathway, to increases in growth of greater than
30% in C3 plants, such as beans, peanut, rice, wheat, soybean,
and others. In general, doubling CO2 caused an approximate
30% increase in reproductive yield of C3 species and a less
than 10% increase for C4 species. Differences among the
259
Ozone
Although attention has been directed toward CO2 increases as
part of climate change, less attention has been given to ozone
(O3), although concentrations of this gas have increased in
rural areas of the US over the past 50 years, and are expected to
increase further over the next 50 years. Currently, Midwest and
Eastern US have some of the highest rural O3 levels on the
globe. Ozone concentrations increase toward the east and
south, showing levels in Illinois exceed those in Nebraska,
Minnesota, and Iowa. Only Western Europe and Eastern China
have similar (high) levels. Argentina and Brazil and most of
the Southern Hemisphere have much lower levels of O3, and
expect to see little increase in O3 over the next 50 years. Increasing O3 levels will impact crop production, and efforts to
increase O3 tolerance will be important to maintain agricultural productivity. Future trends in global O3 concentrations are linked to Intergovernmental Panel on Climate
Change scenarios, so that agricultural impacts from O3 can be
considered along with the other components in climate
change. Modeled predictions for O3 based on expected economic development and planned emission controls in individual countries estimate signicant increases in the annual
mean surface O3 concentrations in major agricultural areas of
the northern hemisphere (Dentener et al., 2006).
Physiological responses to increased O3 concentrations
have been studied using similar approaches to assessing the
effects of increased CO2. After uptake through the leaf's stomata, ozone interacts with plants' cellular processes, inhibiting
photosynthesis, growth, and yield. Detrimental effects result
from a combination of chemical toxicity and physiological
responses that either amplify or inhibit injury and in many
regions of the US and worldwide (Booker et al., 2009; Morgan
et al., 2006) current ambient O3 levels are already impacting
yields of crops such as alfalfa, bean, clover, cotton, peanut,
potato, rice, soybean, sugar cane, and wheat. In some grass
species, changes in leaf chemistry from elevated O3 exposure
have caused reduced nutritional quality of the grass used to
support grazing animals. This loss of nutritional quality in
these grasslands may be more signicant than biomass losses
(Muntifering et al., 2006). Ozone changes are often not considered part of the climate change puzzle; however, the
changing temperature and humidity of the atmosphere combined with continued fossil fuel combustion will create conditions favorable for O3 formation and higher atmospheric
concentrations.
US maize production
12 000
Grain yield (kg ha1)
260
10 000
8000
6000
4000
2000
0
1940
1960
1980
Year
2000
2020
Forage crops
Forage grasses exhibit the same responses to temperature as
other plant species; however, grasslands are made up of mixtures of plants and rising temperatures may cause a change in
the relative dominance of different species in the community.
These changes in community structure have been discussed
and evaluated relative to climate change by Izaurralde et al.
(2011). The quality aspect of forages is even more critical than
in grains because of the direct consumption of the forage as
the primary source of nutrition for the animal. Efcient animal
production from pastureland and rangeland systems depends
on both forage quality and quantity. Positive and negative
changes in forage quality are possible as a result of atmospheric and climatic change when we examine the potential
vegetation changes and environmental effects on forage protein, carbohydrate, and ber content. Studies on forage quality
have helped to reveal the linkage between changing CO2
concentrations and a plant's ability to extract N from the soil.
Warming temperatures cause N concentrations in the forage to
decrease partially because of the positive effect of increasing
CO2 on enhancing vegetative growth (Morgan et al., 2004).
The fact that these effects will vary among species highlights
the need to understand interactions among all the plant species in a community and how they respond to climate change.
Forage growth is directly linked to precipitation because
many of the production areas are in regions with limited
precipitation during the growing season. Increasing variation
in precipitation will lead to increased variation in forage
production which, in turn, will affect livestock production.
These variations in forage production will have worldwide
impacts on animal production.
Specialty crops
Annual specialty crops include many vegetable and fruit
plants, each with their own environmental ranges. Climate
change will have an impact on them in a similar way as grain
crops; however, because these crops are often directly consumed, the effects of temperature or water stress are more
noticeable.
Temperature is a major environmental change expected to
affect production of annual specialty crops as temperature responses vary more widely among specialty than other crops,
261
Perennial crops
Perennial crops are typically considered as those that are more
permanent, requiring a number of growth cycles before fruit is
produced. One of the characteristics of these plants is their
requirement for winter chilling before owering the next
spring. As discussed earlier in the Section Temperature, there is
evidence that with warming winter temperatures some perennial crops may not have their chilling hour requirement
satised, which will limit owering and ultimately fruit set. An
additional concern is that warm winters may promote early
bud and ower development and late season frost events will
damage these owers and fruit or nut formation. Perennial
crops are valued for a combination of their total production
and the quality of the harvested product, for example, size of a
peach or apricot, the red blush on an apple, oil content of
olives, or the quality of wine produced from a particular
vineyard. By nature, perennial crop production is long-term
and climate change will create interesting problems for production because production areas have less exibility in their
location after establishment and because the production
262
Diseases
Insects
Increasing air temperatures are benecial to insect pests
and like plants, rising temperatures accelerate every aspect of
an insect's life cycle, and warmer winters reduce winter
mortality. Insects, like plants, have an upper threshold of
temperatures above which there is mortality. Similar to plant
response, warming temperatures will cause some insects to
thrive and expand their range, whereas others will have a reduced viability. Warmer temperatures during the summer increases the growth of insect populations; however, a more
positive benet on insect populations is caused by lengthening
of the growing season, which results in more damage to plants
(Bradshaw and Holzapfel, 2010). Increasing air temperatures
also affect the range of insects because they encounter a wider
range of environments in which they can survive; however,
each insect species has a specic range of temperatures in
which it develops, so not all insect populations will automatically expand with warmer temperatures. Insects also require water for survival and limited water supplies will affect
populations.
Temperature plays a large role in the geographic ranges of
insect pests because of the impact it has on the ability of insects to survive winter conditions and the presence, and nutritional quality of the plants upon which they feed. Insects are
Leaf and root pathogens will be favored by increases in humidity and the frequency of heavy rainfall events projected for
many parts of the world will create a more conducive environment for many different pathogens (Garrett et al., 2006,
2011). Increases in temperature also favor populations of
pathogens because the growth rate of these organisms is
temperature dependent. Incidences of warm, moist environments will increase the potential for disease to occur on plant
leaves and fruit (Wu et al., 2011). However, it is difcult to
develop general statements that the incidence of pathogens
will increase because even, short- to medium-term droughts
reduce the duration of leaf wetness causing a reduction in
pathogen attack on leaves. The development of a better
understanding of the effect of climate change on pathogens
remains a challenge for agriculture and a major topic for future
investigation. Protection of the growing plant, and the harvested product placed into storage, from pathogens remains a
challenge. Improving our understanding of the role climate
has on these organisms will increase our ability to ensure a
secure food supply for the future.
Weeds
Weed species are a range of plants which exist within plant
production systems that compete with crops for water, light,
Genetics
All species show a range of genetic responses to selection
pressures. Tolerance of plants to high temperatures can be assessed by evaluating phenotypic traits that promote heat tolerance during owering, increased harvest index (ratio of
reproductive production to total biomass production), smaller
leaves, or diverting more growth into root systems to increase
water uptake. One adaptation strategy would be to select plants
for peak owering times in cooler periods of the day to assist
pollen survival and increase grain set (Prasad et al., 2006).
Another selection target would be to identify plants that demonstrate different recovery responses to high temperature or
water stress. Observations that plants show increased transpiration efciency with increasing CO2 suggest that there may
be genetic differences in these responses; however, these relationships have not been fully evaluated to determine if there is
potential in genetic variation to achieve enhanced transpiration
efciency through genetic manipulation.
Assessing the genetic response of plants to climate variables
has not been the focus of many studies partly because they
require specialized facilities capable of inducing temperature
263
Management
Management as an adaptation strategy offers the most immediate promise to alleviate the effects of climate change. One
obvious management strategy is to provide water by irrigation
to supplement inadequate precipitation. Irrigation has proven
very effective in many parts of the world and efforts to increase
irrigation use efciency and reduce waste have proven benecial to enhancing production under limited water supplies.
Use of drip or trickle irrigation to supply water only to the
plant has shown promise in many parts of the world. However, for irrigation to be effective there has to be an adequate
supply of surface or ground water to meet crop demands.
Other management practices involve changes in planting
dates so that plants grow and mature during times of the year
with reduced probability of high temperature or water stress.
There are limits to the range of potential planting dates in
many environments because plant growth may be limited by
cold in the early spring if the temperatures are below the lower
threshold for development (Figure 2). A more simple management approach may be to alter plant selection and grow
plants which have a different temperature response curve. An
example of this would be to produce wheat or other small
grain, which can be planted in the fall and matures in the early
summer before the primary occurrence of high temperatures or
increased water demand, in place of corn, which is planted in
the spring and is producing grain during the warmest and least
rainy period of the year in a number of environments. Another
alternative would be to replace corn with sorghum or millet,
which is much more tolerant of water stress conditions than
corn, and under water limited environments performs better in
producing a grain. In many arid environments these types of
management decisions offer the potential for ensuring a grain
supply.
There are observations collected from ongoing research on
grain quality, which suggests that management of nutrient
supply for plants should be considered in adaptation strategies
to cope with climate stress. Nutrient management is a portion
of the soil management complex, which may hold some keys
to helping build more resilient crop production systems to the
changing climate. As part of the soil management complex, we
need to ensure that soils have maximum water-holding capacity and nutrient cycling capabilities because these are related
to negating the negative effects of climate stress on plant
growth and development. Strategies to achieve these goals
were recently reviewed by Hateld et al. (2011). There is no
single solution to this problem and development of effective
adaptation strategies will require efforts which integrate across
a number of approaches.
Conclusion
Climate change is occurring with the expectation for increased
temperatures, more variable precipitation, increasing CO2,
264
increasing O3, and higher humidity over the next few decades.
Agriculture has been subjected to climate change in the past
and we have evolved our production systems to cope with
interannual and annual variations in weather. The concern is
that the rate of climate change and the magnitude of the
change may begin to exceed the capacity of some plant species
to adapt resulting in a decline in production. To place this in
perspective, recent analysis for the impacts of increased temperature on wheat production in India by Ortiz et al. (2008)
shows the fragile nature of our production systems. The consequences of increasing temperatures, which are in the moderate range of those suggested by climate scientists, would
create a shortage of wheat production in India and cause the
transition from a self-sufcient country to an importer of
wheat to meet population demands.
Climate change impacts all plant growth and productivity
and understanding how to develop production systems, which
can cope with the increasing temperature and water stress
offers a challenge to be able to maintain adequate food supplies for the increasing population. The effects of different
climate variables on plant growth, development, and yield
demonstrated shows where we need to begin to focus our
efforts to meet this challenge.
References
Ainsworth, E.A., Davey, P.A., Bernacchi, C.J., et al., 2002. A meta-analysis of
elevated [CO2] effects on soybean (glycine max): Physiology, growth and yield.
Global Change Biology 8, 695709.
Allison, I., Bindoff, N.L., Bindschadler, R.A., et al., 2009. The Copenhagen
diagnosis, 2009: Updating the world on the latest climate science. Sydney,
Australia: University of New South Wales Climate Change Research Centre
(CCRC), 60 p.
Altermatt, F., 2010. Climatic warming increases voltinism in European butteries and
moths. Proceedings of the Royal Society B, vol. 277. London, UK: Royal Society
Publishing, pp. 12811287.
Bale, J.S., Hayward, S.A.L., 2010. Insect overwintering in a changing climate.
Journal of Experimental Biology 213, 980994.
Bernacchi, C.J., Kimball, B.A., Quarles, D.R., Long, S.P., Ort, D.R., 2007. Decreases
in stomatal conductance of soybean under open-air elevation of CO2 are closely
coupled with decreases in ecosystem evapotranspiration. Plant Physiology 143,
134144.
Booker, F.L., Muntifering, R., McGrath, M.T., et al., 2009. The ozone component of
global change: Potential effects on agricultural and horticultural plant yield,
product quality and interactions with invasive species. Journal of Integrative Plant
Biology 51, 337351.
Kimball, B.A., Idso, S.B., 1983. Increasing atmospheric CO2: Effects on crop yield,
water use, and climate. Agricultural Water Management 7, 5572.
Lee, J., DeGryze, S., Six, J., 2011. Effect of climate change on eld crop
production in the California's Central Valley. Climatic Change 109 (Suppl.),
S335S353.
Lobell, D.B., Schlenker, W., Costa-Roberts, J., 2011. Climate trends and global crop
production since 1980. Science 333, 208218.
Luedeling, E., Zhang, M., Girvetz, E.H., 2009. Climatic changes lead to declining
winter chill for fruit and nut trees in California during 19502099. PLOS ONE 4,
19. doi:10.1371/journalpone.0006166.
Medvigy, D., Beaulieu, C., 2011. Trends in daily solar radiation and precipitation
coefcients of variation since 1984. Journal of Climate 25, 13301339.
Meehl, G.A., Stocker, T.F., Collins, W.D., et al., 2007. Global climate projections. In:
Solomon, S., Qin, D., Manning, M. et al. (Eds.), Climate Change 2007: The
Physical Science Basis. Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on Climate Change.
Cambridge, UK and New York, USA: Cambridge University Press.
Meehl, G.A., Tebaldi, C., Walton, G., Easterling, D., McDaniel, L., 2009. Relative
increase of record high maximum temperatures compared to record low
minimum temperatures in the US. Geophysical Research Letters 36, 23.
doi:10.1029/2009GL040736.
Morgan, P.B., Mies, T.A., Bollero, G.A., Nelson, R.L., Long, S.P., 2006. Season-long
elevation of ozone concentration to projected 2050 levels under fully open-air
conditions substantially decreases the growth and production of soybean. New
Phytologist 170, 333343.
Morgan, J.A., Mosier, A.R., Milchunas, D.G., et al., 2004. CO2 enhances
productivity, alters species composition, and reduces digestibility of shortgrass
steppe vegetation. Ecologcial Applications 14, 208219.
Morison, J.I.L., 1987. Intercellular CO2 concentration and stomatal response to CO2.
In: Zeiger, E., et al. (Eds.), Stomatal Function. Stanford, CA: Stanford University
Press, pp. 229251.
Muntifering, R.B., Chappelka, A.H., Lin, J.D., Karnosky, D.F., Somers, G.L., 2006.
Chemical composition and digestibility of trifolium exposed to elevated ozone
and carbon dioxide in a free air (FACE) fumigation system. Functional Ecology
20, 269275.
Nearing, M.A., Jetten, V., Baffaut, C., et al., 2005. Modeling response of soil
erosion and runoff to changes in precipitation and cover. CATENA 61 (23),
131154.
O'Neal, M.R., Nearing, M.A., Vining, R.C., Southworth, J., Pfeifer, R.A., 2005.
Climate change impacts on soil erosion in midwest United States with changes
in crop management. CATENA 61, 165184.
265
Ortiz, R., Sayre, K.D., Govaerts, B., et al., 2008. Climate change: Can wheat beat the
heat? Agriculture, Ecosystems & Environment 126, 4658.
Pettigrew, W.T., 2008. The effect of higher temperatures on cotton lint yield
production and ber quality. Crop Science 48, 278285.
Prasad, P.V.V., Boote, K.J., Allen, Jr., L.H., 2006. Adverse high temperature effects
on pollen viability, seed-set, seed yield and harvest index of grain-sorghum
(Sorghum bicolor L. Moench) are more severe at elevated carbon dioxide
due to higher tissue temperatures. Agricultural and Forest Meteorology 139,
237251.
Stanhill, G., Cohen, S., 2001. Global dimming: A review of the evidence for a
widespread and signicant reduction in global radiation with discussion of its
probable causes and possible agricultural consequences. Agricultural and Forest
Meteorology 107, 255278.
Stanhill, G., Cohen, S., 2005. Solar radiation changes in the United States during
the twentieth century: Evidence from sunshine duration measurements. Journal of
Climate 18, 15031512.
Tesfaendrias, M.T., McDonald, M.R., Warland, J., 2010. Consistency of long-term
marketable yield of carrot and onion cultivars in muck (organic) soil in relation
to seasonal weather. Canadian Journal of Plant Science 90 (5), 755765.
Timlin, D., Lutfor Rahman, S.M., Baker, J., et al., 2006. Whole plant photosynthesis,
development, and carbon partitioning in potato as a function of temperature.
Agronomy Journal 98, 11951203.
Tobin, P.C., Nagarkatti, S., Loeb, G., Saunders, M.C., 2008. Historical and projected
interactions between climate change and insect voltinism in a multivoltine
species. Global Change Biology 14, 951957.
Walthall, C.L., Hateld, J.L., Backlund, P., et al., 2012. Climate change and
agriculture in the United States: Effects and adaptation. USDA Technical Bulletin
1935, Washington, DC: USDA, 192 p.
Wolfe, D., Ziska, L.H., Petzoldt, C., et al., 2008. Projected change in climate
thresholds in the northeastern US: Implications for crops, pests, livestock, and
farmers. Mitigation and Adaptation Strategies for Global Change 13 (5),
555575.
Woodward, F.I., Williams, B.G., 1987. Climate and plant distribution at global and
local scales. Plant Ecology 69, 189197.
Wu, F., Bhatnagar, D., Bui-Klimke, T., et al., 2011. Climate change impacts on
mycotoxin risks in US maize. World Mycotoxin Journal 4, 7993.
Ziska, L.H., 2004. Rising carbon dioxide and weed ecology. In: Inderjit (Ed.), Weed
Biology and Management. The Netherlands: Kluwer Academic Publishers,
pp. 159176.
Ziska, L.H., 2010. Elevated carbon dioxide alters chemical management of Canada
thistle in no-till soybean. Field Crops Research 119, 299303.
Glossary
Chilling requirement Minimum quantity of exposure to
cold temperatures required to break dormancy allowing the
tree to ower normally.
Evapotranspiration The sum of evaporation and plant
transpiration from the Earth's land surface to atmosphere.
Phenology The study of periodic plant and animal life
cycle events and how these are inuenced by seasonal and
interannual variations in climate.
Introduction
Horticulture Species Range
The horticulture industry is represented by a diversity of perennial and annual crops, ranging through fruits, nuts, vegetables, edible fungi, and extractive crops (essential oils), with
amenity horticulture, cut owers and turf also categorized as
horticultural crops. Globally, in 2010 approximately 600
million tons of fruit, 9 million tons of tree nuts, and more
than 1.7 billion tons of vegetables were produced (FAOSTAT,
2012). In contrast to many other agricultural industries,
horticultural products are of high value and are often grown
on relatively small areas of land and under dry-land, irrigated,
or covered conditions. There often exists a high level of
management input aimed at ameliorating climate risks (e.g.,
via irrigation) despite this, many activities retain considerable
exposure.
266
Africa (Mathooko and Mutui, 2011) and Asia (Xue and Revell,
2009). China, for example, ranked second in the world as an
exporter of processed vegetables and fourth for unprocessed
vegetables in 2005 (Xue and Revell, 2009). Some production
declines in cooler growing regions of Europe have been related
to increasing oil prices affecting costs of greenhouse heating.
Increasing labor costs, and in some countries a shortage of
seasonal workers, has also been a factor in productivity decline
in Europe (Dehnen-Schmutz et al., 2010).
doi:10.1016/B978-0-444-52512-3.00240-0
267
900
800
Production (tons)
Millions
700
600
500
400
300
200
100
2000
Oceania
Europe
Asia
Americas
Africa
Oceania
Europe
Asia
Americas
Africa
Oceania
Europe
Asia
Americas
Africa
Vegetables and
melons
2010
Figure 1 Horticultural production of fruits and vegetables from 1980 to 2010 from different regions of the world (FAOSTAT, 2012).
Extreme Weather
Extreme weather and climate events such as frost, drought,
heat waves, hail, cyclones, and oods all have the potential to
impact severely on horticultural production. Under global
warming, changes in the frequency, intensity, spatial extent,
duration, and the timing of extreme weather is likely. It should
be appreciated that some climate extremes (e.g., droughts)
may be the result of a combination of weather events that are
not extreme when considered independently (IPCC, 2012).
268
Table 1
Ranking of major (fresh) horticultural production categories (tons produced) in different regions and globally
Africa
Americas
Asia
Europe
Oceania
World
Fruit (fresh)
1
Plantains
2
Bananas
3
Oranges
4
Watermelons
Oranges
Bananas
Grapes
Apples
Grapes
Apples
Oranges
Watermelons
Grapes
Bananas
Apples
Oranges
Bananas
Watermelons
Apples
Oranges
Peaches and
nectarines
Kiwifruit
Grapes
Mangoes,
mangosteens,
and guavas
Plantains
Plantains
Mangoes,
mangosteens,
and guavas
Grapes
Watermelons
Bananas
Apples
Mangoes,
mangosteens,
and guavas
Oranges
Pineapples
Grapes
Pears
Pineapples
Dates
Watermelons
Watermelons
Pineapples
Other melons
(including
cantaloupes)
Pears
Peaches and
nectarines
Apples
10
Other melons
(including
cantaloupes)
Mangoes,
mangosteens,
and guavas
Papayas
Tangerines,
mandarins,
and clementines
Peaches and
nectarines
Other melons
(including
cantaloupes)
Tangerines,
mandarins, and
clementines
Strawberries
Vegetables (fresh)
1
Cassava
2
Yams
3
Potatoes
Potatoes
Cassava
Tomatoes
Potatoes
Sweet potatoes
Tomatoes
4
5
Tomatoes
Sweet potatoes
Onions, dry
Maize and green
Onions, dry
Cassava
Cucumbers
and gherkins
Onions, dry
Taro (cocoyam)
Chillies and
peppers, green
Chillies and
peppers, green
Carrots and turnips
Cabbages and
other brassicas
Eggplants
(aubergines)
Cabbages and
other brassicas
Pumpkins, squash,
and gourds
Sweet potatoes
Pumpkins, squash,
and gourds
Garlic
10
Pears
Other melons
(including
cantaloupes)
Pears
Tangerines,
mandarins,
and clementines
Tangerines,
mandarins,
and clementines
Potatoes
Tomatoes
Cabbages and
other brassicas
Onions, dry
Carrots and turnips
Potatoes
Sweet potatoes
Tomatoes
Potatoes
Cassava
Tomatoes
Yams
Taro (cocoyam)
Sweet potatoes
Onions, dry
Cucumbers and
gherkins
Lettuce and chicory
Maize, green
Cabbages and
other brassicas
Cucumbers and
gherkins
Yams
Pumpkins, squash,
and gourds
Chillies and
peppers, green
Cauliowers and
broccoli
Carrots and
turnips
Pumpkins,
squash,
and gourds
Onions, dry
Onions (including
shallots), green
Eggplants
(aubergines)
Carrots and turnips
Source: Reproduced from FAOSTAT, 2012. Food and Agriculture Organization of the United Nations website. Available at: http://faostat.fao.org/default.aspx (accessed 14.01.14).
Temperature
change (C)
2030 A1B
0.1 0.4
0.5 0.8
0.9 1.2
1.3 1.6
1.7 2.0
2.1 2.4
2.5 2.8
269
60 N
30 N
0
30 S
60 S
(a)
Precipitation
change (%)
2030 A1B
+21 +24
+17 +20
+13 +16
+9 +12
+5 +8
+1 +4
3 0
7 4
10 8
60 N
30 N
0
30 S
60 S
(b)
Figure 2 Projected annual temperature change (1C) (a), and annual rainfall change (%) (b) by 2030 (A1B emission scenario) as it varies spatially
across the globe. Results depicted indicate the median of 23 CMIP3 climate models (Watterson and Whetton, 2011).
270
Central Victoria
140
Marsanne
DOY at maturity
120
Shiraz (Mc)
100
80
60
40
(a)
20
140
DOY at maturity
120
100
80
60
40
Slope = 0.3 days per year P=0.10
20
(b)
Mornington Peninsula
140
DOY at maturity
120
Chardonnay
Pinot noir
100
80
60
40
20
(c)
Margaret River
140
DOY at maturity
120
Cabernet sauvignon
100
80
60
40
Slope = +0.1 days per year P=0.821
20
1930
1940
1950
1960
1970
1980
1990
2000
2010
Vintage year
Figure 3 The observed day of year (DOY) at maturity recorded for six blocks from four regions (a) Central Victoria: Marsanne (19392009) (solid
circles), Shiraz (Mc) (19402009) (open circles) and (b) Rutherglen: Muscat a Petit Grains (19452009) (c) Mornington Peninsula: Chardonnay
(19852009) (solid circles) and Pinot Noir (19842009) (open circles), and (d) Margaret River: Cabernet Sauvignon (19732009). The best t
linear regression indicates the average trend in the maturity day (Webb et al., 2011).
195
195
175
175
155
155
135
135
115
95
285
275
265
115
DOY
Number of days
Number of days
295
255
95
(a)
3 C
3 C
140
3 C
15
2 C
15
Historical
225
2 C
35
1 C
35
Historical
235
2 C
55
1 C
55
Historical
75
1 C
245
75
140
285
120
120
265
255
3 C
2 C
1 C
Historical
3 C
2 C
245
1 C
60
3 C
60
2 C
80
1 C
80
(b)
DOY
100
Historical
Number of days
100
Historical
Number of days
275
Figure 4 Alternate simulations for projected changes to pome fruit full bloom timing at (a) cooler and (b) warmer location. Projections are
relative to 1, 2, and 3 1C increases to mean global temperatures. The relative inuence of the chill and growth periods on expected owering
timing led different prediction of owering delay or owering advancement (unpublished data).
271
272
although chill is prolonged with a warming climate, the projected warmer spring still dominates the dormancy-breaking
process, leading to earlier bloom time. In contrast, in a warmer
region (Figure 4(b)), chill accumulation is already marginal in
the current climate. With warming, chill is noticeably delayed
and the limited inuence of warming in spring does not compensate for this, leading to an overall delay in budburst. This
regional variation in response has implications for future
changes to frost incidence during the owering period for
apples (Darbyshire et al., 2013c).
It should be appreciated that changes to the timing of
owering is yet to be fully understood from a physiological
point of view, with greater research into phenologytemperature
relationships, as well as development of models to represent
these, required (Darbyshire, 2013).
The physiology of tropical crops may also be inuenced by
warmer winters. Temperatures between 11 and 14 1C are optimal for ower growth in lychee (Gao and Huang, 2004).
Winter temperatures higher than this optimal may encourage
vegetative over oral growth and thereby decrease the productive output of the plant (Chen, 2012).
Changes to springtime temperatures may also inuence
production with excessively warm temperatures during bloom
or early fruit set known to induce abscission (premature fruit
fall) in citrus fruit (Rosenzweig et al., 1996), capsicum, and
chilies (Murison, 1995), and adversely affect pollination of
avocado (Schaffer et al., 2002) and some tomato varieties
(Sato et al., 2000). High spring temperatures can cause reductions to peach yields (Lopez et al., 2007), and modeled
impacts have shown that future yields of almonds,
table grapes, oranges, walnuts, and avocados are likely to be
affected (Lobell et al., 2006; Stckle et al., 2010). Berry collapse
in table grapes (Tilbrook and Tyerman, 2008) has been associated with high temperature conditions during postberry set.
High-temperature impacts can be negative for quality and
yield across many varieties. Reduced sugar content in products
such as pea, strawberry, and melon produced under warmer
nights is often attributed to increased night-time respiration.
However, this effect may also be caused by high temperatures
reducing the period over which fruit develops (Wien, 1997).
An increase in maximum temperatures may negatively impact
yield and quality of leafy crops such as lettuce and spinach
(Titley, 2000). Bolting (premature formation of the seed head/
owers) is an example of a negative impact resulting from
growing these crops in high temperature regimes (Dioguardi,
1995). The timing of elevated temperatures has been shown to
reduce vitamin C levels in fruit production in woody perennials (Richardson et al., 2004).
Production of anthocyanins (pigments responsible for the
red, purple, and blue colors) for apple, pear, purple potato,
pomegranate, legumes, and grapes is often related to commercial quality and the health advantages of foods (for a review, see Tsuda, 2012). The accumulation of anthocyanins is
partly dependent on environmental conditions with cool
minimum temperatures during maturation promoting production whereas high maximum temperatures act to destroy
the compound (Lin-Wang et al., 2011; Marais et al., 2001;
Steyn et al., 2004; Xie et al., 2012). As such, coloration may
be degraded due to both higher minimum temperatures
and higher maximum temperatures. Citrus fruit quality, with
respect to both development of sugars and color, is also inuenced by warmer temperatures, with a decrease in tree storage
time and rind regreening increasing as temperatures rise
(Rosenzweig et al., 1996). The red color of ripening capsicums
develops between 18 1C and 25 1C. But if temperatures rise
above 27 1C during the ripening, a yellowish color results
(Murison, 1995). Yellowing can also occur in tomatoes experiencing high temperatures when ripening (Maltby, 1995).
After harvest, many products including beans, melons,
cherries, and strawberries require cooling so as to remove eld
heat quickly (Alique et al., 2006; Coombs, 1995). With projected temperature rises, the costs and benets of shifting
harvest time to a cooler part of the day, or increasing refrigeration, will need to be assessed. Further, higher growing
temperatures may negatively impact the shelf-life of lettuce
(Rogers, 2007).
Benets to horticultural production from increasing temperatures are also likely. For instance, mangoes grown in the
subtropics can suffer from leaf yellowing when winter temperatures fall below 10 1C, due to photoinhibition of the
photosynthetic apparatus (Sukhvibul et al., 2000). This low
temperature photoinhibition has also been reported for lychee
and rambutan (Diczbalis and Menzel, 1998) and banana
(Damasco et al., 1997). In a warmer climate, cold-induced
photoinhibition will be reduced and greater agronomic potential may exist in some areas currently considered to be
marginal. Further, there may be benets for Solanaceous
vegetable crops (e.g., tomatoes and capsicum), which are
currently seeded in heated glasshouses and transplanted into
the eld when the danger of frost has past (Peet and Wolfe,
2000). These crops may be directly seeded at locations where
frost risk reduces, lowering production costs. Production of
dried fruit, such as Thompson Seedless (sultana) and raisins,
could also benet as solar drying capacity increases as temperatures rise and humidity and rainfall decrease in regions
with Mediterranean climates (Possingham, 2008).
(a)
(c)
273
(b)
(d)
Figure 5 Impact of direct radiation damage to (a) oranges, (b) apples, (c) pears, and (d) wine grapes during the 2009 summer heatwave in
South-east Australia (pome fruit photos courtesy Malcom McCaskill, Vic DPI).
274
October
260
Calendar DOY
240
220
200
180
June
160
1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010
Year
Figure 6 Observed day of year (DOY) relating to the last frost event (daily minimum temperature r0 1C) at Tatura, Australia (unpublished data).
275
276
crops are grown, has a signicant inuence on crop performance (i.e., time to harvest, product quality, and, to a lesser
extent, yield). In a warmer future climate, this practice of
carefully selecting appropriate sites for annual crops will
continue. However, when selecting sites for perennial species it
is imminently more important and urgent to consider the
changing climate. This is because some of these crops (e.g.,
fruit trees and grape vines) have an average life of more than
30 years. Within that time-frame global average warming of at
least 1 1C is anticipated (Rahmstorf et al., 2007), and crops
planted today are expected to remain productive.
By selecting more elevated sites, or avoiding north-westerly
aspects in the Southern Hemisphere and south-westerly aspects in the Northern Hemisphere, horticultural potential can
be extended where regions may otherwise become too warm.
Ultimately, if climate warming increases to a level whereby the
region becomes too hot for the particular crop, pole-ward
shifting of horticultural zones will enable production to continue, with increasing suitability of currently cold-marginal
regions (Olesen and Bindi, 2002). For example, horticulture
production is currently limited by winter temperatures and late
spring frost in northern European regions like Scandinavia and
Siberia (Dehnen-Schmutz et al., 2010) and the UK (Daccache
et al., 2011). Further, an assessment of the productive range of
apples in Finland for the year 2040 found that land
suitable for production will increase northward as will the
range of varieties available for cultivation (Kaukoranta et al.,
2010).
Mapping of threshold temperatures and other relevant aspects of the climate for a range of future climate regimes can
expose risky, or less-risky, areas in which to plant crops. With a
potential reduction of frost-prone areas under climate change,
the area suitable for growing tropical and subtropical crops is
projected to expand, such as for olives (Olesen and Bindi,
2002), citrus, avocados, and bananas in the Mediterranean
region of Europe (Houerou et al. 1992) and for avocados and
pecan nuts in Southern Africa (Schulze and Kunz 1995).
Changing average rainfall conditions may increase or reduce suitability for growing certain crops. Note that where
crops are irrigated the catchment may be remote from the
production area. In these cases information regarding projected rainfall over the catchment region will be essential for
planning purposes (Chiew et al., 2009).
A global-scale increase in extreme rainfall may mean increasing risk of oods or erosion (IPCC, 2012). Impacts are
complex and inuenced by localized factors, but avoiding lowlying sites and considered planting of erosion-prone slopes
may help avoid some of the potential impacts from these
precipitation events. In tropical regions, although the number
of cyclones is projected to reduce in future, the intensity of
these may increase, so selecting sites to avoid cyclone hazard,
for example, away from the coast, may be advisable.
Crop Management
The timing of management activities, such as planting, fertilizing, and irrigation can be adjusted in response to climate
shifts (Krug, 1997). Because climate change is expected to reduce the duration from sowing to harvest for some annual
100
75
50
n = 18
25
n = 72
0
Yes
No
277
Water Management
In many regions of the world, horticultural production occurs
where the water requirement of crops is far higher than that
provided by effective rainfall. In these places irrigation has
been widely adopted to maximize yield and quality, giving
more surety of harvest dates and also facilitating marketing
278
60
50
40
30
20
10
0
600
Evaporative cooling
No evaporative cooling
Air temperature
1200
1800
0000
Integrating Knowledge
Rain, or the threat of rain, may cause growers to pick early to
reduce risk of disease (Jackson and Lombard, 1993). Shortterm forecasting of extreme rainfall events close to harvest will
become crucial given the projected increase in these events.
Farmers can incorporate knowledge of seasonal forecasts, informed by improved information regarding patterns of regional climate drivers (e.g., El Nio-Southern Oscillation;
Meinke and Stone, 2005). However, to benet from seasonal
climate forecasts, the decision capacity of the smallholder
farmers needs to be improved and greater emphasis should be
placed on farmer involvement and a demand-driven participatory approach (Selvaraju et al., 2004).
Consumer Behavior
Availability of most horticultural crops (e.g., strawberries)
tends to vary throughout the year and may be reduced in some
seasons due to production difculties caused by effects of
higher temperatures, droughts, or other climatic events. In
these cases consumers can pay higher prices to growers or pay
more for an imported product (if available). In Australia, banana prices increased dramatically after Severe Tropical Cyclone Larry devastated the crop in 2006 (Clements and
Maesepp, 2011). Color or nutrition levels of produce could be
impacted by climate change, with some of the possible esthetic
impacts identied being regreening of oranges, and yellowing
of tomatoes and capsicums. Ongoing marketing programs are
increasing consumer awareness of new and varied alternative
produce.
279
Conclusion
The effects of climate change on crop quality will vary. The
magnitude and extent of these impacts will be governed by the
present climate of the region, the rate of projected change of
climate and crop type. Management inputs available to
ameliorate any adverse climatic impacts will be determined by
the value of the crop and grower capacity. Because overall
vulnerability will be crop- and site-specic, it is difcult to
determine this for the horticulture industry as a whole, especially at a global scale.
Adapting to a changing climate may occur autonomously. For instance, farm managers currently adjust to
gradually increasing temperatures by modifying timing of
planting on a year-by-year basis. In some instances management may become easier, for example, frost avoidance
mechanisms may not need to be implemented. Glasshouses
may not require as much heating, though cooling requirements may be increased. However, planned adaptation will
also be needed, particularly for high value, long-lasting
permanent perennial crops (e.g., apples) with the associated
infrastructure.
A focus on conventional breeding programs and biotechnology, once some of the potential vulnerabilities of
horticultural crops have been identied, can build resilient
cultivars that are more suited to future climates, for example,
drought-tolerant cultivars. Considering the impacts of rising
CO2 on crops (and the interaction of CO2 with increased
temperature) would assist this endeavor.
Seasonal forecasts can be utilized to address interannual
climate variability to enable effective use of resources (e.g.,
labor and planting material). As knowledge of climate systems
improves, these forecasts should become more accurate and
sophisticated and could include considerations of climate
change trends.
Validation of climate indices that determine locations of
current horticultural enterprises can be modeled relatively
quickly so that predictions of potentially suitable crops for
each region, or potentially suitable sites for particular crops,
can be assessed. Risks associated with climate extremes can be
assessed at the same time as suitable macroclimates and
mesoclimates are being evaluated. Substantial benets can be
achieved if damaging temperature threshold events can be
avoided in future.
Similarly, calculating the risks associated with changes to
water availability may alleviate any adverse impacts with regard to allocating water to various agricultural sectors in the
future, or in avoiding ood-prone areas. It will be possible to
assess the water requirements for horticultural crops more
accurately if the effect of rising CO2 on crop water use is better
understood. It will remain necessary to continue improvements in irrigation technology.
After identifying relevant, crop-specic, climatic thresholds,
it will be possible to estimate whether climate change will
increase or decrease the risks of growing crops in particular
geographic locations. Some new regions may be identied as
becoming more suitable for horticultural production, whereas
others may become less suitable. An increase in production
from subtropical and tropical regions could see new products
being introduced, or a changed accessibility of produce. This
280
References
Ainsworth, E.A., Long, S.P., 2005. What have we learned from 15 years of free-air
CO2 enrichment (FACE)? A meta-analytic review of the responses of
photosynthesis, canopy properties and plant production to rising CO2. New
Phytologist 165, 351371.
Aldous, D.E., Holborn, S., 2012. Lifestyle horticulture in Australia: Commodities,
enterprise numbers, employment and economic analysis. Acta Horticulturae 930,
3541.
Al-Jamal, M.S., Ball, S., Sammis, T.W., 2001. Comparison of sprinkler, trickle and
furrow irrigation efciencies for onion production. Agricultural Water Management
46, 253266.
Alexander, L.V., Zhang, X., Peterson, T.C., et al., 2006. Global observed changes in
daily climate extremes of temperature and precipitation. Journal of Geophysical
Research 111, 122.
Alique, R., Martnez, M.A., Alonso, J., 2006. Metabolic response to two
hydrocooling temperatures in sweet cherries cv Lapins and cv Sunburst. Journal
of the Science of Food and Agriculture 86, 18471854.
Aurambout, J., Finlay, K., Constable, F., Rowles-van Rijswijk, B., Luck, J., 2006. A
review of the impacts of climate change on plant biosecurity. Report to the CRC
for National Plant Biosecurity. VIC, Australia: Victorian Government Department
of Primary Industries Landscape Systems Science, pp. 42.
Australian Bureau of Meteorology, 2006. Severe Tropical Cyclone Larry. Queensland
Regional Ofce, Australian Bureau of Meteorology.
Bonarriva, J., 2003. Industry and Trade Summary: Cut Flowers. Washington, DC:
U.S. International Trade Commission.
Botzen, W.J.W., Bouwer, L.M., van den Bergh, J.C.J.M., 2010. Climate change and
hailstorm damage: Empirical evidence and implications for agriculture and
insurance. Resource and Energy Economics 32, 341362.
Bronick, C.J., Lal, R., 2005. Soil structure and management: A review. Geoderma
124, 322.
Cai, W., Cowan, T., Briggs, P.R., Raupach, M.R., 2009. Rising temperatures depletes
soil moisture and exacerbates severe drought conditions across southeast
Australia. Geophysical Research Letters 36, L21709.
Chakroborty, S., 2004. Potential impact of climate change on plant pathogen
interactions. Australasian Plant Pathology 34, 443448.
Chen, Q., 2012. Adaptation and mitigation of impact of climate change on tropical
fruit industry in China. Acta Horticulturae 928, 101104.
Chiew, F.H.S., Teng, J., Vaze, J., et al., 2009. Estimating climate change impact on
runoff across southeast Australia: Method, results, and implications of the
modeling method. Water Resources Research 45, W10414.
Clark, L.J., 2004. Impact of drip irrigation on the properties of red brown earths
following changing management practices in vineyards. PhD Thesis, Soil and
Land Systems School of Earth and Environmental Sciences, University of
Adelaide, Waite Campus.
Clements, K.W., Maesepp, M., 2011. A self-reective inverse demand system.
Applied Economics Letters 18 (18), 17391743.
Coakley, S.M., Scherm, H., Chakraborty, S., 1999. Climate change and plant disease
management. Annual Review of Phytopathology 37, 399426.
Coombs, B., 1995. Horticulture Australia. Australia: Morescope Publishing.
CSIRO and Australian Bureau of Meteorology, 2007. Climate change in Australia.
Technical Report CSIRO and Bureau of Meteorology through the Australian
Climate Change Science Program. Melbourne, Australia: CSIRO. Available at:
http://www.climatechangeinaustralia.gov.au/technical_report.php (accessed
13.01.14).
Daccache, A., Weatherhead, E.K., Stalham, M.A., Knox, J.W., 2011. Impacts of
climate change on irrigated potato production in a humid climate. Agricultural
and Forest Meteorology 151, 16411653.
Damasco, O.P., Smith, M.K., Godwin, I.D., et al., 1997. Micropropagated dwarf offtype Cavendish bananas (Musa spp., AAA) show improved tolerance to
suboptimal temperatures. Australian Journal of Agricultural Research 48,
377384.
Darbyshire, R., 2013. Winter and spring phenology of Australian pome fruit in
historical and future climates. PhD Thesis, University of Melbourne.
Darbyshire, R., Webb, L., Goodwin, I., Barlow, S., 2013a. Impact of future warming
on winter chilling in Australia. International Journal of Biometeorology 57,
355366.
Darbyshire, R., Webb, L., Goodwin, I., Barlow, S., 2013b. Evaluation of recent trends
in Australian pome fruit spring phenology. International Journal of
Biometeorology 57, 409421.
Darbyshire, R., Webb, L., Goodwin, I., Barlow, S., 2013c. Challenges in predicting
climate change impacts on pome fruit phenology. International Journal of
Biometeorology. doi: 10.1007/s00484-013-0705-4.
Daymond, A.J., Wheeler, T.R., Hadley, P., Ellis, R.H., Morison, J.I.L., 1997. The
growth, development and yield of onion (Allium cepa L.) in response to
temperature and CO2. Journal of Horticultural Science 72, 135145.
Dehnen-Schmutz, K., Holdenrieder, O., Jeger, M.J., Pautasso, M., 2010. Structural
change in the international horticultural industry: Some implications for plant
health. Scientia Horticulturae 125, 115.
Deuter, P.L., 1989. The development of an insecticide resistance strategy for the
Lockyer Valley, Queensland. Acta Horticulturae 247, 267272.
Diczbalis, Y., Menzel, C.M., 1998. Low temperatures decrease CO2 assimilation and
growth in the tropical rambutan. Journal of Horticultural Science and
Biotechnology 73, 6571.
Ding, Y., Hayes, M.J., Widhalm, M., 2011. Measuring economic impacts of drought:
A review and discussion. Disaster Prevention and Management 20, 434446.
Dioguardi, D., 1995. Lettuces. In: Coombes, B. (Ed.), Horticulture Australia. VIC,
Australia: Morescope Publishing, pp. 221226.
Doi, H., Gordo, O., Katano, I., 2008. Heterogeneous intra-annual climatic changes
drive different phenological responses at two trophic levels. Climate Research 36,
181190.
Drake, B.G., Gonzalez-Meler, M.A., Long, S.P., 1997. More efcient plants: A
consequence of rising atmospheric CO2. Annual Review of Plant Physiology and
Molecular Biology 48, 609639.
Easterling, W.E., Aggarwal, P.K., Batima, P., et al., 2007. Climate change 2007:
Impacts, adaptation and vulnerability. Food, bre and forest products. In: Parry,
M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J., Hanson, C.E. (Eds.),
Contribution of Working Group II to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge
University Press, pp. 273313.
Eccel, E., Rea, R., Caffarra, A., Crisci, A., 2009. Risk of spring frost to apple
production under future climate scenarios: The role of phenological acclimation.
International Journal of Biometeorology 53, 273286.
Erez, A., Couvillon, G.A., 1983. Evaporative cooling to improve rest breaking of
nectarine buds by counteracting high daytime temperatures. HortScience 18 (4),
480481.
Evans, N., Baierl, A., Semenov, M.A., Gladders, P., Fitt, B.D.L., 2008. Range and
severity of a plant disease increased by global warming. Journal of the Royal
Society Interface 5, 525531.
Falloon, P., Betts, R., 2010. Climate impacts on European agriculture and water
management in the context of adaptation and mitigation The importance of an
integrated approach. Science of the Total Environment 408, 56675687.
FAOSTAT, 2012. Food and Agriculture Organization of the United Nations website.
Available at: http://faostat.fao.org/default.aspx (accessed 14.01.14).
Fereres, E., Goldhamer, D.A., Parsons, L.R., 2003. Irrigation water management of
horticultural crops. HortScience 38, 10361042.
Finetto, G.A., 2004. The behaviour of some apple rootstocks in relation to the
chilling requirement. Acta Horticulturae 662, 245251.
Flore, J., 1994. Stone fruit. In: Schaffer, B., Andersen, P. (Eds.), Handbook of
Environmental Physiology of Fruit Crops: Volume 1 Temperature Crops. New
York: CRC Press, pp. 233270.
Fuhrer, J., 2003. Agroecosystem responses to combinations of elevated CO2, ozone,
and global climate change. Agriculture, Ecosystems & Environment 97, 120.
Gao, S., Huang, Z., 2004. Thermal index in lychee bud differentiation period and its
impact on yield. Meteorological Monthly 30, 1721.
George, A.P., Nissen, R.J., 1990. Effects of hydrogen cyanamide on yield, growth
and dormancy release of table grapes in subtropical Australia. Acta Horticulturae
279, 427436.
281
Leahy, P., 2006. Dealing with Larry's destruction. Australian Bananas 22, 3.
Available at: http://www.milburnmedia.com/BananaMagazineJune2006.pdf
(accessed 13.01.14).
Legave, J., Farrera, I., Almeras, T., Calleja, M., 2008. Selecting models of apple
owering time and understanding how global warming has had an impact on this
trait. Journal of Horticultural Science and Biotechnology 83, 7684.
Lin-Wang, K., Micheletti, D., Palmer, J., et al., 2011. High temperature reduces
apple fruit colour via modulation of the anthocyanin regulatory complex. Plant,
Cell and Environment 34, 11761190.
Liu, H.F., Wu, B.H., Fan, P.G., Li, S.H., Li, L.S., 2006. Sugar and acid
concentrations in 98 grape cultivars analyzed by principal component analysis.
Journal of the Science of Food and Agriculture 86, 15261536.
Lobell, D.B., Field, C.B., Cahill, K.N., Bonls, C., 2006. Impacts of future climate
change on California perennial crop yields: Model projections with climate and
crop uncertainties. Agricultural And Forest Meteorology 141, 208218.
Lopez, G., Johnson, R.S., DeJong, T.M., 2007. High spring temperatures decrease
peach fruit size. California Agriculture 61, 3134.
Lucas, C., Hennessy, K.J., Mills, G.A., Bathols, J., 2007. Bushre weather in
Southeast Australia recent trends and projected climate change impacts.
Consultancy Report Prepared for the Climate Institute of Australia. Melbourne:
Bushre Cooperative Research Centre, Australian Bureau of Meteorology and
CSIRO Marine and Atmospheric Research.
Luedeling, E., Girvetz, E.H., Semenov, M.A., Brown, P.H., 2011. Climate change
affects winter chill for temperate fruit and nut trees. Plos One. doi:10.1371/
journal.pone.0020155.
Magarey, P.A., Wachtel, M.F., Nicholas, P.R., 1994. Disorders and injuries. In:
Nicholas, P., Magarey, P., Wachtel, M. (Eds.), Diseases and Pests. Grape
Production Series. Number 1. Adelaide: Winetitles, pp. 7580.
Maggs, D.H., 1975. Inuence of a prolonged owering period on the uniformity of
an apple crop. Australian Journal of Experimental Agriculture and Animal
Husbandry 15, 709714.
Maltby, J.E., 1995. Tomatoes. In: Coombes, B. (Ed.), Horticulture Australia. VIC,
Australia: Morescope Publishing, pp. 289296.
Manrique, L.A., Bartholomew, D.P., 1991. Growth and yield performance of potato
grown at three elevations in Hawaii: II Dry matter production and efciency in
partitioning. Crop Science 31, 367372.
Marais, E., Jacobs, G., Holcroft, D.M., 2001. Colour response of 'Cripps' Pink'
apples to postharvest irradiation is inuenced by maturity and temperature.
Scientia Horticulturae 90, 3141.
Marais, J., 2001. Effect of grape temperature and yeast strain on Sauvignon blanc
wine aroma composition and quality. South African Journal for Enology and
Viticulture 22, 4751.
Mathooko, F.M., Mutui, T.M., 2011. Challenges and opportunities in poostharvest
horticulture research and training in developing countries: The case of Kenya.
Acta Horticulturae 920, 2331.
McIntyre, G.N., Lider, L.A., Ferrari, N.L., 1982. The chronological classication
of grapevine phenology. American Journal for Enology and Viticulture 33,
8085.
Measham, P.F., Bound, S.A., Gracie, A.J., Wilson, S.J., 2009. Incidence and type of
cracking in sweet cherry (Prunus avium L.) are affected by genotype and season.
Crop and Pasture Science 60, 10021008.
Meinke, H., Stone, R., 2005. Seasonal and inter-annual climate forecasting:
The new tool for increasing preparedness to climate variability and change in
agricultural planning and operations. In: Salinger, J., Sivakumar, M.V.K., Motha,
R. (Eds.), Increasing Climate Variability and Change. Netherlands: Springer,
pp. 221253.
Meza, F.J., Silva, D., Vigil, H., 2008. Climate change impacts on irrigated maize in
Mediterranean climates: Evaluation of double cropping as an emerging adaptation
alternative. Agricultural Systems 98, 2130.
Middleton, S., McWaters, A., 2002. Hail netting of apple orchards Australian
experience. Compact Fruit Tree 35, 5155.
Miglietta, F., Bindi, M., Vaccari, F.P., et al., 2000. Crop ecosystem responses to
climatic change: Root and tuberous crops. In: Reddy, H.F., Hodges, K.R. (Eds.),
Climate Change And Global Crop productivity. USA: CABI Publishing,
Mississippi State University, pp. 189212.
Morgan, J.A., Pataki, D.E., Korner, C., et al., 2004. Water relations in grassland
and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140,
1125.
Moriondo, M., Good, P., Durao, R., et al., 2006. Potential impact of climate change
on re risk in the Mediterranean area. Climate Research 31, 8595.
Morison, J.L., Lawlor, D.W., 1999. Interactions between increasing CO2
concentration and temperature on plant growth. Plant, Cell and Environment 22,
659682.
282
Murison, J., 1995. Capsicums and chillies. In: Coombes, B. (Ed.), Horticulture
Australia. VIC, Australia: Morescope Publishing.
Nakice novic, N., Swart, R., 2000. Special Report on Emissions Scenarios: A Special
Report of Working Group III of the Intergovernmental Panel on Climate Change.
Cambridge: Cambridge University Press. pp. 599.
Nir, G., Klien, I., Lavee, S., Spieler, G., Barak, U., 1988. Improving grapevine
budbreak and yields by evaporative cooling. Journal of the American Society for
Horticultural Science 113, 512517.
Ogurtsov, V.A., Van Asseldonk, M.P.A.M., Huirne, R.B.M., 2008. Assessing and
modelling catastrophic risk perceptions and attitudes in agriculture: A review.
NJAS Wageningen Journal of Life Sciences 56, 3958.
Olesen, J.E., Grevsen, K., 1993. Simulated effects of climate change on
summer cauliower production in Europe. European Journal of Agronomy 2,
313323.
Olesen, J.E., Bindi, M., 2002. Consequences of climate change for European
agricultural productivity, land use and policy. European Journal of Agronomy 16,
239262.
Olesen, J.E., Friis, E., Grevsen, K., 1993. Simulated effects of climate change on
vegetable crop production in Europe. In: Kenny, G.J., Harrison, P.A., Parry, M.L.
(Eds.), The Effect of Climate Change on Agricultural and Horticultural Potential
in Europe, Environmental Change Unit. Oxford: University of Oxford,
pp. 177200.
Oukabli, A., Bartolin, S., Viti, R., 2003. Anatomical and morphological study of
apple (Malus X domestica Borkh.) ower buds growing under inadequate winter
chilling. Journal of Horticultural Science & Biotechnology 78, 580585.
Parchomchuk, P., Meheriuk, M., 1996. Orchard cooling with pulsed overtree
irrigation to prevent solar injury and improve fruit quality of Jonagold apples.
HortScience 31 (5), 802804.
Pardini, A., Faiello, C., Longhi, F., Mancuso, S., Snowball, R., 2002. Cover crop
species and their management in vineyards and olive groves: Review paper.
Advances in Horticultural Science 16, 225234.
Pearson, S., Wheeler, T.R., Hadley, P., Wheldon, A.E., 1997. A validated
model to predict the effects of environment on the growth of lettuce (Lactuca
sativa L.): Implications for climate change. Journal of Horticultural Science 72,
503517.
Peet, M.M., Wolfe, D.W., 2000. Crop ecosystem responses to climate change:
Vegetable crops. In: Reddy, K.R., Hodges, H.F. (Eds.), Climate Change and
Global Crop Productivity. USA: CABI Publishing, Mississippi State University,
pp. 213243.
Petri, J.L., Leite, G.B., 2004. Consequences of insufcient winter chilling on apple
tree bud-break. Acta Horticulturae 662, 5360.
Petrie, P.R., Sadras, V.O., 2008. Advancement of grapevine maturity in Australia
between 1993 and 2006: Putative causes, magnitude of trends and viticultural
consequences. Australian Journal of Grape and Wine Research 14, 3345.
Possingham, J.V., 2008. Developments in the production of table grapes, wine, and
raisins in tropical regions of the world. Acta Horticulturae 785, 4550.
Potter N.J., Chiew F.H.S., Frost A.J., et al., 2008. Characterisation of recent rainfall
and runoff in the MurrayDarling Basin. A Report to the Australian Government
from the CSIRO MurrayDarling Basin Sustainable Yields Project. Water for a
Healthy Country Flagship, pp. 48. Canberra, Australia: CSIRO.
Rahmstorf, S., Cazenave, A., Church, J.A., et al., 2007. Recent climate observations
compared to projections. Science 316, 709.
Richardson, A.C., Marsh, K.B., Boldingh, H.L., et al., 2004. High growing
temperatures reduce fruit carbohydrate and Vitamin C in fruit. Plant, Cell and
Environment 27, 423435.
Rigby, J.R., Porporato, A., 2008. Spring frost risk in a changing climate.
Geophysical Research Letters 35, L12703. doi:10.1029/2008GL033955.
Rogers, G.S., 2007. Post harvest improvement in iceberg and cos lettuce to extend
shelf life for fresh cut salads. Sydney: Horticulture Australia, 134 pp.
Rosenberg, N.J., Kimball, B.A., Martin, P., Cooper, C.F., 1990. From climate and
CO2 enrichment to evapotranspiration. In: Waggoner, P.E. (Ed.), Climate Change
and U.S. Water Resources. New York, NY: Wiley, pp. 151175.
Rosenzweig, C., Phillips, J., Goldberg, R., Carroll, J., Hodges, T., 1996. Potential
impacts of climate change on citrus and potato production in the US.
Agricultural Systems 52, 455479.
Rosenzweig, C., Iglesias, A., Yang, X.B., Epstein, P., Chivian, E., 2001. Climate
change and extreme weather events; implications for food production, plant
diseases, and pests. Global Change and Human Health 2, 90104.
Rosenzweig, C., Karoly, D., Vicarelli, M., et al., 2008. Attributing physical and
biological impacts to anthropogenic climate change. Nature 453, 353358.
Sadras, V.O., Moran, M.A., 2012. Elevated temperature decouples anthocyanins and
sugars in berries of Shiraz and Cabernet Franc. Australian Journal of Grape and
Wine Research 18, 115122.
Salami, H., Shahnooshi, N., Thomson, K.J., 2009. The economic impacts of
drought on the economy of Iran: An integration of linear programming and
macroeconometric modelling approaches. Ecological Economics 68, 10321039.
Salinari, F., Giosu, S., Tubiello, F.N., et al., 2006. Downy mildew (Plasmopara
viticola) epidemics on grapevine under climate change. Global Change Biology
12, 12991307.
Salvestrin, J., 1995. Onions. In: Coombes, B. (Ed.), Horticulture Australia. Victoria,
Australia: Morescope Publishing, pp. 240246.
Sato, S., Peet, M.M., Thomas, J.F., 2000. Physiological factors limit fruit set of
tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant,
Cell and Environment 23, 719726.
Saure, M.C., 1985. Dormancy release in deciduous fruit trees. Horticultural Reviews
7, 239300.
Schaffer, B., Andersen, P., 1994. Handbook of Environmental Physiology of Fruit
Crops. Vol. 1: Temperate Crops. New York: CRC Press, 368 pp.
Schaffer, B., Whiley, A.W., Wolstenholme, B.N., 2002. Avocado: Botany, Production
and Uses. Wallingford, Oxon: CAB Publishing, CAB International.
Schaffer, B., Searle, C., Whiley, A.W., Nissen, R.J., 1996. Effects of atmosphertic
CO2 enrichment and root restriction on leaf gas exchange and growth of banana
(Musa). Physiologia Plantarum 97, 685693.
Schep, L., Temple, W., Beasley, M., 2009. The adverse effects of hydrogen
cyanamide on human health: An evaluation of inquiries to the New Zealand
National Poisons Centre. Clinical Toxicology 47, 5860.
Schultz, H.R., 2000. Climate change and viticulture: A European perspective on
climatology, carbon dioxide and UV-B effects. Australian Journal of Grape and
Wine Research 6, 212.
Schulze, R.E., Kunz, R.P., 1995. Potential shifts in optimal growth areas of selected
commercial tree species and subtropical crops in southern Africa due to global
warming. Journal of Biogeography 22, 679688.
Seguin, B., de Cortazar, I.G., 2005. Climate warming: Consequences for viticulture
and the notion of 'terroirs' in Europe. Acta Horticulturae 689, 6171.
Selvaraju, R., Meinke, H., Hansen, J., 2004. Approaches allowing smallholder
farmers in India to benet from seasonal climate forecasting. In: Fischer, T.,
et al. (Ed.), New Directions for a Diverse Planet: Proceedings of the 4th
International Crop Science Congress, Brisbane, Australia (Crop Science),
pp. 112. Available at: http://www.cropscience.org.au/icsc2004/symposia/2/7/
146_selvarajur.htm (accessed 14.01.14).
Snyder, R.L., Moratiel, R., Zhenwei, S., et al., 2011. Evaporation response to climate
change. Acta Horticulturae 922, 9198.
Sport and Recreation Victoria, 2007. Sport and recreation victoria country football
grounds assistance program stage 2. Outcomes Report Sport and Recreation
Victoria Department for Victorian Communities, Melbourne, Victoria, pp. 26.
Melbourne, VIC: Community Sport and Recreation.
Steyn, W.J., Holcroft, D.M., Wand, S.J.E., Jacobs, G., 2004. Anthocyanin
degradation in detached pome fruit with reference to preharvest red color loss
and pigmentation patterns of blushed and fully red pears. Journal of the
American Society for Horticultural Science 129, 1319.
Stckle, C.O., Nelson, R.L., Higgins, S., et al., 2010. Assessment of climate change
impact on Eastern Washington agriculture. Climate Change 102.7702.
Storck, H., 1978. Towards an economics of energy in horticulture. Acta Horticulturae
76, 1530.
Sukhvibul, N., Whiley, A.W., Smith, M.K., Hetherington, S.E., 2000. Susceptibility of
mango (Mangifera indica L.) to cold induced photoinhibition and recovery at
different temperatures. Australian Journal of Agricultural Research 51, 503513.
Sutherst, R.W., Collyer, B.S., Yonow, T., 2000. The vulnerability of Australian
horticulture to the Queensland fruit y, Bactrocera (Dacus) tryoni, under climate
change. Australian Journal of Agricultural Research 51, 467480.
Thomaia, T., Sfakiotakis, E., Diamantidis, G., Vasilakakisa, M., 1998. Effects of low
preharvest temperature on scald susceptibility and biochemical changes in
Granny Smith' apple peel. Scientia Horticulturae 76, 115.
Thomas, A.L., Muller, M.E., Dodson, B.R., Ellersieck, M.R., Kap, M., 2004. A
kaolin-based particle lm suppresses certain insect and fungal pests while
reducing heat stress in apples. Journal of American Pomological Society 58,
4251.
Thomas, M.R., Van Heeswijck, R., 2004. Classication of grapevines and their
interrelationships. In: Dry, P.R., Coombe, B.G. (Eds.), Viticulture Volume 1
Resources, second ed. Adelaide, South Australia: Winetitles, pp. 119131.
Thompson, T., Grauke, L., 2003. Pecan tree growth and precocity. Journal of the
American Society for Horticultural Science 128, 6366.
Thorne, E.T., Stevenson, J.F., Rost, T.L., Labavitch, J.M., Matthews, M.A., 2006.
Pierce's disease symptoms: Comparison with symptoms of water decit
and the impact of water decits. American Journal of Enology and Viticulture 57,
111.
Tilbrook, J., Tyerman, S.D., 2008. Cell death in grape berries: Varietal differences
linked to xylem pressure and berry weight loss. Functional Plant Biology 35,
173184.
Tindall, J.A., Beverly, R.B., Radcliffe, D.E., 1991. Mulch effect on soil properties and
tomato growth using micro-irrigation. Agronomy Journal 83, 10281034.
Titley M., 2000. Australian lettuce production and processing An overview.
Australian Lettuce Industry Conference, Hay, New South Wales, pp. 1231.
Orange, Australia: NSW Agriculture.
Topp, B., Wilk, P., Bignell, G., Russell, D., 2008. Summary of the DPI&F
subtropical peach breeding from 20022007. Low Chill Stonefruit Grower 1,
45.
Topp, B.L., Sherman, W.B., 2000. Breeding strategies for developing temperate fruits
for the sub-tropics, with particular reference to Prunus. Acta Horticulturae 522,
235240.
Tsuda, T., 2012. Anthocyanins as functional food factors Chemistry, nutrition and
health promotion. Food Science and Technology Research 18, 315324.
Van Dijk, A., Evans, R., Hairsine, P., et al., 2006. Risks to the Shared Water
Resources of the MurrayDarling Basin. Canberra: MurrayDarling Basin
Commission, 46 pp. Available at: http://www.mdbc.gov.au/__data/page/1131/
CSIRO_Part_2_risks_to_shared_water_resources.pdf (accessed 14.01.14).
Vano, J.A., Scott, M.J., Voisin, N., et al., 2010. Climate change impacts on water
management and irrigated agriculture in the Yakima River Basin, Washington,
USA. Climatic Change 102, 287317.
Velasco, R., Zharkikh, A., Troggio, M., et al., 2007. A high quality draft consensus
sequence of the genome of a heterozygous grapevine variety. Plos One 2, e1326.
Voller, C.F.P., 1986. Predicting rest-breaking: Principles and problems. Deciduous
Fruit Grower 36, 302308.
Watterson, I.G., Whetton, P.H., 2011. Distributions of decadal means of temperature
and precipitation change under global warming. Journal of Geophysical Research
116, D07101.
Webb, L., 2006. The impact of greenhouse gas-induced climate change on the
Australian wine industry. PhD Thesis, School of Agriculture and Food Systems,
University of Melbourne, Parkville, Victoria. pp. 277.
Webb, L., 2011. Projected climate: Means and extremes. How will this impact the
wine industry? 7th University House Wine Symposium. Canberra, Australia:
Australian National University.
Webb, L., Snyder, R.L., 2013. Frost hazard. In: Bobrowsky, P. (Ed.), Encyclopaedia
of Natural Hazards. Dordrecht, Heidelberg, New York, London: Springer,
pp. 363366.
Webb, L., Whetton, P., Barlow, E.W.R., 2007a. Shifting Viticulture Suitability.
Australian and New Zealand Grapegrower and Winemaker.
Webb, L., Whiting, J., Watt, A., et al., 2010. Managing grapevines through severe
heat: A survey of growers after the 2009 summer heatwave in south-eastern
Australia. Journal of Wine Research 21, 147165.
283
Webb, L.B., Watterson, I.G., Bhend, J., Whetton, P.H., 2013. Global climate
analogues for winegrowing regions in future periods: Projections of temperature
and precipitation. Australian Journal of Grape and Wine Research 19, 331341.
Webb, L.B., Whetton, P.H., Barlow, E.W.R., 2007b. Modelled impact of future
climate change on the phenology of winegrapes in Australia. Australian Journal
of Grape and Wine Research 13, 165175.
Webb, L.B., Whetton, P.H., Barlow, E.W.R., 2011. Observed trends in winegrape
maturity in Australia. Global Change Biology 17, 27072719.
Webb, L.B., Whetton, P.H., Bhend, J., et al., 2012. Earlier wine-grape ripening
driven by climatic warming and drying and management practices. Nature
Climate Change 2, 259264.
Whiting, J., Krstic, M., 2007. Understanding the sensitivity to timing and
management options to mitigate the negative impacts of bush re smoke on
grape and wine quality, Scoping study. Knoxeld, VIC, Australia: Department of
Primary Industries, Primary Industries Research.
Wien, H.C., 1997. The Physiology of Vegetable Crops. Oxon, UK: CAB International,
Wallingford.
Wilk, P., 2005. Low Chill Stone Fruit Varieties 2005. NSW, Australia: NSW
Department of Primary Industries, pp. 12. Available at: http://www.dpi.nsw.gov.
au/__data/assets/pdf_le/0020/138125/Low-chill-stone-fruit-varieties-2005.pdf
(accessed 14.01.14).
Woldendorp, G., Hill, M.J., Doran, R., Ball, M.C., 2008. Frost in a future climate:
Modelling interactive effects of warmer temperatures and rising atmospheric
[CO2] on the incidence and severity of frost damage in a temperate evergreen
(Eucalyptus pauciora). Global Change Biology 14, 294308.
Wurr, D.C.E., Edmonsen, R.N., Fellows, J.R., 2000. Climate change: A response
surface study of the effects of CO2 and temperature on the growth of French
beans. Journal of Agricultural Science 135, 379387.
Wurr, D.C.E., Hand, D.W., Edmondson, R.N., et al., 1998. Climate change: A
response surface study of the effects of CO2 and temperature on the growth
of beetroot, carrots and onions. Journal of Agricultural Science 131,
125133.
Xie, X.B., Li, S., Zhang, R.F., et al., 2012. The bHLH transcription factor MdbHLH3
promotes anthocyanin accumulation and fruit colouration in response to low
temperature in apples. Plant, Cell and Environment 35, 18841897.
Xue, L., Revell, B.J., 2009. Which way forward for China's vegetable exports? British
Food Journal 111, 2643.
Zegbe-Domngueza, J.A., Behboudian, M.H., Lang, A., Clothier, B.E., 2003. Decit
irrigation and partial rootzone drying maintain fruit dry mass and enhance fruit
quality in Petopride processing tomato (Lycopersicon esculentum, Mill.).
Scientia Horticulturae 98, 505510.
Zso, Z., Varadi, G., Balo, B., et al., 2009. Heat acclimation of grapevine leaf
photosynthesis: Mezo- and macroclimatic aspects. Functional Plant Biology 36,
310322.
Glossary
Anthropogenic Caused or inuenced by humans.
Aquifers An underground layer of permeable rock,
sediment (usually sand or gravel), or soil that yields water.
Forward genetics Comprise of genetics techniques that
aims to identify genes/mutations that produce a certain
phenotype.
Genebanks Type of biorepository which preserves the
genetic material. In plants, this could be by freezing cuts
from the plant or stocking the seeds.
Genetic engineering Direct manipulation of the genes in
an organism, with the intent of making that organism
better, using biotechnology.
Glaciers A huge mass of ice slowly owing over a land
mass, formed from compacted snow in an area where snow
accumulation exceeds melting and sublimation.
Climate Change
Climate changes are occurring and the discussions on their
impact are rising. Climate changes are already providing signicant challenges to natural systems. The discussion on the
consequences of climate changes concerns different knowledge areas. Most of the observed increases in global average
temperatures since the mid-twentieth century are very likely
due to the observed increase in anthropogenic greenhouse gas
(GHG) concentrations. The Fourth Assessment Report of the
Intergovernmental Panel on Climate Change (IPCC, 2007)
indicates that the warming of the climate system is unequivocal, as it is now evident from observations of increases
in global average air and ocean temperatures, widespread
melting of snow and ice, and rising global average sea level.
Signicant changes in physical and biological systems have
already occurred on all continents and in most oceans, and
most of these changes are in the direction expected with
warming temperature (Rosenzweig et al., 2008). Global climate change is predicted to lead to extreme temperatures and
severe drought in some parts of the world, whereas other parts
will suffer from heavy storms and periodic ooding (Marshall
et al., 2012).
Estimates of changes in the global temperature are still
uncertain. For the future, best estimates of temperature increases are in the range of 1.84 1C in 209099 relative to
198099, depending on the scenario of future GHG emissions
that is used to drive the climate models (IPCC, 2007).
Nevertheless, however low they may be, the consequences will
be felt by all humanity to a greater or lesser degree. The most
relevant fact is that most of the effects of these changes will
affect developing countries (Lobell et al., 2008).
There is a broad scientic agreement that the climate conditions are being changed on a global scale by human
284
doi:10.1016/B978-0-444-52512-3.00005-X
The main climate changes that are occurring affect the level
of the oceans, precipitation, and temperature. The global sea
level has increased by approximately 1222 cm during the
twentieth century, but satellite records conrm that the rate of
sea level rise has now almost doubled to approximately
3.4 mm year1 (IPCC, 2007; Allison et al., 2009). Precipitation
is highly variable and trends are more difcult to isolate, but
the overall precipitation and heavy precipitation events have
increased in most regions; at the same time the occurrence of
drought has also been on the rise, particularly since 1970
(IPCC, 2007; Allison et al., 2009). Winter temperatures have
increased more rapidly than summer temperatures, and
nighttime minimum temperatures have warmed faster than
the daytime maxima (IPCC, 2007; Meehl et al., 2007).
All climate changes will have additional impacts via
changes in the ecosystem, losses in agriculture, and of genetic
diversity and changes to biotic and abiotic interactions with
other species and ecosystem processes. These impacts are potentially very signicant in determining the effects of climate
change.
285
286
The man-induced world climate change will increase the frequency of precipitations of higher magnitude as well as tropical cyclone activity (IPCC, 2007). As a result, the occurrence
of ooding events on ood plains (i.e., lowlands) and cultivated lands is expected to be higher (Arnell and Liu, 2001).
Under ooding conditions, the water table rises above soil
level and envelopes some aerial portions of the plant. Soil
water excess determines a severe decrease in the oxygen
diffusion rate into the soil (Ponnamperuma, 1972, 1984;
Armstrong 1979). Shortly after the soil is ooded, the respiration of roots and microorganisms depletes the remnant
oxygen and the environment becomes hypoxic (i.e., oxygen
levels limit mitochondrial respiration) and later anoxic (i.e.,
respiration is completely inhibited) (Blom et al., 1994; Bailey
Serres and Voesenek, 2008; Wegner, 2010).
When ooding results in complete submergence, and in
normally submersed aquatic plants, availability of carbon dioxide, light, and oxygen to the shoots typically diminishes
(Jackson and Ram, 2003). Plant roots suffer hypoxia or anoxia.
The rst constraint for plant growth under ooding is the
immediate lack of oxygen necessary to sustain aerobic respiration of submerged tissues (Armstrong, 1979; Vartapetian and
Jackson, 1997; Voesenek et al., 2004).
Under conditions of water excess, the soil type and its
features will be crucial in determining how deep the stress will
inuence plant development. With the reduction of the soil
redox potential a range of potentially toxic compounds appear, such as suldes, soluble Fe and Mn, ethanol, lactic acid,
acetaldehyde, and acetic and formic acid, and may injure plant
tissues by impairing proper cell metabolism (Kozlowski, 1997;
Fiedler et al., 2007). Therefore, lack of oxygen and later the
accumulation of such compounds are the major constraints
that plants suffer under ooding conditions. A major constraint resulting from water excess, at least for poorly adapted
species, is an inadequate supply of oxygen to submerged tissues; diffusion of oxygen through water is 104-fold slower
than in air (Armstrong and Drew, 2002). In addition to the
oxygen deciency, excess water also leads to other changes in
the soil that inuence levels the hormones ethylene in the
plants (Smith and Russell, 1969; Jackson, 1982).
287
expansion growth and also affects the yield, but the tolerance of
any species to this menace varies remarkably (Anjum et al.,
2003; Bhatt and Srinivasa, 2005; Kusaka et al., 2005; Shao et al.,
2008). A ramied root system has been implicated in the
drought tolerance and high biomass production primarily due
to its ability to extract more water from soil and its transport to
the above-ground parts for photosynthesis. In addition to other
factors, changes in photosynthetic pigments are of paramount
importance to drought tolerance (Jaleel et al., 2009).
Other very important effects from climate change are the
excess rainfall that will increase the frequency of precipitation of
higher magnitude as well as tropical cyclone activity that cause
stress for ooding. Those natural disturbances affect crop and
forage production worldwide (BaileySerres and Voesenek, 2008;
Colmer and Voesenek, 2009). Plants develop a suite of anatomical, morphological, and physiological responses in order to
deal with partial submergence imposed by ooding (Armstrong,
1979; Kozlowski and Pallardy, 1984; Vartapetian and Jackson,
1997; Striker et al., 2005; Colmer and Voesenek, 2009).
The most common anatomical response is the generation
of aerenchyma in tissues, which facilitates the transport of
oxygen from shoots to roots (Justin and Armstrong, 1987;
Seago et al., 2005; Colmer, 2003). At the morphological level,
usual responses to ooding include adventitious rooting and
increases in plant height and consequently, in the proportion
of biomass above water level (Naidoo and Mundree, 1993;
Grimoldi et al., 1999). This also helps to facilitate the oxygenation of submerged tissues through the aerenchyma tissue
(Laan et al., 1990; Colmer, 2003). At the physiological level,
ooding modies water relations and carbon xation in
plants. Closing of stomata, with or without leaf dehydration,
reduction of transpiration, and inhibition of photosynthesis
are responses that can occur in hours or days, depending on
the tolerance to ooding of each plant species (Bradford and
Hsiao, 1982; Else et al., 1995; Insausti et al., 2001; Striker et al.,
2005; Mollard et al., 2008, 2010).
Plant species can also adjust to these novel climate conditions through phenotypic plasticity, that is the range of
phenotypes a single genotype can express as a function of its
environment, or adapt through natural selection or migrate to
follow conditions to which they are adapted; these options are
not mutually exclusive, that is, the capacity of a given plant to
alter its physiology, morphology, or phenology and allows it
to tolerate, avoid, or escape a certain stress condition (Nicotra
et al., 2010; Grime et al., 1986). The phenotypic plasticity is
understood to be genetically controlled, heritable, and of potential importance to species evolution (Bradshaw, 2006;
Lande, 2009). With mounting evidence from molecular and
developmental biology, the understanding of the mechanisms
of plasticity, which will be crucial for predicting changes in
species distributions, community composition, and crop
productivity under climate change will be easier (Van Kleunen
et al., 2007; Van Kleunen and Fischer, 2001).
288
environmental challenges (Yadav et al., 2011), but considerable time and investment is required to deliver changes in the
productivity or quality of varieties. The genetic basis of adaptation to environments is complex, and it is difcult to unravel
what sets of genes are required for optimal performance and to
explain the interactions of genes controlling any given trait.
Investment in plant breeding requires assessment of when and
where this is the most economical response for an industry in
dealing with climate change (Chapman et al., 2012).
Biotechnology techniques can help to accelerate the improvement of performance under harsh environmental conditions, particularly because breeding for abiotic stress
tolerance sometimes has linkage drag issues, i.e., undesirable
genes are also transferred along with desirable traits; and also
because reproductive barriers limit the transfer of favorable
alleles from diverse genetic resources. For instance, advances in
genomics coupled with bioinformatics and stress biology can
provide useful genes or alleles for conferring stress tolerance.
Two biotechnology approaches have a key role in this work,
the molecular breeding (MB) and genetic engineering (GE),
and their integration with conventional breeding to develop
crops that are more tolerant of abiotic stresses (Varshney et al.,
2011).
Molecular Breeding
The detection and exploitation of genetic variation have always been an integral part of plant breeding. DNA-based
molecular markers are useful for detecting the genetic variation
available in germplasm collections and breeding lines. During
the past two decades, many different molecular markers have
been developed for most major crop species. These markers
have been used extensively for the development of saturated
molecular genetic and physical maps and for the identication
of genes or quantitative trait loci (QTLs) controlling traits of
economic importance for marker-assisted selection (MAS)
(Varshney et al., 2009). Despite the great collaboration performed by molecular markers, the genomics-assisted breeding
approaches have greatly advanced with the increasing of genome and transcriptome sequence data for several model plant
and crop species, such as rice (IRGSP, 2005), poplar (Tuskan
et al., 2006), sorghum (Paterson et al., 2012), maize (Schnable
et al., 2009), and soybean (Schmutz et al., 2010).
The MB approach involves rst identifying QTLs or genes
for traits of interest, such as tolerance to abiotic stresses, after
identifying the markers associated with QTLs or genes; the
candidates can be introgressed in elite lines through markerassisted backcrossing (MABC). For two most important
abiotic stress, heat and drought, some QTLs for tolerance were
identied in important crops, such as wheat rice and maize
(Paliwal et al., 2012; Changrong et al., 2012; Almeida et al.,
2013).
There are two general approaches to understand the function of a gene: forward genetics and reverse genetics (Alberts
et al., 2007). Reverse genetics is a particular approach in discovering the function of a gene. It begins with a well-characterized phenotype and works toward identifying the gene(s)
responsible for the phenotype. Genetic mapping approaches,
such as QTL mapping and association mapping, are part of
289
Genetic Engineering
The terms GE or genetic modication (GM; also used for
genetically modied) have been used for the processes of
transforming plants (Lawlor, 2013). Crop GE with signaling
components and transcription factors (TFs) lead to the expression of their target transcriptome that consists of several
genes involved in stress adaptation. However, only a few crops,
such as rice (Xiao et al., 2009; Oh et al., 2009), maize (Nelson
et al., 2007; Castiglioni et al., 2008), and canola (Brassica
napus) (Vanderauwera et al., 2007; Wang et al., 2005), expressing the desired TF and other genes, have been tested
290
traits include drought and temperature stress resistance, resistance to pests and disease, which continue to cause crop
losses, salinity, and water logging (Humphreys, 2005; Oerke,
2006). The genetic improvement of plants, based on experiences of the past, is an area that can make contributions to the
adaptation of plants to the new agricultural scenario of the
coming years (Ramalho et al., 2009).
Experience has shown that biotic and abiotic stresses occur
together, although not necessarily all at once. Normally, when
temperatures are elevated, water stress on plants is strong and
pest incidence, among other stresses increases. To identify
more tolerant cultivars to all these factors the available alternative, with proven efciency, is to evaluate the progeny and/
or cultivars in the conditions in which the crops will be grown
(Ramalho et al., 2009).
In this context, the main drawback to the work of breeders
is the interaction of genotypes with environments. In other
words, genotypes respond differently to environmental stimuli. Therefore, especially under tropical conditions, where the
diversity of climate and management adopted by farmers is
higher, the interaction of genotype by environment is the
greatest challenge to be met. Cultivars must be well adapted
and more stable.
References
Alberts, B., Johnson, A., Lewis, J., et al., 2007. Molecular Biology of the Cell, fth
ed. New York, NY: Garland Science Publishing.
Allison, E.H., Perry, A.L., Adger, W.N., et al., 2009. Vulnerability of national
economies to the impacts of climate change on sheries. Fish and Fisheries 10,
173196.
Almeida, G.D., Makumbi, D., Magorososho, C., et al., 2013. QTL mapping in
three tropical maize populations reveals a set of constitutive and adaptive
genomic regions for drought tolerance. Theoretical and Applied Genetics 126,
583600.
Altieri, M.A., Koohafkan, P., 2003. Enduring Farms: Climate Change,
Smallholders and Traditional Farming Communities. Third World Network
Environmental & Development Series 6. Penang, Malaysia: Third World Network
(TWN), pp. 62.
Anjum, F., Yaseen, M., Rasul, E., Wahid, A., Anjum, S., 2003. Water stress in
barley (Hordeum vulgare L.). I. Effect on morphological characters. Pakistan
Journal of Agricultural Sciences 40, 4344.
Armstrong, W., 1979. Aeration in higher plants. Advances in Botanical Research 7,
225332.
Armstrong, W., Drew, M.C., 2002. Root growth and metabolism under oxygen
deciency. In: Waisel, Y., Eshel, A., Kafka, U. (Eds.), Plant Roots: The Hidden
Half, third ed. New York, NY: Marcel Dekker, pp. 729761.
Arnell, N., Liu, C., 2001. Hydrology and water resources. In: McCarthy, J.J.,
Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.S. (Eds.), Climate Change:
Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the
Third Assessment Report of the Intergovernmental Panel on Climate Change.
Cambridge: Cambridge University Press.
Ashmore, M.R., Toet, S., Emberson, L.D., 2006. Ozone A signicant threat to
future world food production? New Phytologist 170, 199201.
Atkinson, M.D., Kettlewell, P.S., Poulton, P.R., Hollins, P.D., 2008. Grain quality in
the Broadbalk wheat experiment and the winter North Atlantic oscillation. Journal
of Agricultural Science 146, 541549.
Babu, R.C., Nguyen, B.D., Chamarerk, V., et al., 2003. Genetic analysis of drought
resistance in rice by molecular markers: Association between secondary traits
and eld performance. Crop Science 43, 14571469.
BaileySerres, J., Voesenek, L.A.C.J., 2008. Flooding stress: Acclimations and
genetic diversity. Annual Review of Plant Biology 59, 313339.
Balla, K., Bedi, Z., Veisz, O., 2007. Heat stress inducted changes in the activity of
antioxidant enzymes in wheat. Cereal Research Communications 35, 197200.
Battisti, D.S., Naylor, R.L., 2009. Historical warnings of future food insecurity with
unprecedented seasonal heat. Science 323, 240244.
Bernier, J., Kumar, A., Ramaiah, A.V., Spaner, D., Atlin, G., 2007. A large-effect QTL
for grain yield under reproductive-stage drought stress in upland rice. Crop
Science 47, 507518.
Bernier, J., Kumar, A., Spaner, D., et al., 2009. Characterization of the effect of rice
drought tolerance qtl12.1 over a range of environments in the Philippines and
eastern India. Euphytica 166, 207217.
Bhatt, R.M., Srinivasa, R.N.K., 2005. Inuence of pod load response of okra to water
stress. Indian Journal of Plant Physiology 10, 5459.
Blom, C.W.P.M., Voesenek, L.A.C.J., Banga, M., et al., 1994. Physiological ecology
of riverside species: Adaptive responses of plants to submergence. Annals of
Botany 74, 253263.
Bradford, K.J., Hsiao, T.C., 1982. Stomatal behavior and water relations of
waterlogged tomato plants. Plant Physiology 70, 15081513.
Bradshaw, A.D., 2006. Unraveling phenotypic plasticity Why should we bother?
New Phytologist 170, 644648.
Bray, E.A., 1997. Plant responses to water decit. Trends in Plant Science 2, 4854.
Bruinsma, J., 2009. The Resource Outlook to 2050: By How Much Do Land, Water
and Crop Yields Need to Increase By 2050?' Expert Meeting on How to feed the
World in 2050. FAO of the United Nations Economic and Social Development
Department, pp. 2426. Rome: FAO.
Castiglioni, P., Warner, D., Bensen, R.J., et al., 2008. Bacterial RNA chaperones
confer abiotic stress tolerance in plants and improved grain yield in maize under
water-limited conditions. Plant Physiology 147, 446455.
Ceccarelli, S., Grando, S., Maatougui, M., et al., 2010. Climate change and
agriculture paper. Plant breeding and climate changes. Journal of Agricultural
Science 148, 627637.
Changrong, Y., Argayoso, M.A., Redoa, E.D., et al., 2012. Mapping QTL for heat
tolerance at owering stage in rice using SNP markers. Plant Breeding 131,
3341.
Chaves, M.M., Pereira, J.S., Maroco, J., et al., 2002. How plants cope with water
stress in the eld photosynthesis and growth? Annals of Botany 89, 907916.
Chapman, S.C., Chakraborty, S., Dreccer, M.F., Howden, S.M., 2012. Plant
adaptation to climate change Opportunities and priorities in breeding. Crop
and Pasture Science 63, 251268.
Cline, W.R., 2007. Global Warming and Agriculture: Impact Estimates by Country.
Washington, DC: Peterson Institute for International Economics.
Collard, B.C.Y., Jahufer, M.Z.Z., Brouwer, J.B., Pang, E.C.K., 2005. An introduction
to markers, quantitative trait loci (QTL) mapping and marker-assisted selection
for crop improvement: The basic concepts. Euphytica 142, 169196.
Collins, N.C., Tardieu, F., Tuberosa, R., 2008. Quantitative trait loci and crop
performance under abiotic stress: Where do we stand? Plant Physiology 147,
469486.
Colmer, T.D., 2003. Long-distance transport of gases in plants: A perspective on
internal aeration and radial oxygen loss from roots. Plant Cell and Environment
26, 1736.
Colmer, T.D., Voesenek, L.A.C.J., 2009. Flooding tolerance: Suites of plant traits in
variable environments. Functional Plant Biology 36, 665681.
Dixon, J., Nalley, L., Kosina, P., et al., 2006. Adoption and economic impact of
improved wheat varieties in the developing world. Journal of Agricultural Science
144, 489502.
Else, M.A., Davies, W.J., Malone, M., Jackson, M.B., 1995. A negative hydraulic
message from oxygen-decient roots of tomato plants? Inuence of soil ooding
on leaf water potential, leaf expansion, and synchrony between stomatal
conductance and root hydraulic conductivity. Plant Physiology 109,
10171024.
FAO, 2005. Impact of Climate Change, Pests, and Diseases on Food Security and
Poverty Reduction. Special Event Background Document. In: 31st Session of the
Committee on World Food Security. Rome: FAO, pp. 2326.
FAO, 2007. Climate Change The Issue. Available at: http://www.fao.org/clim/
issues_en.htm (accessed 07.05.14).
Farooq, M., Basra, S.M.A., Wahid, A., et al., 2008. Physiological role of
exogenously applied glycinebetaine in improving drought tolerance of ne grain
aromatic rice (Oryza sativa L.). Journal of Agronomy and Crop Science 194,
325333.
291
Farre, G., Ramessar, K., Twyman, R.M., Capell, T., Christou, P., 2010. The
humanitarian impact of plant biotechnology: Recent breakthroughs vs bottlenecks
for adoption. Current Opinion in Plant Biology 13, 219225.
Feng, Z.Z., Kobayashi, K., 2009. Assessing the impacts of current and future
concentrations of surface ozone on crop yield with meta-analysis. Atmospheric
Environment 43, 15101519.
Fiedler, S., Vepraskas, M.J., Richardson, J.L., 2007. Soil redox potential: Importance,
eld measurements, and observations. Advances in Agronomy 94, 256.
Fridman, E., Zamir, D., 2012. Next-generation education in crop genetics. Current
Opinion in Plant Biology 15, 218223.
Fuhrer, J., 2009. Ozone risk for crops and pastures in present and future climate.
Naturwissenschaften 96, 173194.
Gaspar, T., Franck, T., Bisbis, B., et al., 2002. Concepts in plant stress physiology.
Application to plant tissue cultures. Plant Growth Regulation 37, 263285.
Gibberd, M.R., Cocks, P.S., 1997. Effect of waterlogging and soil pH on the microdistribution of naturalized annual legumes. Australian Journal of Agricultural
Research 48, 223229.
Gibberd, M.R., Gray, J.D., Cocks, P.S., Colmer, T.D., 2001. Waterlogging tolerance
among a diverse range of Trifolium accessions is related to root porosity, lateral
root formation, and aerotrophic rooting. Annals of Botany 88, 579589.
Grime, J.P., Crick, J.C., Rincn, E., 1986. The ecological signicance of plasticity.
In: Jennings, D.H., Trewavas, A.J. (Eds.), Plasticity in Plants: Symposia of the
Society for Experimental Biology. Scarborough: Pindar, pp. 529.
Grimoldi, A.A., Insausti, P., Roitman, G.G., Soriano, A., 1999. Responses to ooding
intensity in Leontodon taraxacoides. New Phytologist 141, 119128.
Grist, D.H. (Ed.), 1986. Rice, sixth ed. New York, NY: Longman.
Habash, D.Z., Kehel, Z., Nachit, M., 2009. Genomic approaches for designing durum
wheat ready for climate change with a focus on drought. Journal of Experimental
Botany 60, 28052815.
Hansen, J., Sato, M., Ruedy, R., 2012. Perception of climate change. Proceedings of
the National Academy of Sciences of the United States of America 109, 32.
Harb, A., Krishnan, A., Ambavaram, M.M.R., Pereira, A., 2010. Molecular and
physiological analysis of drought stress in Arabidopsis reveals early responses
leading to acclimation in plant growth. Plant Physiology 154, 12541271.
Hattori, Y., Nagai, K., Furukawa, S., et al., 2009. The ethylene response factors
SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460,
10261030.
HilleRisLambers, D., Vergara, B.S., 1982. Summary results of an international
collaboration on screening methods for ood tolerance. In: Proceedings of the
1981 International Deepwater Rice Workshop, 347353. Los Baos, Philippines:
International Rice Research Institute.
Hirayama, T., Shinozaki, K., 2010. Research on plant abiotic stress responses in the
post-genome era: Past, present and future. Plant Journal 61, 10411052.
Holland, J.B., 2004. Implementation of molecular markers for quantitative traits in
breeding programs Challenges and opportunities. In: Proceedings of 4th
International Crop Science Congress, Brisbane, Australia, September 26October
1, 2004. NSW, Australia: The Regional Institute Ltd.
Humphreys, M.O., 2005. Genetic improvement of forage crops Past, present and
future. Journal of Agricultural Science 143, 441448.
Insausti, P., Grimoldi, A.A., Chaneton, E.J., Vasellati, V., 2001. Flooding induces a
suite of adaptive plastic responses in the grass Paspalum dilatatum. New
Phytologist 152, 291299.
Intergovernmental Panel On Climate Change, IPCC, 2007. Climate change 2007: The
physical science basis. Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on Climate Change, pp. 996.
Cambridge: Cambridge University Press.
IRGSP, 2005. The map-based sequence of the rice genome. Nature 1, 793800.
Jackson, M.B., 2004. The impact of ooding stress on plants and crops. Available
at: http://www.plantstress.com/Articles/waterlogging_i/waterlog_i.htm (accessed
07.05.14).
Jackson, M.B., Ram, P.C., 2003. Physiological and molecular basis of susceptibility
and tolerance of rice plants to complete submergence. Annals of Botany 91,
227241.
Jaleel, C.A., Anivannan, P., Lakshmanan, G.M.A., Gomathinayagam, M.,
Panneerselvam, R., 2008. Alterations in morphological parameters and
photosynthetic pigment responses of Catharanthus roseus under soil water
decits Colloids Surf B. Biointerfaces 61, 298303.
Jaleel, C.A., Manivannan, P., Wahid, A., et al., 2009. Drought stress in plants: A
review on morphological characteristics and pigments composition. International
Journal of Agriculture and Biology 11, 100105.
Jones, P.D., Briffa, K.R., Osborn, T.J., et al., 2009. High-resolution
palaeoclimatology of the last millennium: A review of current status and future
prospects. Holocene 19, 349.
292
Justin, S.H.F.W., Armstrong, W., 1987. The anatomical characteristics of roots and
plant response to soil ooding. New Phytologist 106, 465495.
Kamoshita, A., Wade, L.J., Ali, M.L., et al., 2002. Mapping QTLs for root
morphology of a rice population adapted to rainfed lowland conditions.
Theoretical and Applied Genetics 104, 880893.
Khowaja, F.S., Norton, G.J., Courtois, B., Price, A.H., 2009. Improved resolution in
the position of drought-related QTLs in a single mapping population of rice by
meta-analysis. BMC Genomics 10, 276.
Kozlowski, T.T., 1997. Responses of woody plants to ooding and salinity. Tree
Physiology Monograph No. 1. Victoria: Heron Publishing, pp. 129.
Kozlowski, T.T., Pallardy, S.G., 1984. Effects of ooding on water, carbohydrate and
mineral relations. In: Kozlowski, T.T. (Ed.), Flooding and Plant Growth. Orlando,
FL: Academic Press Inc, pp. 165193.
Kusaka, M., Ohta, M., Fujimura, T., 2005. Contribution of inorganic components to
osmotic adjustment and leaf folding for drought tolerance in pearl millet.
Physiologia Plantarum 125, 474489.
Laan, P., Tosserams, M., Blom, C.W.P.M., Veen, B.W., 1990. Internal oxygen
transport in Rumex species and its signicance for respiration under hypoxic
conditions. Plant and Soil 122, 3946.
Lanceras, J., Pantuwan, G., Jongdee, B., Toojinda, T., 2004. Quantitative trait loci
associated with drought tolerance at reproductive stage in rice. Plant Physiology
135, 384399.
Latte, R., Blum, A., Atlin, G., et al., 2004. Using secondary traits to help identify
drought tolerant genotypes. In: Fischer, K.S., Latte, R., Fukai, S., Atlin, G.,
Hardy, B. (Eds.), Breeding Rice for Drought-Prone Environments. Los Banos:
International Rice Research Institute, pp. 3748.
Lande, R., 2009. Adaptation to an extraordinary environment by evolution of
phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology
22, 14351446.
Lawlor, D.W., 2013. Genetic engineering to improve plant performance under
drought: Physiological evaluation of achievements, limitations, and possibilities.
Journal of Experimental Botany 64, 83108.
Lobell, D.B., Burke, M.B., Tebaldi, C., et al., 2008. Prioritizing climate change
adaptation needs for food security in 2030. Science 319, 607610.
Mackill, D.J., Amante, M.M., Vergara, B.S., Sarkarung, S., 1993. Improved
semidwarf rice lines with tolerance to submergence of seedlings. Crop Science
33, 749753.
Mackill, D.J., Ismail, A.M., Pamplona, A.M., et al., 2010. Stress tolerant rice
varieties for adaptation to a changing climate. Crop, Environment &
Bioinformatics 7, 250259.
Mahajan, S., Tuteja, N., 2005. Cold, salinity and drough stresses on overview.
Archives of Biochemistry and Biophysics 444, 139158.
Marshall, A., Reidunn, B.A., Audenaert, D., et al., 2012. Tackling drought stress:
Receptor-like kinases present new approaches. Plant Cell 24, 22622278.
Martinez, J.P., Silva, H., Ledent, J.F., Pinto, M., 2007. Effect of drought stress on
the osmotic adjustment, cell wall elasticity and cell volume of six cultivars of
common beans (Phaseolus vulgaris L.). European Journal of Agronomy 26,
3038.
McClean, C.J., 2005. Africa plant diversity and climate change. Annals of the
Missouri Botanical Garden 92, 139152.
Meehl, G.A., Stocker, T.F., Collins, W.D., et al., 2007. Global Climate Projections.
In: Solomon, S., Qin, D., Manning, D., Chen, Z., Marquis, M., Averyt, K.B.,
Tignor, M., Miller, H.L. (Eds.), Climate Change, The Physical Science Basis.
Contribution of Working Group I to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge; New York, NY:
Cambridge University Press.
Mollard, F.P.O., Striker, G.G., Ploschuk, E.L., Insausti, P., 2010. Subtle
topographical differences along a oodplain promote different plant strategies
among Paspalum dilatatum subspecies and populations. Austral Ecology 35,
189196.
Mollard, F.P.O., Striker, G.G., Ploschuk, E.L., Vega, A.S., Insausti, P., 2008.
Flooding tolerance of Paspalum dilatatum (Poaceae: Paniceae) from upland and
lowland positions in a natural grassland. Flora 203, 548556.
Moorhead, A., 2009. Climate, agriculture and food security: A strategy for change.
Washington, DC: Alliance of the CGIAR Centers.
Naidoo, G., Mundree, S.G., 1993. Relationship between morphological and
physiological responses to waterlogging and salinity in Sporobolus virginicus
(L.) Kunth. Oecologia 93, 360366.
Nam, N.H., Chauhan, Y.S., Johansen, C., 2001. Effect of timing of drought stress on
growth and grain yield of extra-short-duration pigeonpea lines. Journal of
Agricultural Sciences 136, 179189.
Nelson, D.E., Repetti, P.P., Adams, T.R., et al., 2007. Plant nuclear factor Y (NF-Y)
B subunits confer drought tolerance and lead to improved corn yields on water-
Sinclar, T.R., Sinclair, C.D., Messina, A., Beatty, M., 2010. Samples assessment
across the United States of the benets of altered soybean drought traits.
Agronomy Journal 102, 373377.
Smith, C.P., 2011. Farming's Climate-Smart Future: Placing Agriculture at the Heart
of Climate-Change Policy. Netherlands: Technical Centre for Agriculture and
Rural Co-Operation, GMDC Library.
Smith, K.A., Russell, R.S., 1969. Occurrence of ethylene, and its signicance, in
anaerobic soil. Nature 222, 769771.
Stern, N., 2005. Stern Review on the Economics of Climate Change. Cambridge:
Cambridge University Press.
Striker, G.G., Insausti, P., Grimoldi, A.A., Ploschuk, E.L., Vasellati, V., 2005.
Physiological and anatomical basis of differential tolerance to soil ooding of
Lotus corniculatus L. and Lotus glaber Mill. Plant and Soil 276, 301311.
Swamy, M.B.P., Vikram, P., Dixit, S., Ahmed, H.U., Kumar, A., 2011. Meta-analysis
of grain yield QTL identied during agricultural drought in grasses showed
consensus. BMC Genomics 12, 319.
Tierney, M.B., Lamour, K.H., 2005. An introduction to reverse genetic tools for
investigating gene function. Plant Health Instructor 1025, 01.
Thomas, C.D., Cameron, A., Green, R.E., et al., 2004. Extinction risk from climate
change. Nature 427, 145148.
Toker, C., Lluch, C., Tejera, N.A., Serraj, R., Siddique, K.H.M., 2007. Abiotic
stresses. In: Yadav, S.S., Redden, R.J., Chen, W., Sharma, B. (Eds.), Chickpea
Breeding and Management. Wallingford, UK: CAB, pp. 474496.
Toojinda, T., Siangliw, M., Tragoonrung, S., Vanavichit, A., 2003. Molecular genetics
of submergence tolerance in rice: QTL analysis of key traits. Annals of Botany
91, 243253.
Tubiello, F.N., Fischer, G., 2007. Reducing climate change impacts on agriculture:
Global and regional effects of mitigation 20002080. Technological Forecasting
and Social Change 74, 10301056.
Tuskan, G.A., DiFazio, S., Jansson, S., et al., 2006. The genome of black
cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 15961604.
Vanderauwera, S., Steene, N.V., Cotte, B.V., Metzlaff, M., Breusegem, F.V., 2007.
Silencing of poly (ADP-ribose) polymerase in plants alters abiotic stress signal
transduction. Proceedings of the National Academy of Sciences of the United
States of America 104, 1515015155.
Van Kleunen, M., Fischer, M., 2001. Adaptive evolution of plastic foraging
responses in a clonal plant. Ecology 82, 33093319.
Van Kleunen, M., Lenssen, J.P.M., Fisher, M., Kroon, H., 2007. Selection on
phenotypic plasticity of morphological traits in response to ooding and
competition in the clonal shore plant Ranunculus reptans. Journal of Evolutionary
Biology 20, 21262137.
Varshney, R.K., Bansal, K.C., Aggarwal, P.K., Datta, S.K., Craufurd, P.Q., 2011.
Agricultural biotechnology for crop improvement in a variable climate: Hope or
hype? Trends in Plant Science 16, 363371.
Varshney, R.K., Nayaki, S.N., May, G.D., et al., 2009. Next-generation sequencing
technologies and their implications for crop breeding. Trends in Biotechnology
27 (9), 522530.
Vartapetian, B.B., Jackson, M., 1997. Plant adaptations to anaerobic stress. Annals
of Botany 79, 320.
Venuprasad, R., Bool, M.E., Dalid, C.O., et al., 2009. Genetic loci responding to two
cycles of divergent selection for grain yield under drought stress in a rice
breeding population. Euphytica 167, 261269.
293
Vergara, B.S., Mazaredo, A., 1975. Screening for resistance to submergence under
greenhouse conditions. Proceedings of the International Seminar on Deepwater
Rice, pp. 6770. Rice Research Institute: Dhaka.
Voesenek, L.A.C.J., Rijnders, J., Peeters, A.J.M., Van De Steeg, H.M.V., De Kroon,
H., 2004. Plant hormones regulate fast shoot elongation under water: From
genes to communities. Ecology 85, 1627.
Walker, G., 2007. A world melting from the top down. Nature 446, 718721.
Wang, Y., Ying, J., Kuzma, M., et al., 2005. Molecular tailoring of farnesylation for
plant drought tolerance and yield protection. Plant Journal 43, 413424.
Wassmann, R.S.V.K., Jagdish, S., Heur, A., et al., 2009. Climate change affecting
rice production: The physiological and agronomic basis for possible adaptation
strategies. Advances in Agronomy 101, 59122.
Wegner, L.H., 2010. Oxygen transport in waterlogged plants. In: Mancuso, S.,
Shabala, S. (Eds.), Waterlogging Signalling and Tolerance in Plants. Heidelberg:
SpringerVerlag Berlin, pp. 322.
White, T.L., Adams, W.T., Neale, D.B., 2007. Forest Genetics. CABI, pp. 682.
Williams, S.E., Bolitho, E.E., Fox, S., 2003. Climate change in Australian tropical
rainforests: An impending environmental catastrophe. Proceedings of the Royal
Society of London Series B-Biological Sciences 270 (1527), 18871892.
Xiao, B.Z., Chen, X., Xiang, C.B., et al., 2009. Evaluation of seven function-known
candidate genes for their effects on improving drought resistance of transgenic
rice under eld conditions. Molecular Plant 2, 7383.
Xu, K., Mackill, D.J., 1996. A major locus for submergence tolerance mapped on
rice chromosome 9. Molecular Breeding 2, 219224.
Xu, K., Xia, X., Fukao, T., et al., 2006. Sub1A is an ethylene response factor-like
gene that confers submergence tolerance to rice. Nature 442, 705708.
Yadav, S.S., Redden, R., Hateld, J.L., et al., 2011. Crop Adaptation to Climate
Change. Hoboken, NJ: John Wiley & Sons.
Zhao, C.X., Guo, L.Y., Jaleel, C.A., Shao, H.B., Yang, H.B., 2008. Prospects for
dissecting plant-adaptive molecular mechanisms to improve wheat cultivars in
drought environments. Compt Rendu de la Societe Biologique 331, 579586.
Zheng, B., 2006. QTLs and candidate genes for rice root growth under ooding and
upland conditions. Acta Genetica Sinica 33, 141151.
Zheng, B., Yang, L., Mao, C., Huang, Y., Wu, P., 2008. Comparison of QTLs for
rice seedling morphology under different water supply conditions. Journal of
Genetics and Genomics 35, 473484.
Zheng, B.S., Yang, L., Zhang, W.P., et al., 2003. Mapping QTLs and candidate
genes for rice root traits under different water supply conditions and comparative
analysis across three populations. Theoretical and Applied Genetics 107,
15051515.
Relavant Websites
https://www.fao.org.br/
FAO.
https://www.ipcc.ch/
Intergovernmental Panel on Climate Change.
Glossary
Climate change A change in the state of the climate that
can be identified (e.g., by using statistical tests) by changes
in the mean or the variability of climate properties and that
persists for an extended period, typically decades or longer.
Climate change may be due to natural internal processes or
external forces or due to persistent anthropogenic changes
in the composition of the atmosphere or in land use.
Climate change adaptation An adjustment in natural or
human systems in response to actual or expected climatic
stimuli or their effects, which moderates harm or exploits
benecial opportunities.
Climate change mitigation A human intervention to
reduce the human impact on the climate system; it includes
strategies to reduce greenhouse gas (GHG) sources and
emissions and enhance GHG sinks.
Command-and-control policy In the climate change case,
this involves a government-imposed limit on greenhouse
gas emissions where the limit should reect a balance
between the damages from emissions and the cost of
reducing emissions.
Externalities Occur when a change in the production or
consumption of an individual or rm affects indirectly the
well-being of another individual or rm. Externalities can be
positive or negative.
Greenhouse gas (GHG) Those gaseous constituents of the
atmosphere, both natural and anthropogenic, that absorb
and emit radiation at specic wavelengths within the
spectrum of thermal infrared radiation emitted by the
Earth's surface, the atmosphere itself, and by clouds. This
property causes the greenhouse effect. Water vapor (H2O),
Introduction
294
doi:10.1016/B978-0-444-52512-3.00001-2
295
0.6
0.5
Degrees celsius
0.4
0.3
0.2
0.1
19
5
19 0
5
19 2
54
19
5
19 6
5
19 8
60
19
6
19 2
64
19
6
19 6
6
19 8
7
19 0
7
19 2
74
19
7
19 6
78
19
8
19 0
82
19
8
19 4
8
19 6
88
19
9
19 0
92
19
9
19 4
9
19 6
98
20
0
20 0
02
20
0
20 4
0
20 6
0
20 8
10
20
12
0.1
0.2
El Nino
La Nina
Other
Figure 1 Temperature evolution from 1950 to 2012. NOAA, State of the climate, Global Analysis Annual 2012 (http://www.ncdc.noaa.gov/sotc/
global/2012/13).
What is Projected?
Given continuing emissions, a changed future climate is expected
in terms of temperature changes, as projected in Figure 3, along
with associated precipitation and other changes (Knutti and
Sedlek, 2012). In turn, this would cause changes in such things
as fresh water supplies; snow pack; location of agricultural crop
production; extreme event incidence; sea level; coastal inundation; and pest, diseases, bird, animal, and plant ranges.
296
400
2000
350
1600
1400
1200
300
CH4 (ppb)
1800
Carbon dioxide (CO2)
Methane (CH4)
Nitrous oxide (N2O)
1000
800
600
250
0
500
1000
Year
1500
2000
Production
With regard to the agricultural sector, climate change can alter
yields and crop acreage (Adams et al., 1990, 1999; Reilly et al.,
2002; IPCC, 2007b). Climate change has diverse implications
involving the effects of carbon dioxide, temperature, precipitation (amount, distribution, and intensity), and extreme
events (droughts, hurricanes, oods, etc.). All of these, in turn,
alter production, as a number of authors have reviewed.
Using a historical statistical approach, Chen et al. (2004)
found that crop yield effects of temperature and precipitation
changes varies with crop. This has been subsequently veried by
others (Tack et al., 2012; Schlenker and Roberts, 2009). Studies
have also investigated the effects of climate extremes, such as
hot days, standard deviation in temperature, precipitation intensity, and droughts (McCarl et al., 2008; Huang and Khanna,
2010). Studies have also been carried out using crop simulators
nding temperature and precipitation effects (Parry et al., 2004;
Tubiello et al., 2002; Backlund et al., 2008; Iglesias et al., 2012).
Yield effects also arise from increased atmospheric concentrations of carbon dioxide, where it serves as a fertilizer,
simulating some species of crops to grow faster (C3 crops,
including wheat, potatoes, etc.; Darwin and Kennedy, 2000).
However, this is not the case for C4 crops (corn, sorghum,
etc.), where benets appear to arise only under moisture stress
(Leakey, 2009). Attavanich and McCarl (2011) included this in
a statistical investigation by merging the United States Department of Agriculture data with crop data from eld-level
free air carbon enrichment experiments (Long et al., 2006)
nding that in some cases yields are substantially inuenced
and possibly confused with technical progress.
Changes in crop production also affect crop prices, economic returns, and land allocation with substantial shifts
projected (Adams et al., 1990, 1995, 1999; Reilly et al., 2002;
McCarl, 2011).
Climate change can also alter resources for production.
Kjellstrom et al. (2009) concluded that heat exposure caused
5
4
3
Historical (42)
RCP 2.6 (26)
RCP 4.5 (32)
RCP 6.0 (17)
RCP 8.5 (30)
What could happen
2
1
0
1
1900
1950
2000
2050
2100
Year
Figure 3 Global temperature change from new coupled model intercomparison project phase 5 (CMIP5) climate model projections. RCP,
representative concentration pathways. Adapted from Knutti, R., Sedlcek, J., 2012. Robustness and uncertainties in the new CMIP5 climate model
projections. Nature Climate Change 3, 369373.
Welfare
Efforts have been made to estimate the economic consequences of climate change on agriculture in terms of land
values and social welfare in terms of producer income and
measures of consumer satisfaction. A series of studies initially
found climate change to be detrimental for the welfare of
those involved with agriculture but as the crop scope, carbon
dioxide effects, and adaptation possibilities were added, it
became benecial (Adams et al., 1990, 1995, 1999; Reilly et al.,
2002; McCarl, 2011). However, others argued that it would be
detrimental, and appraisals in countries like Mali, Butt et al.
(2005) certainly showed that. In terms of land value, Mendelsohn et al. (1994) analyzed a cross-section dataset consisting of 3000 counties in the United States and found that
higher annual temperatures reduced average farm values.
Broader scoped studies have shown varying results depending
on location with some regions beneting but some warm regions losing (see the review and results in Van Passel et al.,
2012).
In terms of water resource effects, Hurd and Rouhi-Rad
(2012) and Adams and Peck (2008) stated that climate change
effects on water give rise to economic welfare loss through
lower consumer surplus resulting from higher water prices and
costs of actions taken due to water shortage.
Forestry is sensitive to climate change as well. However,
Alig et al. (2002) showed that in the United States small
welfare increases would arise. In terms of global timber markets, Sohngen and Mendelsohn (1998) found that supply of
timber would increase and bring benet to the whole timber
market.
In terms of more aggregate measures, Tol (2014) reviewed
17 multisector studies and concluded that the initial net effects
are positive but they become negative in the long run.
All in all, as shown above, climate change poses a serious
and persistent threat to portions of the world and to increasingly larger parts as changes become larger.
297
Mitigation involves actions aimed at reducing the magnitude of climate change drivers, like reducing GHG emissions. Such actions are designed to reduce current and
future atmospheric concentrations. In turn, such actions are
designed to limit future climate change along with ocean
acidication (IPCC, 2007d; Fri et al., 2010).
Adaptation involves actions to reduce the damage arising
from a given amount of climate change plus exploiting
the positive opportunities. This involves manipulating
management, information dissemination, infrastructure
investment, and enterprise choice to improve coping
mechanisms.
Geoengineering (also climate engineering) involves purposeful intervention in the Earth's climatic system with the
aim of reducing climate change. The two basic thrusts involve solar radiation management and carbon dioxide removal (Izrael et al., 2009). The subject is controversial and
298
Information Efforts
Information Value
One policy approach where there has been a lot of investment
involves information development. Coping with climate
change involves decisions across multiperiods based on information available to decision makers. Under climate change,
decisions are often made in the face of uncertainty and are
adjusted over time. In fact, information on climate change and
its impacts are insufcient today. First, science and technology
have not been developed yet to accurately assess and predict
climate change. There are still numerous unexplored problems
associated with climate change. Moreover, it is costly to collect
and disseminate all relevant information, particularly in developing countries (Berrang-Ford et al., 2011; Bryan et al.,
2009; Deressa et al., 2009).
Because the information is crucial for decision making,
there is implicit value associated with it. The authors have used
Figure 4 to shed light on the value of information within the
climate change context. Here, they focus mainly on information for adaptation. Similar arguments can be extended to
mitigation decisions.
The curves in Figure 4 represent different agricultural productions in terms of value of activity on land in response to
climate variables, for instance, temperature in this case. As
Value of activity
Corn
A
B
Wheat
Grazing
Idle
T3
T1
T4
T2
Temperature
Figure 4 Value of activity on land in response to temperature. Adapted from Mendelsohn, R., Nordhaus, W., Shaw, D., 1994. The impact of
global warming on agriculture: A Ricardian analysis. American Economic Review 84 (4), 753771 and Kelly, D.L., Kolstad, C.D., Mitchell, G.T.,
2005. Adjustment costs from environmental change. Journal of Environmental Economics and Management 50(3), 468495.
299
Generally speaking, economists prefer market-based trading or taxation methods to direct market regulation. Through
such mechanisms, policy makers internalize the externality:
providing emitters with incentives to reduce emissions and
innovate in developing new, lower emitting technologies
(Nordhaus, 2008).
Recently, attention has been paid to voluntary participation
in emission reduction programs with emitters allowed to opt
in and choose to produce carbon offsets. If emitters choose to
join the program (opt in), then they are going to be directly
paid for the GHG abatement and will also be provided with
liability for any future GHG emissions. Also, AF is generally
mentioned as sectors that are not capped but ones that may
sell emission reductions or sequestration increases into the
market place.
Beyond the market and command-and-control approaches,
a number of other policy approaches are possible. For example, Fri et al. (2010) mentioned:
300
301
Who Adapts?
Climate adaptation can be initiated by actors across multiple
levels, such as individuals, rms, and public entities. In general, such adaptation actions are undertaken by private and
public parties with important distinctions.
Private party adaptation (also called autonomous adaptation IPCC, 2001; Smith et al., 2000) is initiated by private
agents acting in their own best interests. Such individuals are
altering operations in reaction to climate. Much private party
adaptation has been done in AF for centuries (McCarl, 2007).
Adaptations can be observed today. For example, in AF, Seo
and Mendelsohn (2008a) found evidence of shifts in livestock
populations as climate evolves, whereas Mu et al. (2013)
found evidence of land use and stocking rate shifts and Park
(2012) found evidence of crop mix shifts.
Public party adaptation, sometimes called planned adaptation, is collectively implemented by governments or other
societal organizations. Activities in this domain correct for
market failures in the classical public good sense (Samuelson,
1954) where private parties do not reap the full gain of
adaptation or where private parties cannot adapt due to limited resources, knowledge, or capability (Speranza et al., 2010;
Hallegatte et al., 2011).
302
planting and harvesting date, crop varieties, crops mix, livestock species, irrigation, pest management strategy, shade
provision, insurance use, re control, etc. (Klein et al., 1999;
McCarl, 2007). In unmanaged AF ecosystems, natural adaptation is occurring but perhaps at an undesirable pace and thus
shifting to more active management may be possible. On the
public side, a number of possible strategies can be pursued,
including the following, as summarized by McCarl (2007):
Observed adaptation
Contemporary adaptation has been examined by looking at
how AF practices vary over space and respond to climate
conditions over time (Chen and McCarl, 2001; Seo and
Modeled adaptation
A number of studies have tried to examine potential adaptations by predicting their nature and implications using
modeling. In such efforts, adaptation can only employ possibilities portrayed in the model, so it is important to have an
augmented set of production possibilities that can be used in
the face of climate change. A number of ndings have arisen
from such studies. For example:
Economic Tools
Many studies have been done regarding climate change issues.
Broadly speaking, these have involved a statistical, spatially
observed data approach and a simulation, structural approach
303
Combined methods
Statistical spatial modeling
Statistical, spatial-based models examine climate change effects, adaptation, and mitigation using historical data on
practices employed and their consequences. Typically, statistical or econometrical approaches over panel datasets are
used, separating those factors that could account for different
effects in different places. In the effects and adaptation arenas,
one looks at data across space and time characterized by alternative climates and can infer the following: (1) effects of
climate change on land values (Mendelsohn et al., 1994), crop
yields (Chen et al., 2004), or input use (Chen and McCarl,
2001) or (2) adaptation in terms of land use (Mu et al., 2013),
crop mix (Park, 2012), livestock species (Zhang et al., 2013),
or livestock type (Seo et al., 2009b). In the mitigation arena,
one looks at how productivity is altered by adoption of mitigation strategies and infers the cost of achieving mitigation
(Antle and Capalbo, 2001).
Advantages of this method are that the behavior of farmers
and changes in the environment are both embedded in the
data and in the estimated model and one can control a
number of factors, like soil quality (Adams et al., 1998). Disadvantages are that prices are assumed to be constant, that
there is generally no cost for farmers or companies to adapt to
climate change, and that the model cannot completely capture
phenomena in the dataset or beyond the range of the dataset
(like high CO2 levels) (McCarl et al., 2010).
Structural modeling
A structural modeling approach generally combines biophysical and economic models under climate change data to
project the effects of climate change issues (Lambi and Molua,
2007). In general, it uses an assumed behavioral economic
model often based on mathematical optimization. For instance, researchers often used welfare maximization under
climate change to simulate market reactions (Adams et al.,
1990, 1999; Reilly et al., 2002).
The strength of this approach is that it presents comprehensive responses and adjustments from physical and
economic aspects of agriculture to climate change examining
phenomena beyond the scope of the current data (Schimmelpfennig et al., 1996). For instance, Butt et al. (2005) and
Arndt et al. (2012) used structural methods to simulate the
effects of climate change in developing countries without large
data requirements. Also, changes in market prices can be
captured and then employed in welfare analysis (Adams and
Hurd, 2002).
However, this type of model assumes the motivation for
decision making (i.e., prot maximization) and the mechanism for market clearing. The strength of the adaptations and
mitigation modeling is purely dependent on the production
possibilities included in the model (Adams et al., 1998;
McCarl et al., 2010) and can lead to under- or overestimates
(Adams and Hurd, 2002). Another problem associated with
this method is that one usually extends the conclusions of
some regionally specic experimental cases to more general
Concluding Comments
The authors have reviewed the evidence for climate change, the
causes and the projections followed by a review of possible
information, adaptation, and mitigation actions. In the discussion, they have attempted to provide the reader with an
introduction to the vast literature by extensive referencing.
Given the vastness of the issue, this was intended only to be an
introduction and a guide to where one might go to learn more.
References
Adams, R.M., Adams, D.M., Callaway, J., Chang, C.C., McCarl, B.A., 1993.
Sequestering carbon on agricultural land: Social cost and impacts on timber
markets. Contemporary Economic Policy 11 (1), 7687.
Adams, D.M., Alig, R.J., McCarl, D.A., Callaway, J.M., Winnett, S.M., 1999.
Minimum cost strategies for sequestering carbon in forests. Land Economics 75
(3), 360374.
Adams, R.M., Fleming, R.A., Chang, C.C., McCarl, B.A., Rosenzweig, C., 1995. A
reassessment of the economic effects of global climate change on US
agriculture. Climatic Change 30 (2), 147167.
Adams, R.M., Hurd, B.H., 2002. Natural resource system challenge: Climate change,
human systems and policy. In: Yotova, A. (Ed.), Encyclopedia of Life Support
Systems (EOLSS), Developed Under the Auspices of the UNESCO, vol. 1.
Oxford: EOLSS Publishers.
Adams, R.M., Hurd, B.H., Lenhart, S., Leary, N., 1998. Effects of global climate
change on agriculture: An interpretative review. Climate Research 11 (1),
1930.
Adams, R.M., McCarl, B.A., Segerson, K., et al., 1999. The economic effects of
climate change on US agriculture. In: Mendelsohn, R., Neumann, J.E. (Eds.),
Impact of Climate Change on the United States Economy. Cambridge: Cambridge
University Press.
Adams, R.M., Peck, D.E., 2008. Effects of climate change on water resources.
Choices 23 (1), 1214.
304
Adams, R.M., Rosenzweig, C., Peart, R.M., et al., 1990. Global climate change and
US agriculture. Nature 345, 219224.
Alig, R.J., Adams, D.M., McCarl, B.A., 2002. Projecting impacts of global climate
change on the US forest and agriculture sectors and carbon budgets. Forest
Ecology and Management 169 (1), 314.
Antle, J.M., Capalbo, S.M., 2001. Econometric-process models for integrated
assessment of agricultural production systems. American Journal of Agricultural
Economics 83 (2), 389401.
Arndt, C., Chinowsky, P., Robinson, S., et al., 2012. Economic development under
climate change. Review of Development Economics 16 (3), 369377.
Attavanich, W., McCarl, B.A., 2011. The effect of climate change, CO2 fertilization,
and crop production technology on crop yields and its economic implications on
market outcomes and welfare distribution. In: Selected Paper Presented at 2011
Agricultural and Applied Economics Association Annual Meeting, July 2426.
Pittsburgh, PA: AAEA.
Attavanich, W., McCarl, B.A., Ahmedov, Z., Fuller, S.W., Vedenov, D.V., 2013.
Climate change and infrastructure: Effects of climate change on US grain
transport. Nature Climate Change 3, 638643.
Backlund, P., Janetos, A.C., Schimel, D., 2008. The Effects of Climate Change on
Agriculture, Land Resources, Water Resources, and Biodiversity in the United
States. Synthesis and Assessment Product 4.3. Washington, DC: U.S.
Environmental Protection Agency, Climate Change Science Program,
240 pp. Available at: http://treesearch.fs.fed.us/pubs/32781
(accessed 29.04.14).
Baker, J.S., McCarl, B.A., Murray, B.C., et al., 2010. Net farm income and land use
under a U.S. greenhouse gas cap and trade. American Journal of Agricultural
Economics, Applied Economic Perspectives and Policy Issues 17, 15.
Barrett, S., 2007. The incredible economics of geoengineering. Environmental and
Resource Economics 39 (1), 4554.
Bates, B.C., Kundzewicz, Z.W., Wu, S., Palutikof, J.P. (Eds.), 2008. Climate change
and water. IPCC Technical Paper VI. Geneva: IPCC Secretariat.
Bellamy, R., Chilvers, J., Vaughan, N.E., Lenton, T.M., 2012. A review of climate
geoengineering appraisals. Wiley Interdisciplinary Reviews: Climate Change 3 (6),
597615.
Berkhout, F., Hertin, J., Gann, D.M., 2006. Learning to adapt: Organisational
adaptation to climate change impacts. Climatic Change 78 (1), 135156.
Berrang-Ford, L., Ford, J.D., Paterson, J., 2011. Are we adapting to climate change?
Global Environmental Change 21 (1), 2533.
Boyd, P.W., 2008. Ranking geoengineering schemes. Nature Geoscience 1, 723724.
de Bruin, K.C., Dellink, R.B., Tol, R.S., 2009. AD-DICE: An implementation of
adaptation in the DICE model. Climatic Change 95 (12), 6381.
Bryan, E., Deressa, T.T., Gbetibouo, G.A., Ringler, C., 2009. Adaptation to climate
change in Ethiopia and South Africa: Options and constraints. Environmental
Science and Policy 12 (4), 413426.
Butt, T.A., McCarl, B.A., Angerer, J., Dyke, P.T., Stuth, J.W., 2005. The economic
and food security implications of climate change in Mali. Climatic Change 68
(3), 355378.
Butt, T.A., McCarl, B.A., Kergna, A.O., 2006. Policies for reducing agricultural
sector vulnerability to climate change in Mali. Climate Policy 5 (6),
583598.
Chen, C.C., Gillig, D., McCarl, B.A., 2001. Effects of climatic change on a water
dependent regional economy: A study of the Texas Edwards Aquifer. Climatic
Change 49 (4), 397409.
Chen, C.C., McCarl, B.A., 2001. Pesticide usage as inuenced by climate: A
statistical investigation. Climatic Change 50, 475487.
Chen, C.C., McCarl, B.A., Schimmelpfennig, D.E., 2004. Yield variability as
inuenced by climate: A statistical investigation. Climatic Change 66 (12),
239261.
Darwin, R., Kennedy, D., 2000. Economic effects of CO2 fertilization of crops:
Transforming changes in yield into changes in supply. Environmental Modeling
and Assessment 5 (3), 157168.
Deressa, T.T., Hassan, R.M., Ringler, C., Alemu, T., Yesuf, M., 2009. Determinants
of farmers' choice of adaptation methods to climate change in the Nile basin of
Ethiopia. Global Environmental Change 19 (2), 248255.
Dietz, S., Stern, N., 2008. Why economic analysis supports strong action on climate
change: A response to the stern review's critics. Review of Environmental
Economics and Policy 2 (1), 94113.
Easterling, W.E., Crosson, P.R., Rosenberg, N.J., et al., 1993. Agricultural impacts of
and responses to climate change in the MissouriIowaNebraskaKansas
(MINK) region. Climatic Change 24 (12), 2361.
Elbakidze, L., McCarl, B.A., 2007. Sequestration offsets versus direct emission
reductions: Consideration of environmental co-effects. Ecological Economics 60
(3), 564571.
Fargione, J., Hill, J., Tilman, D., Polasky, S., Hawthorne, P., 2008. Land clearing
and the biofuel carbon debt. Science 319 (5867), 12351238.
Fri, R., Brown, M., Arent, D., et al., 2010. America's climate choices limiting the
magnitude of future climate change. National Academy Report. Washington, DC:
The National Academies Press.
Gleick, P.H., Adams, D.B., Busalacchi, Jr., A.J., et al., 2000. Water: The
potential consequences of climate variability and change. A Report of the
National Water Assessment Group for the US Global Change Research
Program. Oakland, CA: Pacic Institute for Studies in Development,
Environment, and Security.
Hallegatte, S., De Perthuis, C., Lecocq, F., 2011. Designing climate change
adaptation policies: An economic framework. In: World Bank (Ed.), Policy
Research Working Paper Series, 5568. Washington, DC: World Bank.
Hoogwijk, M., Faaij, A., de Vries, B., Turkenburg, W., 2009. Exploration of regional
and global costsupply curves of biomass energy from short-rotation crops at
abandoned cropland and rest land under four IPCC SRES land-use scenarios.
Biomass and Bioenergy 33 (1), 2643.
Huang, H., Khanna, M., 2010. An econometric analysis of US crop yield and
cropland acreage: Implications for the impact of climate change. In: Selected
paper prepared for presentation at the Agricultural & Applied Economics
Association 2010. AAEA, CAES and WAEA Joint Annual Meeting, July 2527,
2010. Denver, CO: AAEA.
Hurd, B., Rouhi-Rad, M., 2012. Estimating economic effects of changes in climate
and water availability. Climatic Change 117, 110.
Iglesias, A., Quiroga, S., Moneo, M., Garrote, L., 2012. From climate change
impacts to the development of adaptation strategies: Challenges for agriculture in
Europe. Climatic Change 112 (1), 143168.
IPCC, 1990. Climate Change: The IPCC Scientic Assessment. Cambridge:
Cambridge University Press.
IPCC, 1996. IPCC Second Assessment, Climate Change 1995. Cambridge:
Cambridge University Press.
IPCC, 2000. Land Use, Land Use Change, and Forestry, Summary for Policymakers.
Cambridge: Cambridge University Press.
IPCC, 2001. In: McCarthy, J.J., Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.
S. (Eds.), Climate Change 2001: Impacts, Adaptation and Vulnerability
Contribution of Working Group II to the Third Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge: Cambridge University
Press.
IPCC, 2007a. Climate Change 2007: The Physical Science Basis Contribution of
Working Group I to the Fourth Assessment Report of the Intergovernmental Panel
on Climate Change. Cambridge: Cambridge University Press.
IPCC, 2007b. Climate Change 2007: Impacts, Adaptation and Vulnerability
Contribution of Working Group II to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge: Cambridge University
Press.
IPCC, 2007c. Climate Change 2007: Synthesis Report Contribution of Working
Groups I, II and III to the Fourth Assessment Report of the Intergovernmental
Panel on Climate Change. Cambridge: Cambridge University Press.
IPCC, 2007d. Climate Change 2007: Mitigation of Climate Change Contribution
of Working Group III to the Fourth Assessment Report of the Intergovernmental
Panel on Climate Change. Cambridge: Cambridge University Press.
Izrael, Y.A., Ryaboshapko, A.G., Petrov, N.N., 2009. Comparative analysis of geoengineering approaches to climate stabilization. Russian Meteorology and
Hydrology 34 (6), 335347.
Johansson, D.J., Azar, C., 2007. A scenario based analysis of land competition
between food and bioenergy production in the US. Climatic Change 82 (34),
267291.
Kauppi, P.E., Sedjo, R., 2001. Technological and economic potential of options to
enhance, maintain, and manage biological carbon reservoirs and geoengineering. Climate Change 4, 301343.
Kim, M.K., McCarl, B.A., 2009. Uncertainty discounting for land-based
carbon sequestration. Journal of Agricultural and Applied Economics 41 (1),
111.
Kim, M.K., McCarl, B.A., Murray, B.C., 2008. Permanence discounting for landbased carbon sequestration. Ecological Economics 64 (4), 763769.
Kim, S.W., 2011. The effect of transactions costs on GHG emission mitigation for
agriculture and forestry. PhD Dissertation, Texas A&M University.
Kjellstrom, T., Kovats, R.S., Lloyd, S.J., Holt, T., Tol, R.S., 2009. The direct impact
of climate change on regional labor productivity. Archives of Environmental and
Occupational Health 64 (4), 217227.
Klein, R.J., Nicholls, R.J., Mimura, N., 1999. Coastal adaptation to climate change:
Can the IPCC technical guidelines be applied? Mitigation and Adaptation
Strategies for Global Change 4 (34), 239252.
Knutti, R., Sedlcek, J., 2012. Robustness and uncertainties in the new CMIP5
climate model projections. Nature Climate Change 3, 369373.
Konyar, K., Howitt, R.E., 2000. The cost of the Kyoto Protocol to US crop
production: Measuring crop price, regional acreage, welfare, and input
substitution effects. Journal of Agricultural and Resource Economics 347367.
Krankina, O.N., Harmon, M.E., 2006. Forest management strategies for carbon
storage. In: Cloughesy, M. (Ed.), Forests, Carbon, and Climate Change: A
Synthesis of Science Findings. Portland, Oregon, USA: Oregon Forest Resources
Institute, pp. 7992.
Lambi, C.M., Molua, E.L., 2007. The economic impact of climate change on
agriculture in Cameroon. World Bank Policy Research Working Paper Series,
SSRN. Available at: http://ssrn.com/abstract=1016260 (accessed 29.04.14).
Latta, G., Adams, D.M., Alig, R.J., White, E., 2011. Simulated effects of mandatory
versus voluntary participation in private forest carbon offset markets in the United
States. Journal of Forest Economics 17 (2), 127141.
Leakey, A.D., 2009. Rising atmospheric carbon dioxide concentration and the future
of C4 crops for food and fuel. Proceedings of the Royal Society B: Biological
Sciences 276 (1666), 23332343.
Leary, N., 2009. Climate Change and Adaptation. London: Earthscan.
Lee, H.C., McCarl, B.A., Schneider, U.A., Chen, C.C., 2007. Leakage and
comparative advantage implications of agricultural participation in greenhouse
gas emission mitigation. Mitigation and Adaptation Strategies for Global Change
12 (4), 471494.
Long, S.P., Ainsworth, E.A., Leakey, A.D., Nsberger, J., Ort, D.R., 2006. Food for
thought: Lower-than-expected crop yield stimulation with rising CO2
concentrations. Science 312 (5782), 19181921.
Mankiw, N.G., 2007. One answer to global warming: A new tax. The New York
Times, 16 September 2007. Available at: http://www.nytimes.com/2007/09/16/
business/16view.html (accessed 18.12.09).
Mankiw, N.G., 2012. Principles of Economics, sixth ed. Mason: South-Western.
McCarl, B.A., 2007. Adaptation options for agriculture, forestry and sheries. A
Report to the UNFCCC Secretariat Financial and Technical Support Division.
Available at: http://unfccc.int/les/cooperation_and_support/nancial_mechanism/
application/pdf/mccarl.pdf (accessed 29.04.14).
McCarl, B.A., 2011. Vulnerability of Texas agriculture to climate change. In:
Schmandt, J., Clarkson, J., North, G.R. (Eds.), Impact of Global Warming on
Texas, second ed. Texas: University of Texas Press.
McCarl, B.A., 2012. Some thoughts on climate change as an agricultural economic
issue. Journal of Agricultural and Applied Economics 44 (3), 299.
McCarl, B.A., Gowen, M., Schneider, U., Yeats, T., 1999. The Impact of Carbon
Permit Prices on the US Agricultural Sector. Athens, GA: US Environmental
Protection Agency. Prepared for the Climate Policies and Programs Division.
McCarl, B.A., Hurd, B.H., Feng, S.J., et al., 2010. Global climate change and its
impact on agriculture: Challenges for the 21st century. In: Cossia, J. (Ed.),
Global Warming in the 21st Century. New York, NY: Nova Science Publishers
Inc.
McCarl, B.A., Schneider, U.A., 2000. US agriculture's role in a greenhouse gas
emission mitigation world: An economic perspective. Review of Agricultural
economics 22 (1), 134159.
McCarl, B.A., Schneider, U.A., 2001. The cost of greenhouse gas mitigation in US
agriculture and forestry. Science 294 (21), 24812482.
McCarl, B.A., Villavicencio, X., Wu, X., 2008. Climate change and future analysis: Is
stationarity dying? American Journal of Agricultural Economics 90 (5),
12411247.
Mearns, R., Norton, A. (Eds.), 2010. Social Dimensions of Climate Change: Equity
and Vulnerability in a Warming World. Washington, DC: The World Bank.
Mendelsohn, R., Dinar, A., 2003. Climate, water, and agriculture. Land Economics
79 (3), 328341.
Mendelsohn, R., Nordhaus, W., Shaw, D., 1994. The impact of global warming
on agriculture: A Ricardian analysis. American Economic Review 84 (4),
753771.
Michaelowa, A., Jotzo, F., 2005. Transaction costs, institutional rigidities
and the size of the clean development mechanism. Energy Policy 33 (4),
511523.
Moulton, R.J., Richards, K.R., 1990. Costs of sequestering carbon through tree
planting and forest management in the United States. General Technical Report
WO-58. Washington, DC: USDA Forest Service.
Mu, J.E., McCarl, B.A., Wein, A., 2013. Adaptation to climate change: Changes in
farmland use and stocking rate in the U.S. Mitigation and Adaptation Strategies
for Global Change. 18, 713730. Available at: http://link.springer.com/article/
10.1007%2Fs11027-012-9384-4 (accessed 29.04.14).
Murray, B.C., McCarl, B.A., Lee, H.C., 2004. Estimating leakage from forest carbon
sequestration programs. Land Economics 80 (1), 109124.
305
306
Seo, S.N., Mendelsohn, R., Dinar, A., Kurukulasuriya, P., 2009b. Adapting to
climate change mosaically: An analysis of African livestock management by
agro-ecological zones. Berkeley Electronic Journal of Economic Analysis and
Policy 9 (2), 4.
Smith, B., Burton, I., Klein, R.J., Wandel, J., 2000. An anatomy of adaptation to
climate change and variability. Climatic Change 45 (1), 223251.
Smith, P., Martino, D., Cai, Z., et al., 2006. Greenhouse gas mitigation options
in agriculture. Climate Change, Mitigation. Report from Working Group III
(Chapter 8). Washington, DC: Intergovernmental Panel on Climate Change.
Sohngen, B., Mendelsohn, R., 1998. Valuing the impact of large-scale ecological
change in a market: The effect of climate change on US timber. American
Economic Review 686710.
Sohngen, B., Mendelsohn, R., 2003. An optimal control model of forest
carbon sequestration. American Journal of Agricultural Economics 85 (2),
448457.
Sohngen, B., Mendelsohn, R., Sedjo, R., 2001. A global model of climate change
impacts on timber markets. Journal of Agricultural and Resource Economics 26
(2), 326343.
Sderholm, P., Sundqvist, T., 2003. Pricing environmental externalities in the power
sector: Ethical limits and implications for social choice. Ecological Economics 46
(3), 333350.
Sparovek, G., Barretto, A., Berndes, G., Martins, S., Maule, R., 2009. Environmental,
land-use and economic implications of Brazilian sugarcane expansion
19962006. Mitigation and Adaptation Strategies of Global Change 14,
285298.
Speranza, C.I., Kiteme, B., Ambenje, P., Wiesmann, U., Makali, S., 2010. Indigenous
knowledge related to climate variability and change: Insights from droughts in
semi-arid areas of former Makueni District, Kenya. Climate Change 100,
295315.
Spittlehouse, D.L., Stewart, R.B., 2003. Adaptation to climate change in forest
management. British Columbia Journal of Ecosystems and Management 4 (1),
111.
Stavins, R.N., 1999. The costs of carbon sequestration: A revealed-preference
approach. American Economic Review 89 (4), 9941009.
Stavins, R.N., Newell, R., 2000. Climate change and forest sinks: Factors affecting
the costs of carbon sequestration. Journal of Environmental Economics and
Management 40, 211235.
Stern, N.N.H. (Ed.), 2007. The Economics of Climate Change: The Stern Review.
Cambridge: Cambridge University Press.
Tack, J., Harri, A., Coble, K., 2012. More than mean effects: Modeling the effect of
climate on the higher order moments of crop yields. American Journal of
Agricultural Economics 94 (5), 10371054.
Tol, R.S.J., 2014. Climate Economics: The Economics of Climate, Climate Change,
and Climate Policy. Cheltenham: Edward Elgar.
Tubiello, F.N., Donatelli, M., Rosenzweig, C., Stockle, C.O., 2000. Effects of climate
change and elevated CO2 on cropping systems: Model predictions at two italian
locations. European Journal of Agronomy 13 (23), 179189.
Tubiello, F.N., Jagtap, S., Rosenweig, C., Goldberg, R., Jones, J.W., 2002. Effects of
climate change on U.S. crop production: Simulation results using two different
GCM scenarios. Part I: Wheat, potato, corn, and citrus. Climate Research 20 (3),
259270.
United Nations Framework Convention on Climate Change (UNFCCC), 2007.
Investment and Financial Flows Relevant to the Development of an Effective and
Appropriate International Response to Climate Change. Geneva: UNFCCC.
United States Department of Agriculture, Global Change Program Ofce, 1999.
Economic Analysis of U.S. Agriculture and the Kyoto Protocol.
Van Passel, S., Massetti, E., Mendelsohn, R., 2012. A Ricardian Analysis of the
Impact of Climate Change on European Agriculture (No. 83.2012). Italy: Nota di
Lavoro, Fondazione Eni Enrico Mattei. Available at: http://www.feem.it/userles/
attach/201345151394NDL2012-083.pdf (accessed 29.04.14).
Wang, W.W., McCarl, B.A., 2013. Temporal investment in climate change adaptation
and mitigation. Climate Change Economics 4 (2). doi: 10.1142/
S2010007813500097.
Weitzman, M.L., 2007. The stern review on the economics of climate change.
Journal of Economic Literature 45 (3), 703724.
West, T.O., Six, J., 2007. Considering the inuence of sequestration duration and
carbon saturation on estimates of soil carbon capacity. Climatic Change 80,
2541.
Wilson, J., 2006. Using wood to reduce global warming. In: Proceedings: Forests,
Carbon and Climate Change: A Synthesis of Science Findings. Portland, OR:
Oregon Forest Research Institute.
World Bank, 2010. Economics of Adaptation to Climate Change. Washington, DC:
World Bank.
Yu, T., Babcock, B.A., 2010. Are U.S. corn and soybeans becoming more drought
tolerant. American Journal of Agricultural Economics 92 (5), 13101323.
Zhang, Y.W., Hagerman, A.D., McCarl, B.A., 2013. Inuence of climate factors on
spatial distribution of Texas cattle breeds. Climatic Change 118, 113.
Zilberman, D., Zhao, J., Heiman, A., 2012. Adoption versus adaptation with
emphasis on climate change. Annual Review of Resource Economics 4 (1),
2753.
Relevant Websites
http://climatechangeecon.org/
Climate Change Economics.
https://sites.google.com/site/climateconomics/home
Economics of Climate Change.
http://www.ipcc.ch/
IPCC.
http://www.globalchange.gov/
USGCRP.
Glossary
Clone An organism that is an exact genetic copy of
another.
Cryopreservation Maintenance of viable tissues, cells, or
embryos at very low temperature.
Enucleation The process of removing the recipient cell
chromosomes or nucleus.
Epigenetics Heritable changes to DNA and its associated
proteins that control/establish gene expression patterns
without affecting the underlying DNA sequence.
Nuclear reprogramming The process of returning a
differentiated cell nucleus to a totipotent state.
Introduction
Animal Cloning and Nuclear Reprogramming
A clone is an organism that is an exact genetic copy of another.
Many plants and animals in nature utilize cloning as a form of
reproduction. Somatic cell nuclear transfer (SCNT) is a technique that allows the production of cloned animals. With this
technique, the nucleus of a donor cell, containing an animal's
genetic material, is introduced into an enucleated oocyte called
the recipient cytoplast. Embryonic development is then induced and, providing that the right conditions are maintained,
the reconstructed embryo can develop into an individual that
will be genetically identical to the one from which the nuclear
material was derived (Figure 1).
The process by which the somatic cell nucleus is transformed into an embryo is called nuclear reprogramming and
involves changes to the epigenetic mechanisms that control
gene expression and cell differentiation status. Most cells in an
organism contain the same genetic information, which is
stored in their deoxyribonucleic acid (DNA). Epigenetics refers
to heritable changes to DNA and its associated proteins (collectively referred to as chromatin) that control/establish gene
expression patterns without affecting the underlying DNA sequence. As embryonic cells differentiate into different tissues
and cell types, the DNA remains the same, but the cells acquire
different epigenetic modications. The normal development
of an embryo and fetus depends on a precise sequence of
chromatin conguration changes, which are usually related to
methylation of genomic DNA and modications to the histone proteins to which DNA is wrapped around. These epigenetic changes are heritable from cell to cell and are acquired
in a progressive and sequential manner as cells differentiate.
The presence of these epigenetic marks and their ability to be
passed to daughter cells after cell division is a mechanism to
maintain the functional and differentiation status of the cells.
This mechanism explains why when a cell in the skin divides,
its daughter cells continue to be skin cells and do not turn into
neurons or any other cell type. It was thought that development of an embryo to an adult was a unidirectional process
and the differentiation status of a cell, and thus its epigenetic
modications, were xed and irreversible. Cloning using adult
differentiated somatic cells disproved that dogma (Gurdon,
1962; Wilmut et al., 1997), demonstrating the enormous
plasticity of the mammalian epigenome. Successful cloning by
SCNT involves epigenetic reprogramming whereby the gene
expression prole and the epigenetic memory of the differentiated cell is abolished and the new embryo-specic gene
expression and epigenetic prole is established, driving correct
embryonic and fetal development. This includes abrogation of
the expression of approximately 800010 000 genes in the
somatic cell and initiation of the embryonic program with
approximately 10 000 genes (Niemann and Lucas-Hahn,
2012). Failure to reprogram the donor genome is thought to
be the main reason for the low efciency of cloning (Rideout
et al., 2001; Bourc'his et al., 2001; Dean et al., 2001). Thus,
cloning efciency depends on the ability of donor cells to be
totally reprogrammed to an embryonic state and the ability of
the recipient cytoplasm to reprogram the exogenous (i.e.,
donor) nucleus.
The oocyte is one of the few cells that have the ability to
induce the necessary changes to a somatic cell nucleus, so that
embryonic development can proceed to term. This capacity
probably extends from the natural role oocytes have during
normal development. When the oocyte and sperm, two highly
differentiated cells, meet at fertilization in order to generate
a new individual, their genomes must be combined and rendered amenable to embryonic and fetal development.
This process includes extensive and dynamic epigenetic
remodeling.
Historical Perspective
The original idea of generating an animal from a somatic cell
was proposed by Spemann in the early 1900s (Spemann,
1914) as a way to test the developmental potential of a cell's
doi:10.1016/B978-0-444-52512-3.00222-9
307
308
Cytoplast
Metaphase
Oocyte
Enucleation
Donor cell
Nuclear
transfer
Cell culture
Electrofusion
Embryo
In vitro
culture
Embryo
transfer
(recipient)
Fetus
Adult
Cell source
nucleus. However, the required technology to perform Spemann's proposed experiment was not available until the
1950s, when Briggs and King developed nuclear transfer
techniques in amphibians (Rana pipiens), obtaining adult
animals when injecting embryonic cells into enucleated oocytes (Briggs and King, 1952). In 1962, John Gurdon used a
similar technique to produce frogs (Xenopus tropicalis) from
intestinal cells, demonstrating that a somatic cell nucleus has
all the genetic material necessary for development of a complete individual (Gurdon, 1962). Gurdon was awarded the
Nobel Prize for these accomplishments.
In mammals, nuclear transfer technology was developed
several decades later as technological improvements allowed
scientists to work with the smaller mammalian embryos. The
transfer of an embryonic nucleus into an enucleated mouse
zygote (1-cell embryo) was reported by Illmensee and Hoppe
in 1981, resulting in the development of adult animals
(Illmensee and Hoppe, 1981). However, controversy surrounded these results, as other groups were unable to replicate
them. McGrath and Solter (1983) developed a more efcient
technique by which the donor cell was fused with, instead of
being injected into, an enucleated zygote; however, they were
not able to produce offspring when two-cell and older embryos were used as cell donors. In 1986, Willadsen used
sheep mature oocytes as recipient cytoplasts instead of zygotes
and was able to obtain offspring after the transfer of cells
from early stage cleavage embryos (up to a 32-cell embryo)
(Willadsen, 1986). The embryo cloning approach developed
by Willadsen provided the opportunity for producing a limited
number of clones from a single embryo. This technique was
then successfully applied to several species, including cattle
embryos transferred to surrogate mothers result in live offspring; however, since the rst successful attempt, progress has
been made that reects improved technical skills and increasing knowledge of the underlying mechanisms (Niemann
and Lucas-Hahn, 2012). For example, in cattle, efciencies of
2025% of live offspring are not uncommon for experienced
commercial and research laboratories (Panarace et al., 2007;
Kues et al., 2008). In pigs, although the average yield of live
births per embryo transferred is only 35%, by transferring a
large number of embryos per recipient sow, pregnancy rates
can reach 80% with litter sizes averaging 6 cloned piglets;
which, although lower than that of natural breeding (10%),
is a signicant advance.
Interestingly, the in vitro development of SCNT embryos
to the blastocyst stage is similar to that attained by in vitro
fertilization (IVF). Also, after initial embryo transfer, a
similar pregnancy rate was observed between SCNT- and IVFor in vivo-derived bovine embryos (Kuroiwa et al., 2004;
Hill et al., 2000; Heyman et al., 2002). However, high incidences of pregnancy loss occur during the rst trimester
of gestation (Hill et al., 2000; Heyman et al., 2002;
Zakhartchenko et al., 2001). Also, late gestation losses are
higher in SCNT pregnancies as compared with IVF- and in vivoderived pregnancies (Heyman et al., 2002). Fetal and placental
abnormalities are often reported. Finally, high proportions of
cloned offspring die soon after birth or require intensive care.
The losses during gestation and in the early postnatal period
are the main causes for the low overall efciency of cloning by
SCNT.
The majority of clones that survive to 6 months of age
continue to develop normally and do not differ from naturally
conceived animals in terms of blood and urine biochemistry
(Chavatte-Palmer et al., 2002), immune system (Lanza et al.,
2001), and reproductive parameters (Enright et al., 2002)
among others. Also, there is no difference in the composition
of meat and milk from clones of cattle compared with their
naturally produced counterparts of the same age, and similar
results have been reported for cloned pigs (Archer et al., 2003).
Some abnormalities manifested in animals derived from
SCNT include Large Offspring Syndrome, diabetes, pulmonary hypertension, viral infection, dystocia, kidney problems,
leg malformations, pneumonia, heart defects, liver brosis,
osteoporosis, joint defects, anemia, and placental abnormalities (Cibelli et al., 2002). However, all the abnormalities seen
in clones disappeared in the clone's offspring, leading to the
conclusion that the abnormalities must be of epigenetic rather
than genetic origin.
309
Species
References
Sheep
Cow
Goat
Pig
Rabbit
Mule
Horse
310
inherent to current cloning methodologies can lead to abnormal epigenetic proles, which, in turn, may alter meat and/
or milk qualities. Also, animal welfare issues generated by the
current methodologies, related to the increased incidence of
pregnancy complications and need for additional early postnatal care of cloned animals, are of further concern. As these
are reasonable concerns, more studies related to the inuence
of cloning on epigenetic status and the effects on food products derived from cloned animals are required.
Donor cell
The donor cell has a key role in cloning and can be determinant of the success or failure of the procedure. In general,
the efciency of cloning is considered inversely proportional
to the differentiation state of the somatic cell. Adult somatic
cells are usually more difcult to reprogram than fetal cells,
whereas embryonic cells often result in the greatest cloning
efciency. However, there is great variability between
311
312
(a)
(b)
(c)
(f)
(e)
(d)
Figure 2 Traditional nuclear transfer. (a) Oocyte (arrow: DNA stained with Hoechst 33342); (b) Enucleation (arrow: aspirated metaphase plate);
(c) Donor cell inside the transfer micropipette (arrow); (d) Nuclear transfer (arrow: donor cell in perivitelline space); (e) Fusion; and (f) Blastocysts
produced by traditional nuclear transfer.
Hand-made cloning
The cloning technique called HMC (Figure 3) is considered
easier to perform and requires less equipment when compared
with other techniques (Vajta et al., 2005), thus reducing the
initial investment for implementing a cloning program.
For HMC, the ZP of the oocyte is removed by enzymatic
treatment (typically using pronase). Then, zona-free oocytes
are manually bisected using an ultrasharp blade. This step is
typically performed under a low-power stereoscope (2060
magnication) and does not require micromanipulation
equipment. Hemioocytes are then stained with a uorescent
DNA stain (Hoechst 33342), screened for nuclear material
under UV light, and nonnucleated ones selected. For embryo
reconstruction, two nonnucleated hemioocytes (hemicytoplasts) and one donor cell are fused together by electrical
stimulation, achieving approximately 100120% of the original oocyte cytoplasmic volume. Phytohemagglutinin (PHA)
is commonly used to facilitate adherence of hemicytoplasts and
somatic cells. After treatment of hemicytoplasts with PHA, the
somatic cell is glued to the surface of the cytoplast, which
facilitates cell alignment and fusion.
Embryos produced by HMC or any other technology that
involves removal of the ZP need to be cultured individually in
a conical container, in order to prevent embryo aggregation
and cell dispersion, respectively. Normally, HMC embryos are
cultured in microwells using the well-of-the-well (WOW)
system, which consists of small depressions or microwells on
the surface of a plastic embryo culture dish (Vajta et al., 2000).
(a)
(b)
(c)
(e)
(g)
(f)
(h)
(i)
313
(d)
(j)
Figure 3 Handmade cloning. (a) Oocytes; (b) Oocyte without zona pellucida; (c) Handbisected hemioocytes; (d) Hemioocyte without DNA;
(e) Hemioocyte with DNA (arrow indicates DNA this hemioocyte is discarded); (f) Donor cell (arrow) attached to two hemicytoplasts; (g) Fusion;
(h) Reconstructed embryo; (i) Reconstructed embryo (arrow) inside well-of-the-well; and (j) Blastocysts produced by hand-made cloning.
Oocyte Activation
The natural activation of an embryo, and consequently the
beginning of the rst cleavage divisions, are caused by oscillation of intracellular calcium triggered by the sperm. Because
somatic cells do not carry this sperm capacity, articial activation of SCNT embryos is absolutely required. Numerous
procedures have been developed to activate mammalian oocytes (Machaty, 2006). As calcium is a key regulator of oocyte
activation, several approaches to articial oocyte activation
rely on inducing single or repetitive rises in calcium levels. In
livestock, oocyte activation can be achieved through a variety
of protocols (Machaty, 2006). The most prevalent protocols
314
(a)
(b)
(f)
(e)
(c)
(d)
Figure 4 Zonafree nuclear transplantation. (a) Oocytes without ZP; (b) Visualization of oocyte DNA before enucleation; (c) Enucleation (arrows:
PB and metaphase plate inside enucleation mircopipette); (d) Cell transfer (arrow: donor cell attached to cytoplast); (e) Fused reconstructed
embryos; and (f) Reconstructed embryo (arrow) inside WOW.
Conclusion
The ability to produce offspring from cultured somatic cells
allows the rapid propagation of superior genotypes, genetic
improvement of domestic species, the production of biopharmaceuticals and nutraceuticals by cloned animals, organs
for xenotransplantation, genetically engineered animal models
of human diseases, and preservation of endangered species.
Although these applications for SCNT are far reaching, its
broad implementation has been hindered by low efciency.
Although advances in recent decades have allowed improvement in the preimplantation development of cloned
embryos, their full-term developmental potential remains low.
High rates of early pregnancy loss are often observed along
with an increased incidence of abortions in late pregnancy.
Moreover, high mortality rates of offspring from cloned embryos are reported, which makes the overall efciency of SCNT
range between 1 and 5%.
The inefciencies of cloning negatively affect the economic
and commercial viability of SCNT. However, a wealth of
References
Alberio, R., Zakhartchenko, V., Motlik, J., Wolf, E., 2001. Mammalian oocyte
activation: Lessons from the sperm and implications for nuclear transfer.
International Journal of Developmental Biology 45, 797809.
Archer, G.S., Dindot, S., Friend, T.H., et al., 2003. Hierarchical phenotypic
and epigenetic variation in cloned swine. Biology of Reproduction 69,
430436.
Baguisi, A., Behboodi, E., Melican, D.T., et al., 1999. Production of goats by
somatic cell nuclear transfer. Nature Biotechnology 17, 456461.
Berg, D.K., Li, C., Asher, G., Wells, D.N., Oback, B., 2007. Red deer cloned from antler
stem cells and their differentiated progeny. Biology of Reproduction 77, 384394.
Beyhan, Z., Iager, A.E., Cibelli, J.B., 2007. Interspecies nuclear transfer: Implications
for embryonic stem cell biology. Cell Stem Cell 5, 502512.
Bourc'his, D., Le Bourhis, D., Patin, D., et al., 2001. Delayed and incomplete
reprogramming of chromosome methylation patterns in bovine cloned embryos.
Current Biology 11, 15421546.
Brem, G., Khholzer, B., 2002. The recent history of somatic cloning in mammals.
Cloning and Stem Cells 4, 5763.
Briggs, R., King, T., 1952. Transplantation of living nuclei from blastula cells into
enucleated frogs' eggs. Proceedings of the National Academy of Sciences of the
USA 38, 455463.
Campbell, K.H.S., Fisher, P., Chen, W.C., et al., 2007. Somatic cell nuclear transfer:
Past, present and future perspectives. Theriogenology 68, S214S231.
Campbell, K.H.S., McWhir, J., Ritchie, W.A., Wilmut, I., 1996. Sheep cloned by
nuclear transfer from a cultured cell line. Nature 380, 6466.
Chavatte-Palmer, P., Heyman, Y., Richard, C., et al., 2002. Clinical, hormonal, and
hematologic characteristics of bovine calves derived from nuclei from somatic
cells. Biology of Reproduction 66, 15961603.
Chesne, P., Adenot, P.G., Viglietta, C., et al., 2002. Cloned rabbits produced by
nuclear transfer from adult somatic cells. Nature Biotechnology 20, 366369.
Choi, Y.H., Love, C.C., Chung, Y.G., et al., 2002. Production of nuclear transfer
horse embryos by Piezo-driven injection of somatic cell nuclei and activation
with stallion sperm cytosolic extract. Biology of Reproduction 67, 561567.
Cibelli, J.B., Campbell, K.H., Seidel, G.E., West, M.D., Lanza, R.P., 2002. The health
prole of cloned animals. Nature Biotechnology 20, 1314.
Cibelli, J.B., Stice, S.L., Golueke, P.J., et al., 1998. Cloned transgenic calves
produced from nonquiescent fetal broblasts. Science 280, 12561258.
Dean, W., Santos, F., Stojkovic, M., et al., 2001. Conservation of methylation
reprogramming in mammalian development: Aberrant reprogramming in cloned
embryos. Proceedings of the National Academy of Sciences of the USA 98,
1373413738.
315
Du, F., Xu, J., Zhang, J., et al., 2009. Benecial effect of young oocytes for rabbit
somatic cell nuclear transfer. Cloning and Stem Cells 11, 131140.
Enright, B.P., Taneja, M., Schreiber, D., et al., 2002. Reproductive characteristics of
cloned heifers derived from adult somatic cells. Biology of Reproduction 66,
291296.
European Food Safety Authority - EFSA, 2010. Statement of EFSA. Update on the
state of play of animal cloning. EFSA Journal 8, 121.
European Food Safety Authority - EFSA, 2012. Scientic opinion. Guidance on the
risk assessment of food and feed from genetically modied animals and on
animal health and welfare aspects. EFSA Journal 10, 143.
Fissore, R.A., Robl, J.M., 1994. Mechanism of calcium oscillations in fertilized
rabbit eggs. Developmental Biology 166, 634642.
Folch, J., Cocero, M.J., Chesne, P., et al., 2009. First birth of an animal from an
extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71,
10261034.
Food and Drug Administration FDA, 2008. Guidance for industry. Use of animal
clones and clone progeny for human food and animal feed. Available at: http://
www.fda.gov/AnimalVeterinary/SafetyHealth/AnimalCloning/default.htm (accessed
15.01.08).
Fox, J.L., 2008. Cloned animals deemed safe to eat, but labelling issues loom.
Nature Biotechnology 26, 249250.
Galli, C., Lagutina, I., Crotti, G., et al., 2003. Pregnancy: A cloned horse born to its
dam twin. Nature 424, 635.
Gandhi, A.P., Lane, M., Gardner, D.K., Krisher, R.L., 2000. A single medium
supports development of bovine embryos throughout maturation, fertilization and
culture. Human Reproduction 15, 395401.
Gao, S., Chung, Y.G., Parseghian, M.H., et al., 2004. Rapid H1 linker histone
modications following fertilization or somatic cell nuclear transfer: Evidence
for a uniform developmental program in mice. Developmental Biology 266,
6275.
Gomez, M.C., Pope, C.E., Giraldo, A., et al., 2004. Birth of African Wildcat cloned
kittens born from domestic cats. Cloning and Stem Cells 6, 247258.
Gurdon, J.B., 1962. The developmental capacity of nuclei taken from intestinal
epithelium cells of feeding tadpoles. Journal of Embryology and Experimental
Morphology 10, 622640.
Heyman, Y., Chavatte-Palmer, P., Lebourhis, D., et al., 2002. Frequency and
occurrence of late-gestation losses from cattle cloned embryos. Biology of
Reproduction 66, 613.
Hill, J.R., Burghardt, R.C., Jones, K., et al., 2000. Evidence for placental abnormality
as the major cause of mortality in rst-trimester somatic cell cloned bovine
fetuses. Biology of Reproduction 63, 17871794.
Illmensee, K., Hoppe, P.C., 1981. Nuclear transplantation in Mus musculus:
Developmental potential of nuclei from preimplantation embryos. Cell 23, 918.
Janssen, D.L., Edwards, M.L., Koster, J.A., Lanza, R.P., Ryder, O.A., 2004. Postnatal
management of cryptorchid banteng calves cloned by nuclear transfer utilizing
frozen broblast cultures and enucleated cow ova. Reproduction Fertility and
Development 6, 206.
Jiang, Y., Kelly, R., Peters, A., et al., 2011. Interspecies somatic cell nuclear transfer
is dependent on compatible mitochondrial DNA and reprogramming factors. Plos
One 4 (6), e14805.
Kim, M.K., Jang, G., Oh, H.J., et al., 2007. Endangered wolves cloned from adult
somatic cells. Cloning and Stem Cells 9, 130137.
Kono, T., Tsunoda, Y., Nakahara, T., 1991. Production of identical twin and triplet
mice by nuclear transplantation. Journal of Experimental Zoology 257, 214219.
Kues, W.A., Rath, D., Niemann, H., 2008. Reproductive biotechnology in farm
animals goes genomics. CAB Reviews 3, 118.
Kuroiwa, Y., Kasinathan, P., Matsushita, H., et al., 2004. Sequential targeting of the
genes encoding immunoglobulin-[mu] and prion protein in cattle. Nature
Genetics 36, 775780.
Lai, L., Kolber-Simonds, D., Park, K.W., et al., 2002. Production of alpha-1,3galactosyltransferase knockout pigs by nuclear transfer cloning. Science 295,
10891092.
Lanza, R.P., Cibelli, J.B., Diaz, F., et al., 2000. Cloning of an endangered species
(Bos gaurus) using interspecies nuclear transfer. Cloning 2, 7990.
Lanza, R.P., Cibelli, J.B., Faber, D., et al., 2001. Cloned cattle can be healthy and
normal. Science 294, 18931894.
Lee, B.C., Kim, M.K., Jang, G., et al., 2005. Dogs cloned from adult somatic cells.
Nature 436, 641.
Li, Z., Sun, X., Chen, J., et al., 2006. Cloned ferrets produced by somatic cell
nuclear transfer. Developmental Biology 293, 439448.
Loi, P., Ptak, G., Barboni, B., et al., 2001. Genetic rescue of an endangered mammal
by cross-species nuclear transfer using post-mortem somatic cells. Nature
Biotechnology 19, 962964.
316
Machaty, Z., 2006. Activation of oocytes after nuclear transfer. Methods in Molecular
Biology 348, 4358.
McCreath, K.J., Howcroft, J., Campbell, K.H., et al., 2000. Production of genetargeted sheep by nuclear transfer from cultured somatic cells. Nature 405,
10661069.
McGrath, J., Solter, D., 1983. Nuclear transplantation in mouse embryos. Journal of
Experimental Zoology 228, 355362.
Meng, L., Ely, J.J., Stouffer, R.L., Wolf, D.P., 1997. Rhesus monkeys produced by
nuclear transfer. Biology of Reproduction 57, 454459.
Miyoshi, K., Rzucidlo, S.J., Pratt, S.L., Stice, S.L., 2003. Improvements in cloning
efciencies may be possible by increasing uniformity in recipient oocytes and
donor cells. Biology of Reproduction 68, 10791086.
Nagashima, H., Matsunari, H., Nakano, K., et al., 2012. Advancing pig cloning
technologies towards application in regenerative medicine. Reproduction in
Domestic Animals 47 (Suppl. 4), 120126.
Nakada, K., Mizuno, J., 1998. Intracellular calcium responses in bovine oocytes
induced by spermatozoa and by reagents. Theriogenology 50, 269282.
Niemann, H., Lucas-Hahn, A., 2012. Somatic cell nuclear transfer cloning: Practical
applications and current legislation. Reproduction in Domestic Animals 47
(Suppl. 5), 210.
Oback, B., Wiersema, A.T., Gaynor, P., et al., 2003. Cloned cattle derived from a novel
zona-free embryo reconstruction system. Cloning and Stem Cells 5 (1), 312.
Onishi, A., Iwamoto, M., Akita, T., et al., 2000. Pig cloning by microinjection of fetal
broblast nuclei. Science 289, 11881190.
Panarace, M., Aguero, J.I., Garrote, M., et al., 2007. How healthy are clones and
their progeny: 5 years of eld experience. Theriogenology 67, 142151.
Petersen, B., Lucas-Hahn, A., Oropeza, M., et al., 2008. Development and
validation of a highly efcient protocol of porcine somatic cloning using
preovulatory embryo transfer in peripubertal gilts. Cloning and Stem Cells 10,
355362.
Polejaeva, I.A., Chen, S.H., Vaught, T.D., et al., 2000. Cloned pigs produced by
nuclear transfer from adult somatic cells. Nature 407, 8690.
Prather, R.S., Barnes, F.L., Sims, M.M., et al., 1987. Nuclear transplantation in the
bovine embryo: Assessment of donor nuclei and recipient oocyte. Biology of
Reproduction 37, 859866.
Prather, R.S., Sims, M.M., First, N.L., 1989. Nuclear transplantation in early pig
embryos. Biology of Reproduction 41, 414418.
Rideout, W.M., Eggan, K., Jaenisch, R., 2001. Nuclear cloning and epigenetic
reprogramming of the genome. Science 293, 10931098.
Rudenko, L., Matheson, J.C., Sundlof, S.F., 2007. Animal cloning and the FDA The
risk assessment paradigm under public scrutiny. Nature Biotechnology 25, 3943.
Shi, D., Lu, F., Wei, Y., et al., 2007. Buffalos (Bubalus bubalis) cloned by nuclear
transfer of somatic cells. Biology of Reproduction 77, 285291.
Shin, T., Kraemer, D., Pryor, J., et al., 2002. A cat cloned by nuclear
transplantation. Nature 415, 859.
Spemann, H., 1914. U ber verzogerte Kernversorgung von Keimteilen. Verhandlungen
der Deutschen Zoologischen Gesellschaft 24, 216221.
Stice, S.L., Roblm, J.M., 1988. Nuclear reprogramming in nuclear transplant rabbit
embryos. Biology of Reproduction 39, 657664.
Susko-Parrish, J.L., Leibfried-Rutledge, M.L., Northey, D.L., Schutzkus, V., First, N.L.,
1994. Inhibition of protein kinases after an induced calcium transient causes
Relevant Websites
http://www.bio.org/articles/frequently-asked-questions-about-animal-cloning
Biotechnology Industry.
http://www.clonesafety.org/
CloneSafety.
http://www.fda.gov/animalveterinary/safetyhealth/AnimalCloning/default.htm
FDA.
http://animalscience.ucdavis.edu/animalbiotech/Biotechnology/Cloning/index.htm
University of California, Davis.
http://learn.genetics.utah.edu/content/tech/cloning/
University of Utah.
Glossary
Acclimatization The process of hardening or conditioning
micropropagated plants so that they will survive in the
greenhouse or eld.
Adult plant A plant that is physiologically mature enough
to ower under normal inductive conditions. Compare with
juvenile plant.
Adventitious bud, root, or shoot An organ that forms at
an unexpected location, such as roots on a stem or leaf, or
shoots on a root or leaf.
Callus Unorganized group of cells that forms on plant
parts or explants as a result of wounding or application of
plant growth regulators, such as auxins and cytokinins.
Clone A population of organisms (plants) that is asexually
derived and can be traced back to an original individual.
Dedifferentiation When differentiated (specialized) cells
return to the meristematic condition often to replace a
missing or wounded part, such as a root or shoot. This is a
typical wound healing response for plants, and is utilized in
vegetative plant propagation, such as rooting cuttings and
microcuttings, grafting, and other vegetative propagation
techniques.
Differentiation When cells become more specialized than
the meristematic condition. Meristematic cells have one
function: division (mitosis). All other cell types differentiate
from cells produced in meristems via cell division.
Embryogenesis Formation of embryo-like structures
in vitro or in planta, derived directly from explant cells or
indirectly from callus cells.
Ex vitro The environment outside of the vessels containing
plant tissue cultures. Typically the greenhouse and eld are
referred to as ex vitro environments for micropropagated
plants.
Explant The plant tissue or organ that is removed from the
stock plant and is rst placed in vitro during the
Introduction
In 1902, Gottlieb Haberlandt broached the subject of plant
tissue culture and micropropagation in his seminal publication
(Haberlandt, 1902) in which he endeavored to explore totipotency and morphogenesis in plants. His efforts were largely
unsuccessful, primarily related to a lack of knowledge about the
requisite medium components. Subsequently, plant scientists
vigorously pursued denition of conditions necessary to successfully produce viable cell, tissue, and organ cultures (Read,
1992). In the more than a century that has elapsed, there have
been thousands of reports related to attempts to rene media,
environmental conditions (both in vitro and ex vitro), and other
parameters conducive to successful in vitro culture resulting in
doi:10.1016/B978-0-444-52512-3.00224-2
317
318
preponderance of medium formulations used for micropropagation research and commercial multiplication of elite
clones of a myriad of plant species are based on the MS
medium.
It would be nearly impossible to list all of the researchers
and plant species and genotypes that have been reported since
the Murashige review, but a few of the classic examples should
be noted. Ball's work with sterile cultures reported in 1946
helped lay the foundation for the work that followed (Ball,
1946), including that already noted for Murashige, Skoog,
Miller, and Morel. Nitsch and Nitsch were contemporaries
who conducted numerous tissue culture experiments and
provided other medium formulations employed in later research (Nitsch and Nitsch, 1956). They even reported on
ower induction of Plumbago stem segments cultured in vitro
(Nitsch and Nitsch, 1967). Reinert's work with embryogenesis
(Reinert, 1959; Reinert and Mohr, 1967; Reinert et al., 1967)
and that of Steward (Steward et al., 1958) contributed greatly
to the elds of embryogenesis, suspension culture, and medium composition. Many other researchers also worked with
cell suspensions, liquid culture, and medium constituents
named after them when used in later research, for example,
Gamborg's Medium (Gamborg et al., 1968; Vasil et al., 1964;
Norstog, 1965).
As research with plant tissue cultures progressed, especially
with callus suspension and embryogenic cultures, it became
clear that aberrations would frequently occur. The resulting
plants often would be different genetically and phenotypically
from the plant from which the explant was taken. This was
readily apparent when asparagus Asparagus ofcinalis, tobacco
Nicotiana tabacum, carnation Dianthus caryophyllus, and other
plants were regenerated from callus or cell suspension cultures
(Wilmar and Hellendoorn, 1968; Murashige and Nakano,
1966). Sometimes such changes could be advantageous, for
example, changes in scented geranium (Skirvin and Janick,
1976). Shepard et al. (1980) demonstrated wide-ranging variability in Russett Burbank potato regenerated from leaf
protoplasts. Larkin and Skowcroft (1981) coined the term
somaclonal variation and espoused the value of somaclonal
variation for plant improvement. Likewise, Cocking's (Cocking,
1960) demonstration of the potential of culturing plant
protoplasts has also exhibited promise for plant regeneration,
parasexual hybridization, and plant improvement, but also will
not be addressed in this article. Later, Grosser (1994) described
methodology for protoplast isolation and somatic hybridization in citrus, also with encouraging results. Murashige
(1974) commented that off-type plants commonly occur when
plants are adventitiously regenerated from callus and stated
The frequency of genetically aberrant plants can be reduced
considerably, even avoided entirely, if the plant multiplication
can be achieved through an enhancement of axillary shoot
formation. The authors therefore have chosen to restrict our
discussion to use of techniques that to a high degree retain the
genetic and phenotypic identity of the plant being cloned via
micropropagation.
Murashige's review suggested three stages of micropropagation: Stage I, Establishment of the aseptic culture,
Stage II, Multiplication of propagule, and Stage III, Preparation
for re-establishment of plants in soil (Murashige, 1974).
Subsequently, general micropropagation practice, both for
Explant Selection
Many researchers have shown that explants taken from
juvenile stock plants or from juvenile parts of the stock plant
perform better in vitro; this response is similar to the better
rooting of cuttings taken from juvenile plants when compared
with cuttings from mature plants such as Hedera helix (Hackett,
1983). Sources of juvenile material are depicted schematically
by Preece (2008) in which he notes the cone of juvenility,
epicormic shoots, stump sprouts, and root suckers, among
others. Similarly, it has been demonstrated that explants
secured from tissue culture-derived stock plants frequently
respond better in vitro than explants taken from greenhouse
or eld-grown stock plants. This was shown for azalea
(Economou and Read, 1986) and strawberry (Liu and Sanford,
1988). Furthermore, when location on the stock plant is
considered, for example, apical bud versus lateral bud, the best
results vary with species: lateral buds were superior for
deciduous azalea (Economou and Read, 1986), but apical
explants responded better for Fagus sylvatica (Vanderschaege
and Debergh, 1988). Genotypic differences have been widely
reported to lead to varying in vitro performance, for example,
Pelargonium shoot tips and organogenesis in sweet potato
(Pillai and Hildebrandt, 1968a,b; Gunckel et al., 1972). With a
relatively easy to micropropagate species such as petunia,
shoot-forming ability from leaf segment explants varied by as
much as vefold, depending on cultivar (Read, 1990).
319
320
Shoot Forcing
Forcing solutions
Woody plant tissue culture has often proved to be difcult,
primarily because cells or tissues of woody plants are cellulosic
and lignied. As a result, the period of time when soft, nonlignied shoots can be obtained often is limited to a brief
period in the spring when the rst ush of growth occurs.
Employing a solution such as those used commercially for
extending the keeping quality and longevity of cut owers,
such as roses, chrysanthemums, and carnations, has enabled
relatively clean, soft tissue to be obtained for explant use. The
solution used mimics the one used for cut owers: 58.4 mM
sucrose (2% solution) and 592 mM 8-hydroxyquinoline citrate
(200 ppm). Woody stems are cut from the stock plants and the
cut bases placed into vessels containing the forcing solution
(Figure 1). A fresh cut is made to remove 12 mm from the
base of the stem and the solution replaced every 23 days.
Delivery of plant growth-regulating chemicals via the xylem
uptake from the forcing solution may be accomplished by
inclusion in the forcing solution (Read et al., 1984, 1986).
Buds from dormant woody stems have been stimulated to
emerge and elongate in spite of an endodormant condition by
Serial grafting
Stems of a number of woody species have been rejuvenated
by repeatedly grafting mature stems onto juvenile rootstocks.
The process often needs to be repeated several times,
depending on species/genotype, in order for juvenility to be reestablished (Debergh and Maene, 1985; Bonga and Von
Aderkas, 1992). Franclet (1987) and Boulay (1987) have
reported extensively on this process, especially with conifers.
Using small shoot tips as scions enhanced rejuvenation in avocado when conducted in vitro (Pliego-Alfaro and
Murashige, 1987) and was studied for juvenile and mature
clones of Sequoiadendron giganteum by Monteuius et al. (1987).
Stage I: Establishment
The primary objective of Stage I is to successfully introduce
the explant onto the medium by using clean explants and
aseptic techniques (Figure 2). Because the objective of
micropropagation is to produce a population of uniform
genotype (cloning, asexual propagation), this article focuses
on use of existing meristems. Although much research has
(a)
(b)
(c)
(d)
321
Figure 1 (a) and (b) Shoot forcing technology. (a) Cut woody stems of grape (Vitis spp.) with bases immersed in forcing solution and buds
beginning growth. (b) Shoots elongated sufciently to be excised for use as explants for micropropagation. (c) New recently emerged red
epicormic shoots being forced on a 4 cm diameter walnut stem segment. (d) 25 cm long forced shoots ready to be excised for use as explants
for micropropagation.
Explant Disinfestation
Nearly all reports regarding culture establishment initially
describe the disinfestation technique, which employs a
chemical treatment to kill organisms on the surface of the
explant. Bacterial cells, fungal spores, and some arachnid or
small insect pests may inhabit the explant surface and when
the explant is placed on the culture medium these contaminants can multiply and destroy the explant. The most
common disinfestant procedure employed is soaking the
explants in bleach (sodium or calcium hypochlorite solutions), a potent oxidative agent that in optimal concentrations and durations will kill the undesirable organisms. A
wetting solution such as Tween 20 usually is added to the
bleach solution. This will aid in good surface contact and
improved kill of unwanted organisms. The bleach soak is
Medium Disinfestation
The most common method to sterilize the medium is the use
of an autoclave to provide heat treatment under pressure. A
typical treatment is 121 C for 2030 min. Times may vary
and when using a new autoclave one or more test runs is
322
(a)
(b)
(c)
Figure 2 (a) Green, leafy walnut shoot harvested for micropropagation explants. The leaves are removed, as in (c) and surface disinfested.
Following disinfestation and rinsing in sterile water, the shoot is cut into nodal and apical explants (b). (c) Hibiscus nodal explants with new
growth, toward the end of Stage I.
recommended. In recent years, especially for small-scale research or commercial operations, the use of a microwave oven
is an inexpensive alternative to an autoclave (Tisserat et al.,
1992).
Medium Gelling
Choice of gelling agent or use of liquid medium can have an
impact on the success of the micropropagation process.
Debergh (1983) compared seven different brands of agar at
ve different concentrations for gelling Murashige and Skoog
(1962) medium when micropropagating Cynara scolymus and
Oreopanax nymphaeifolia. He found numerous differences in gel
strength and chemical characteristics of the medium with
differences in a defect referred to as hyperhydricity, and related
to cytokinin and water availability. Agar gel strength was related to water availability, with a more rm gel providing less
water availability and therefore less hyperhydricity. Working
with more dened agar sources and agar alternatives Wetzstein
et al. (1994) observed that gel strength was inuenced by
gelling agent and by choice of medium. Woody Plant Medium
(WPM) and Gamborg B5 (GB) was generally more rm than
MS, Gel-gro had greater gel strength than either agar tested,
and autoclaving caused a decrease in pH of all media. Like
Debergh, they emphasized the importance of medium choice,
gelling agent, and sterilization protocols. Use of agitated liquid
medium was employed by Morel (1964) and Preece (2010) has
shown that large shoot masses can be micropropagated
successfully in shallow stationary liquid medium (Figure 3(c)).
It is important to use agars of high purity for plant tissue
culture. Gelcarin gums are also widely used in micropropagation. They create a gelled clear medium compared with the
gelled cloudy medium with agar. Gelcarin gums may result in
better shoot growth in vitro, but hyperhydricity can be a
problem. To solve this, a mixture of half strength agar with
some gelcarin gum results in low hyperhydricity and good
shoot growth.
Medium Composition
It is acknowledged that the culture medium must provide
adequate nutrition and an energy source because unlike an
intact plant, the explant generally cannot adequately produce
its needs. A typical micropropagation medium contains both
inorganic macro- and micronutrients; an energy source, usually sucrose, although other sugars and complex carbohydrates
are sometimes employed; organic chemicals such as vitamins,
amino acids, and hormone-like plant growth regulators, such
as auxins, cytokinins, gibberellins, and occasionally others. In
some medium formulations complex substances are included
such as coconut water (liquid endosperm), tomato juice, and
purees of other fruits and vegetables. A comparison of several
commonly used media is presented in Hartmann et al. (2011).
Nas and Read (2004) developed a medium based on the
chemical composition of hazelnut (Corylus spp.) kernels,
making the assumption that nourishment of explants in vitro
could be consistent with the nutritional needs of the developing embryo in situ during germination. They also presented a comparison of the constituents of the Nas and Read
medium with MS and other media.
(a)
(c)
323
(b)
(d)
Figure 3 Stage II cultures. (a) Stage II walnut microshoots subdivided into nodal segments with axillary buds that elongate into microshoots (b)
that can be further subdivided into nodal segments as in (a), or recut and placed on rooting medium or rooted ex vitro. (c) Hibiscus axillary shoot
proliferation on stationary liquid medium. (d) Growth room for Stage II cultures.
Culture Environment
A clean room for aseptic transfer and subsequent growth
of the explants (Figure 3) is essential to the success of any
micropropagation enterprise. Light level (photon ux), photoperiod, and light quality are all important, particularly when
green leafy explants are used. In some cases, absence of light is
preferred, as in the case of Anthurium andreanum (Pierik et al.,
1979), and Miller and Murashige (1976) showed that tropical
foliage species which often are jungle understory species
beneted from culture under relatively low light. However,
many researchers have reported that higher light levels promote
shoot growth and more photosynthetic activity by green explants (Werckmeister, 1971; Pennazio and Radol, 1973;
Hasegawa et al., 1973). Reported optimum photon ux levels
are varied, but many fall into a range of 7080 mmol m2 s1
(Hutchinson, 1984; Economou, 1982; Villalobos et al., 1984).
Optimum light levels vary with the species, and the literature
should be consulted when beginning with any new species.
When considering photoperiod, species that are physiologically responsive in nature, i.e., owering under short days
(SD, chrysanthemum) or long days (LD, carnation) and
tuberization (SD, dahlia), will likely respond similarly in vitro.
However, in most cases of such morphological responses, for
example, owering in chrysanthemum, the response is undesirable for in vitro culture because such responses will be
competitive with the desired goal of micropropagation. Typically microcultures are incubated under 16 h photoperiods.
This is especially necessary with woody species to keep them
from going dormant.
Light quality, as mentioned earlier regarding stock plants,
can likewise inuence endogenous hormone levels and thus
affect in vitro performance. If there is a predominance of red
light, it may increase endogenous cytokinin levels and enhance
324
Temperature in Micropropagation
As is true for intact plants, temperature governs numerous
processes and plant growth in general. Within limits, growth
and development increase with rising temperature. Culture
temperatures in the range of 2027 C are commonly used.
When considering appropriate culture temperatures, the natural habitat of the species to be cultured should be considered,
for example, 3239 C for species of tropical origin.
Culture Atmosphere
The atmospheric constituents in the culture room and in the
culture vessel could logically have a profound impact on explant responses in vitro. Generally, little research has been
done on the culture room atmosphere, but humidity, carbon
dioxide, oxygen, and ethylene levels have been investigated.
Typically the gaseous atmosphere inside the culture vessel is
90% relative humidity or higher. This high humidity presents a
problem for acclimatization, which is addressed under Stage
IV in this article. Maximum relative humidities are highest for
liquid cultures and those that employ low levels of gelling
agents; high concentrations of agar, for example, approximately 1.0%, create a stiffer medium and lower relative humidity (Debergh et al., 1981; Figure 5).
Carbon dioxide levels in the culture atmosphere can inuence photosynthesis for green leafy explants. Reuther (1987)
demonstrated advantages for CO2 enrichment of grape, Spathiphyllum, and African violet micropropagation. Researchers
have pursued autotrophic culture to enhance micropropagation
efciency (see Stage IV, Kozai (1991)) and the addition of CO2
to combat the detrimental inuence of ethylene buildup in the
culture (Van der Plas and Wagner, 1986).
Ethylene inhibition of explant growth and organogenesis is
an important consideration, because it is clear that cultures that
contain auxin in the medium and contain living tissue (explants) can produce ethylene. When ethylene builds up in sealed
vessels, it can inhibit and even kill the plant material being
cultured. Gavinlertvatana et al. (1979) reported growth suppression of petunia and dahlia and Mingo-Castel et al. (1976)
showed that ethylene inhibited tuber formation in etiolated
potato sprouts, but elevated CO2 levels stimulated tuberization.
The negative effects of ethylene have been counteracted by the
treatment of explants with silver nitrate or cobalt chloride, but
scrubbing ethylene from the vessel atmosphere with potassium
permanganate had little effect on ethylene-induced growth
suppression. Economou (1991) has reviewed the positive and
negative effects of ethylene on in vitro cultures.
Because oxygen is required for respiration of all living cells,
it would seem obvious that oxygen levels could be important
for micropropagation. Agitation of liquid cultures aerates the
medium when propagating orchid meristems, for example.
Stationary liquid medium can be used if it is sufciently
Meristem Culture
The apical meristem area is often free from pathogens, including viruses, because vascular differentiation occurs in
daughter cells that differentiate from meristematic cell divisions, not in the cells in and immediately around the apical
meristem (Preece, 2003). Because it is difcult to excise only
the meristem, young leaf primordia are also included, making
the explants micro shoot tips, typically 0.40.5 mm in diameter. Micro shoot tips are widely used to escape viruses in
perennial, clonally propagated crops. Frequently stock plants
or cultures also receive thermotherapy as a further measure to
produce plants free from important pathogens.
Morel (1960) used this technique to produce virus-free
orchids. In practice, the process involves starting with an elite
plant that usually receives heat treatment, from which the
meristem tip is excised and used as the explant. Following
culture, possibly several re-cultures of the micro shoot tip,
resulting shoots and plants are tested for freedom from those
pathogens that can be detected. This latter step may involve
indexing for viruses, bacteria, or other diseases. It is standard
practice to obtain specic pathogen-tested stock plants for a
wide variety of asexually propagated crops, including potato,
banana, pome fruits, several citrus species, chrysanthemum,
and many others (Klopmeyer, 2000). An interesting example is
the use of meristem cultures for the elimination of Pierce's
disease in Muscadine grape, Vitis rotundifolia (Robacker and
Chang, 1992). For a review of the process of escaping pathogens using this technique, see Sangwan et al. (1987) and
Miloevi et al. (2012).
(a)
325
(b)
(c)
(d)
Figure 4 (a) Walnut microshoots that have been cultured in darkness to etiolate the shoots to enhance adventitious root initiation. (b) and (c)
In vitro rooted microshoots of trifoliate orange ready to transplant to ats ultimately to be used as clonal rootstocks for citrus. (d) In vitro rooted
microshoot of cherry, ready for transplanting into greenhouse growing medium.
herbaceous and woody plants are now routinely micropropagated, among many, including the following:
Herbaceous/ornamentals:
Aechmea Cueva et al. (2006)
Gardenia Hatzilazarou et al. (2006)
Philodendron Jmbor-Benczr and Mrta-Riffer (1990)
Pulmonaria Stimart et al. (1998)
Tillandsia Cueva et al. (2006)
Woody ornamentals:
Acanthopanax Yang and Read (1997)
Acer Preece et al. (1991a,b)
Berberis Uno and Preece (1987)
Cercis (red bud) Figure 8
Hibiscus Air et al. (2009, Figures 2 and 3)
326
Fruits:
Citrus Figure 4
Malus (apple) Zimmerman (1984)
Olea Leva (2011)
Passiora Faria and Segura (1997)
Prunus Figures 4 and 6
Rubus Figure 7
Vaccinium Grout and Read (1986)
Vitis Gago et al. (2009, Figure 1)
Nut crops:
Castanea Yang et al. (1986)
Corylus Nas and Read (2001)
Juglans Leslie et al. (2010, Figures 14)
Pistachia Benmahioul et al. (2012)
Medicinals and herbs
Allium Mohamed-Yasseen et al. (1993)
Balanites Gour et al. (2007)
Hypericum Karppinen et al. (2006)
Rosemarinus Tawk et al. (1992)
Satureja Arrebola et al. (1997)
At times, the available plant material may be limiting,
leading researchers to be concerned about reliability of their
investigations and commercial propagators to question new
protocols. One approach to addressing this problem has been
the studies of Nas et al., (2005) in which experimental designs
were tested when there was a limited amount of potential
explant material. They employed two designs that they proved
to be effective when explant material is limited, Plackett
Burman Design (PBD) and fractional factorial design (FFD).
Although limiting information on treatment interactions when
PBD or FFD are used, their results indicated that several factors
could be tested when explant material is limited and would
facilitate prioritizing the most important factors. Subsequently
these results can provide guidance when sufcient numbers of
explants become available for larger experiments.
327
328
Humidity Control
A primary challenge with establishing microplants in the
ambient environment is the change in relative humidity.
The in vitro environment is typically 100% relative humidity
(a)
(b)
(c)
(d)
329
Figure 6 (a) and (b) In vitro rooted micropropagated cherry plantlets ready for transplanting into a sphagnum peat greenhouse medium before
placement under high relative humidity for acclimatization. (c) The cherry plantlets being planted as the rst step in greenhouse acclimatization.
(d) Walnut plantlets being planted in a at before being placed under high relative humidity in a greenhouse.
acclimatization, the rst new leaves that form are thin and
similar to in vitro leaves; however, as new leaves develop,
they gradually become more like normal leaves that grow on
plants in the greenhouse or eld. Initially the new leaves
that form during acclimatization have tightly packed palisade cells, indicating a transition to higher light and lower
relative humidity.
In vitro rooting is often in vessels with ventilated lids
(Figure 5), which can lower humidity and begin the transition
of microplants to the ex vitro environment. For example, ventilation caused lower water content, which thus increased
epicuticular waxes on the leaf surfaces, and resulted in a higher
resistance to water loss on jojoba propagules (Mills et al.,
2001), which all contribute to acclimatization success.
If ventilated lids still maintain a high relative humidity,
loosening, tilting open, and removing lids of culture vessels
following in vitro rooting but before transplanting will help
prepare microplants for the ambient environment. With desert
date (Balanites aegyptiaca) it was necessary to gradually unscrew
lids of culture vessels before transplanting into vermiculite to
330
(a)
(b)
(d)
(c)
(e)
Figure 7 Rooting and root development on clonal microplants immediately following acclimatization. (a) and (b) Walnut plantlet being
acclimatized and showing root development through a peat pot containing a sphagnum peat-based container (a) or in a similar medium removed
from a plastic container. (c) Blackberry plantlet showing root development along the outside of the sleeve containing a similar peat-based medium.
(d) and (e) Root development on clonal walnut rootstock micropropagated plants after acclimatization and removal of the growing medium.
(a)
(b)
(c)
(d)
331
Figure 8 Acclimatization areas. (a) Clonal walnut rootstock plants being acclimatized within a clear plastic tent. (b) Forest Pansy Red Bud
(foreground) and blackberry plants during acclimatization under a white plastic humidity tent with evenly spaced overhead mist nozzles. (c) and (d)
Walnut microplants being acclimatized in a greenhouse with a fog system lling the greenhouse with humidity in (d).
Shading
Substrates
332
Conclusion
Clonal micropropagation is an important component of the
propagation, nursery, and orchard industries. This technology
has allowed the Oregon hazelnut industry to abandon grafting
and transplant micropropagated trees growing on their own
roots. The California walnut industry has, for the rst time,
clonal rootstocks available only because of micropropagation.
Walnut cuttings root poorly and not at commercially viable
rates.
The micropropagation industry is having an economic
impact on companies that sell the supplies and equipment, the
trucking and transportation industry, the nursery industry, the
forestry industry, the landscape industry, and others. Commercial companies would not devote their resources to purchase micropropagated plants unless there were sufcient
demand for the product. Clearly, there is a place for micropropagation and although micropropagation will never replace grafting, layering, and rooting cuttings, it is an important
component of the commercial propagation industry.
Whether grown commercially, for research, or personal
pleasure, all clonal micropropagation follows the same basic
pathway through the stages of micropropagation. Because axillary shoot proliferation is important, initial explants must
include nodes. Axillary buds are induced to grow from the
nodes, and when desired, excised, rooted, and acclimatized.
Care must be exercised to avoid adventitious shoots and
only axillary shoots should be produced to ensure clonal delity. Adventitious shoots can show a tendency to exhibit
somaclonal variation and the resulting plants may not be trueto-type. Commercial laboratories have failed because of selling
plants derived via adventitious shoot organogenesis. The lack
of uniformity among the plants disappointed customers, who
did not make additional purchases.
Clones that establish, proliferate shoots, root, and acclimatize successfully are the easiest for meeting customer demand and the most cost effective to produce. Genotypes that
offer more production challenges and either grow and multiply, root, and/or acclimatize slower and less successfully are
more expensive to produce and for customers to purchase than
easier genotypes. Typing micropropagation laboratories into
an Internet search engine will access sites with additional information about micropropagation.
333
References
Air, M., Giardina, G., Farruggia, G., Zizzo, G.V., 2009. In vitro propagation of
Hibiscus rosa-sinensis (L.). Acta Horticulturae 812, 107112.
Aftab, F., Mansouri, K., Preece, J.E., 2005. The inuence of environment, media,
and zerotol on forcing and in vitro establishment of softwood shoots from large
stem segments of Acer saccharin L. and Fraxinus pennsylvanica Marsh.
Propagation of Ornamental Plants 5, 113118.
Anderson, M. (2001). Tissue-culture acclimation at Carlton Plants. Combined
Proceedings of the International Plant Propagators Society, vol. 51,
pp. 308309.
Anderson, W.C., 1980. Mass propagation by tissue cultures: Principles and
techniques. In: Zimmerman, R.H. (Ed.), Proceedings Conference on Nursery
Production of Fruit Plants: Applications and Feasibility. Washington, DC: USDA
ARR-NE-11, pp. 114.
Appelgren, M., Heide, O.M., 1972. Regeneration in Streptocarpus leaf discs and its
regulation by temperature and growth substances. Physiologia Plantarum 27,
417423.
Armstrong, M. (2001). Tissue culture acclimation. Combined Proceedings of the
International Plant Propagators Society, vol. 51, pp. 304307.
Arrebola, M.L., Socorro, O., Barcelo-Munoz, A., Simon-Perez, E., Pliego-Alfaro, F.,
1997. Micropropagation of Satureja obovata Lag. HortScience 32,
12781280.
Ball, E., 1946. Development in sterile culture of stem tips and sub-joint regions of
Tropaeolum majus L. and Lupinus albus L. American Journal of Botany 33,
301318.
Bapat, V.A., Rao, P.S., 1990. In vivo growth of encapsulated axillary buds of
mulberry (Morus indica L.). Plant Cell, Tissue and Organ Culture 20,
6970.
Benmahioul, B., Dorion, N., Kaid-Harche, M., Daguin, F., 2012. Micropropagation
and ex vitro rooting of pistachio (Pistachia vera L.). Plant Cell, Tissue and Organ
Culture 108, 353358.
Bonga, J.M., Von Aderkas, P., 1992. In Vitro Culture of Trees. Dordrecht, The
Netherlands: Kluwer Academic Publishers.
Boulay, M., 1987. In vitro propagation of tree species. In: Green, C.E., Somers, D.
A., Hackett, W.P., Biesboer, D.D. (Eds.), Plant Tissue and Cell Culture. New
York: Alan R. Liss, Inc., pp. 367382.
Brainerd, K.E., Fuchigami, L.J., 1981. Acclimatization of aseptically cultured apple
plants to low relative humidity. Journal of the American Society for Horticultural
Science 106, 515518.
Christianson, M.L., Warnick, D.A., 1985. Temporal requirement for phytohormone
balance in the control of organogenesis in vitro. Developmental Biology 112,
494497.
Cocking, E.C., 1960. A method for the isolation of plant protoplasts and vacuoles.
Nature 187, 927929.
Cooper, W.C., 1935. Hormones in relation to root formation on stem cuttings. In:
Schull, C.A., Lipman, C.B., Livingston, B.E., Ball, C.R., Lloyd, F.E. (Eds.),
Plant Physiology, vol. 10. Lancaster, PA: Science Press Printing Co.,
pp. 789794.
Cueva, A., Espinosa, C., Jordan, M., 2006. Efcient in vitro multiplication of
Aechmea Little Harv and Tillandsia cyanea linden ex K. Koch. Propagation of
Ornamental Plants 6 (4), 165169.
Debergh, P., 1983. Effects of agar brand and concentration on the tissue culture
medium. Physiologia Plantarum 59, 270276.
Debergh, P.C., Harboui, Y., Leweur, R., 1981. Mass propagation of globe artichoke
(Cynara scolymus): Evaluation of different hypotheses to overcome vitrication
with special reference to water potential. Physiologia Plantarum 53, 181187.
Debergh, P.C., Maene, L., 1985. Some aspects of stock-plant preparation for tissue
culture propagation. Acta Horticulturae 166, 2123.
334
335
Nitsch, C., Nitsch, J.P., 1967. The induction of owering in vitro in stem segments
of Plumbago Indica L. Planta 72, 355370.
Nitsch, J.P., Nitsch, C., 1956. Auxin-dependent growth of excised Helianthus
tuberosus tissues. American Journal of Botany 43, 839851.
Norstog, K., 1965. Induction of embryolike structures by kinetin in cultured barley
embryos. American Journal of Botany 52, 993999.
Padilla, I.M.G., Burgos, L., 2010. Aminoglycoside antibiotics: structure, functions
and effects on in vitro plant culture and genetic transformation protocols. Plant
Cell Reports 29 (11), 12031213.
Pennazio, S., Radol, P., 1973. Factors affecting the culture in vitro of potato
meristem tips. Potato Research 16, 2029.
Pierik, R.L.M., Ruibing, M.A., 1973. Regeneration of bulblets on bulb scale
segments of hyacinth in vitrol. Netherlands Journal of Agricultural Science 21,
129138.
Pierik, R.L.M., van Leeuwen, P., Rigter, G.C.C.M., 1979. Regeneration of leaf
explants of Anthurium andreanum Lind. in vitro. Netherlands Journal of
Agricultural Science 27, 221226.
Pillai, S.K., Hildebrandt, A.C., 1968a. In vitro differentiation of geranium
(Pelargonium hortorum Bailey) plants from apical meristems. Phyton (Buenos
Aires) 25, 8187.
Pillai, S.K., Hildebrandt, A.C., 1968b. Geranium plants differentiated in vitro from
stem tip and callus cultures. Plant Disease Reporter 52, 600601.
Pliego-Alfaro, F., Murashige, T., 1987. Possible rejuvenation of adult avocado by
graftage onto juvenile rootstocks in vitro. HortScience 22, 13211324.
Preece, J.E. 2001. The most tricky part of micropropagation: establishing plants in
greenhouses and elds. Combined Proceeding International Plant Propagators
Society, vol. 51, 300303.
Preece, J.E., 2003. A century of progress with vegetative plant propagation.
HortScience 38, 10151025.
Preece, J.E., 2008. Stock plant physiological factors affecting growth and
morphogenesis. In: George, E.F., Hall, M.A., de Klerk, G.J. (Eds.), Plant
Propagation by Tissue Culture: The Background, third ed., vol. 1. Dordrecht, The
Netherlands: Springer, pp. 403422.
Preece, J.E., 2010a. Acclimatization of plantlets from in vitro to the ambient
environment. In: Flickinger, M.C. (Ed.), Encyclopedia of Industrial Biotechnology
Bioprocess, Bioseparation, and Cell Technology. New York: John Wiley and
Sons, pp. 19.
Preece, J.E., 2010b. Micropropagation in stationary liquid media. Propagation of
Ornamental Plants 10, 183187.
Preece, J.E., Huetteman, C.A., Ashby, W.C., Roth, P.L., 1991a. Micro- and cutting
propagation of silver maple. I. Results with adult and juvenile propagules.
Journal of the American Society for Horticultural Science 116, 142148.
Preece, J.E., Huetteman, C.A., Ashby, W.C., Roth, P.L., 1991b. Micro-and
cutting propagation of silver maple. II. Genotype and provenance affect
performance. Journal of the American Society for Horticultural Science 116,
149155.
Preece, J.E., Read, P.E., 2003. Novel methods in micropropagation. Acta Horticulture
616, 7176.
Preece, J.E., Sutter, E.G., 1991. Acclimatization of micropropagated plants to the
greenhouse and eld. In: Debergh, P.C., Zimmerman, R.H. (Eds.),
Micropropagation. Dordrecht, The Netherlands: Kluwer, pp. 7193.
Preece, J.E., West, T.P., 2006. Greenhouse growth and acclimatization of
encapsulated Hibiscus moscheutos nodal segments. Plant Cell, Tissue and Organ
Culture 87, 127138.
Read, P.E., 1992. Environmental and hormonal effects in micropropagation. In:
Kurata, K., Kozai, T. (Eds.), Transplant Production Systems. The Netherlands:
Kluwer Academic Publishers, pp. 231246.
Read, P.E., 1990. Environmental effects in micropropagation. In: Ammirato, P.V.,
Evans, D.A., Sharp, W.R., Bajaj, Y.P.S. (Eds.), Handbook of Plant Cell Culture:
Ornamental species, vol. 5, pp. 95125.
Read, P.E., Economou, A.S., Fellman, C.D., 1984. Manipulating stock plants for
improved in vitro mass propagation. In: Novak, F.J., Havel, L., Dolezel, J. (Eds.),
Plant Tissue Cell Cult: Application to Crop Improvement. Proceedings of the
International Symposium for Plant Tissue Cell Culture. Prague: Czech Academy
of Sciences, pp. 467473.
Read, P.E., Fellman, C.D., Economou, A.S., Yang, Q-G., 1986. Programming stock
plants for propagation success. Proceedings of the International Plant
Propagators Society, vol. 35, pp. 8491.
Read, P.E., Garton, S., Carlson, C., Conviser, L., Preece, J., 1979. Programming
stock plants for tissue culture success. Proceedings of the Plant Growth
Regulator Working Group 6, 197204.
Read, P.E., Garton, S., Louis, K.A., 1983. Use of recirculating hydroponic systems
for macro- and micropropagation studies. Acta Horticulture 150, 405414.
336
Read., P.E., Garton, S., Louis, K. and Zimmermann, E. 1982. In vitro propagation of
species for bioenergy plantations. Proceedings of the 5th International Congress
on Plant Tissue and Cell Culture, pp. 757758. Calgary, Canada: University of
Calgary Press.
Read, P.E., Gavinlertvatana, P., Suriyajantratong, P., Garton, S., Brenner, M., 1978.
Stock plants affect tissue culture success. In: Hughes, K., Henke, R., Constantin,
M. (Eds.), Propagation of Higher Plants Through Tissue Culture. Knoxville, TN:
University of Tennessee, pp. 249.
Refouvelet, E., Le Nours, S., Tallon, C.F., Daguin, C., 1998. A new method for
in vitro propagation of lilac Syringa vulgaris L.: Regrowth and storage conditions
for axillary buds encapsulated in alginate beads, development of a preacclimatisation stage. Scientia Horticulturae 74, 233241.
Reinert, J., 1959. Uber die kontrolle der morphogenese und die induktion von
adventivembryonen an gewebekulturen aus karotten. Planta 53, 318333.
Reinert, J., Tozawa, M., Semeroff, S., 1967. Nitrogen compounds as factors of
embryogenesis in vitro. Nature 216, 12151216.
Reuther, G., 1987. Co2 exchange and transpiration of in vitro plantlets. XIV
International Botanical Congress, 92 (Abstract).
Robacker, C.D., Chang, C.J., 1992. Shoot tip culture of Muscadine grape to
eliminate Pierce's disease bacteria. HortScience 27, 449450.
Rodrigues, P.H.V., Lima, A.M.L.P., Ambrosano, G.M.B., de Fatima Batista Dutra, M.,
2005. Acclimatization of micropropagated Heliconia bihai (Heliconiaceae) plants.
Scientia Agricola (Piracicaba, Brazil) 62, 299301.
Rugini, E., 1988. Somatic embryogenesis and plant regeneration in olive (Olea
europaea L.). Plant Cell Tissue & Organ Culture 14, 207214.
Ruta, C., Perrini, R., Tagarelli, A., Morone Fortunato, I., 2009. Use of arbuscular
mycorrhiza for acclimatization of micropropagated plantlets of melon, oregano,
artichoke and Spanish broom. Acta Horticulture 812, 473477.
Sangwan, R.S., Detrez, C., Sangwan-Norreel, B.S., 1987. In vitro culture of shoot-tip
meristems in some higher plants. Acta Horticulturae 212, 661666.
Sarkar, D., Naik, P.S., 1998. Synseeds in potato: An investigation using
nutrient-encapsulated in vitro nodal segments. Scientia Horticulturae 73,
179184.
Scaranari, C., Leal, P.A.M., Mazzafera, P., 2009. Shading and periods of
acclimatization of micropropagated banana plantlets cv. Grande Naine. Scientia
Agricola (Piracicaba, Braz.) 66, 331337.
Shepard, J.F., Bidney, D., Shahin, E., 1980. Potato protoplasts in crop improvement.
Science 208, 1724.
Skirvin, R.M., Janick, J., 1976. Tissue culture induced variation in scented
Pelargonium spp. Journal of the American Society for Horticultural Science 101,
281290.
Skoog, F., Miller, C.O., 1957. Chemical regulation of growth and organ formation in
plant tissues cultured in vitro. Symposium of the Society for Experimental
Biology 11, 118131.
Skoog, F., Tsui, C., 1948. Chemical control of growth and bud formation in tobacco
stem segments and callus cultured in vitro. American Journal of Botany 35,
782787.
Steward, F.C., Mapes, M.O., Mears, K., 1958. Growth and organized development of
cultured cells. II. Organization in cultures grown from freely suspended cells.
American Journal of Botany 45, 705708.
Stimart, D.P., Ascher, P.D., 1981. Developmental response of Lilium longiorum
bulblets to constant or alternating temperatures in vitro. Journal of the American
Society for Horticultural Science 106, 450454.
Stimart, D.P., Mather, J.C., Schroeder, K.R., 1998. Shoot proliferation and rooting
in vitro of Pulmonaria. HortScience 33, 339341.
Tawk, A.A., Read, P.E., Cuppett, S.L., 1992. Effect of some nutritional factors on
monoterpene synthesis in Rosemarinus ofcinalis cultured in vitro. Acta Hortic.
319, 189194.
Thimann, K.V. 1935. On an analysis of activity of two growth-promoting substances
on plant tissues. Proceedings of the Koninklijke Nederlandse Akademie van
Wetenschappen, vol. 38, 896912.
Thimann, K.V., Went, F.W. 1934. On the chemical nature of the root-forming
hormone. Proceedings of the Koninklijke Nederlandse Akademie van
Wetenschappen, vol. 37, 456459.
Tisserat, B., Jones, D., Galletta, P.D., 1992. Microwave sterilization of plant tissue
culture medium. HortScience 27, 358361.
Tsvetkov, I., Jouve, L., Hoffmann, L., Hausman, J.-F., 2007. Effect of auxins and
alginate encapsulation on in vitro rooting of Sorbus domestica. Belgian Journal
of Botany 140, 151156.
Uno, S., Preece, J., 1987. Micro-and cutting propagation of Crimson Pygmy
barberry. HortScience 22, 488491.
Van der Plas, L.H.W., Wagner, M.J., 1986. Effect of oxygen on growth and
respiration of potato tuber callus. Plant Cell, Tissue and Organ Culture 7,
217225.
Vanderschaege, A.M., Debergh, P.C., 1988. Inuence of explant type on
micropropagation of woody species. Mededelingen van de Faculteut
Landbouwwetenschappen, Rijksuniversiteit Gent 53, 17631768.
Van Sambeek, J.W., Lambus, L.J., Khan, S.B., Preece, J.E., 1997a. In vitro
establishment of tissues from adult black walnut. In: Van Sambeek, J.W. (Ed.),
Knowledge for the Future of Black Walnut, pp. 7892. USDA Forest Service
General Technical Report NC-191.
Van Sambeek, J.W., Lambus, L.J. and Preece, J.E. 1997b. Production of epicormic
sprouts on branch segments of adult black walnut for in vitro culture. 88th
Annual Report of the Northern Nut Growers Association, pp. 93104.
Vasil, I.K., Hildebrandt, A.C., Riker, A.J., 1964. Endive plantlets from freely
suspended cells and cell groups in vitro. Science 146, 7677.
Vieitez, A.M., Sanchez, M.C., Amo-Marco, J.B., Ballester, A., 1994. Forced ushing
of branch segments as a method for obtaining reactive explants of mature
Quercus robur trees for micropropagation. Plant Cell, Tissue and Organ Culture
37, 287295.
Villalobos, V.M., Leung, D.W.M., Thorpe, T.A., 1984. Light-cytokinin interaction in
shoot formation in cultured cotyledon explants of radiata pine. Physiologia
Plantarum 61, 497504.
Went, F.W. 1929. On a substance causing root formation. Proceedings of the
Koninklijke Nederlandse Akademie van Wetenschappen, vol. 32, pp. 3539.
Went, F.W. 1934a. A test method for rhizocaline, the root-forming substance.
Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, vol.
37, pp. 445455.
Went, F.W. 1934b. On the pea test method for auxin, the plant growth hormone.
Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, vol.
37, pp. 547555.
Werckmeister, P., 1971. Light induction of geotropism and the control of
proliferation and growth of Cymbidium in tissue culture. Botanical Gazette 132,
346350.
Wetzstein, H.Y., Kim, C., Sommer, H.E., 1994. Vessel volume, gelling agent, and
basal salts affect pH and gel strength of autoclaved tissue culture media.
HortScience 29, 683685.
White, P.R., 1963. The Cultivation of Animal and Plant Cells, second ed. New York:
Ronald Press, p. 228.
Wilmar, C., Hellendoorn, M., 1968. Growth and morphogenesis of asparagus cells
cultured in vitro. Nature 217, 369370.
Wilson, P.J., 1994. The concept of a limiting rooting morphogen in woody stem
cuttings. Journal of Horticultural Science 69, 591600.
Xu, J., Wang, Y., Zhang, Y., Chai, T., 2008. Rapid in vitro multiplication and ex
vitro rooting of Malus zumi (Matsumura) Rehd. Acta Physiologiae Plantarum 30,
129132.
Yang, G., Read, P.E., 1989. Effects of BA, GA, IAA and NAA in the forcing solution
on bud break and shoot elongation in forced woody stems. Proceedings of the
Plant Growth Regulator Society of America 150155.
Yang, G., Read, P.E., 1992. Pre-forcing treatments inuence bud break and shoot
elongation in forced woody species. Journal of Environmental Horticultur 10,
101103.
Yang, G., Read, P.E., 1997. Plant growth regulators in the forcing solution
inuenced bud break and shoot elongation of dormant woody plant species.
PGRSA Quarterly 25, 145151.
Yang, Q-G, Read, P.E., Fellman, C.D., Hosier, M.A., 1986. Effect of cytokinin, IBA
and rooting regime on Chinese chestnut cultured in vitro. HortScience 21,
133134.
Yu, D-H, Meredith, C.P., 1986. The inuence of explant origin on tissue browning
and shoot production in shoot tip cultures of grapevine. Journal of the American
Society for Horticultural Science 111, 972975.
Zimmerman, R.H., 1984. Rooting apple cultivars in vitro: Interactions among light,
temperature, phloroglucinol and auxin. Plant Cell, Tissue and Organ Culture 3,
301311.
Zimmerman, P.W., Wilcoxon, F., 1935. Several chemical growth substances which
cause initiation of roots and other responses in plants. Contributions of the
Boyce Thompson Institute 7, 209229.
Glossary
Agricultural System Model A mathematical model of
soilwaterplantclimate management system.
Cover crops Short-duration crops that are planted after
harvest of main crop (e.g., corn) and planting of the next
main crop in rotation (e.g., soybean).
Crop simulation Computation of plant growth processes
with a mathematical model.
Crop water production function Crop biomass or grain
yield at different levels of water use; transpiration,
evaporation and transpiration, or water supplied in the soil.
Emission scenarios Level of greenhouse gas (GHG)
concentrations in the atmosphere depending upon the
different scenarios of emission from various sources. In the
doi:10.1016/B978-0-444-52512-3.00246-1
337
338
14 000
12 000
10 000
8000
6000
4000
2000
0
1975
1980
1985
1990
1995
2000
2005
50
40
RMSE=4.9, r 2=0.74
30
20
10
0
1988
1990
1992
1994
1996
1998
2000
2002
2004
100
Measured annual N loading
Simulated annual N loading
Annual N loading: RMSE=12.6, r 2=0.71
80
60
40
20
0
1988
100
1990
1992
1994
1996
1998
2000
2002
2004
80
60
40
20
0
1988
1990
1992
1994
1996
1998
2000
2002
2004
Year
Figure 1 Simulated and measured average corn and soybean yield, yearly tile ow, yearly N loading in tile ow, and ow-weighted N
concentration in tile ow across all treatments over 13 years, at Nashua, IA, USA. The results give condence in the model for identifying best
management of N. RMSE, root mean square error; r2, coefcient of determination. Reproduced with permission from Ma, L., Malone, R.W.,
Heilman, P., et al., 2007. RZWQM simulation of long-term crop production, water and nitrogen balances in Northeast Iowa. Geoderma 140,
247259.
339
340
20
Tile driange (cm)
Surface runoff (cm)
N loss to tile (kg N ha1)
N loss to
denitrification (kg N ha1)
15
10
C
PC
S-
S-
N
C
S-
C
P-
C
T-
P-
FD
FD
P-
S-
C
C
S-
N
S-
T-
FD
D
C
P-
C
C
C
-M
C
C
-C
P-
T-N
C
D
C
FD
P-C
C
C
-M
C
C
-N
T-
P-
FD
FD
Management systems
Figure 2 Simulated average annual tile drainage, surface runoff, N loss to tile drainage, and N loss to denitrication for various management
systems based on calibrated model from a study in IA, USA. CC, continuous corn; CS, cornsoybean rotation; FD, free drainage; CD, controlled
drainage; NT, no-till; MP, moldboard plow; CP, chisel plow. The model runs were from 1979 to 2002. The results serve as a guide to
management. N losses are expressed on a per year basis. Reproduced with permission from Ma, L., Malone, R.W., Heilman, P., et al., 2007.
RZWQM simulation of long-term crop production, water and nitrogen balances in Northeast Iowa. Geoderma 140, 247259.
the current irrigation amounts are less than 300 mm for wheat,
and little or no irrigation for maize. This amount of available
water can only sustain an autoirrigation triggered at 40% and
recharged to 60% eld capacity and produce a potential wheat
yield of 76% and a potential maize yield of 86%. At this irrigation level, the N application rate should be reduced to
between 100 and 200 kg N ha1 for wheat, to match the
limited available irrigation water resource in the region for
efcient use of N and water and minimal nitrate-N leaching
loss (Figure 6). For maize, irrigation was not necessary due to
adequate rainfall, and 100 kg N ha1 per crop application
rates are reasonable considering the high risk of nitrate-N
leaching potential (Figure 6).
Thorp et al. (2006) used the calibrated CERES-Maize model
to prescribe N rate for a heterogeneous eld in Iowa, USA,
using long-term weather data (37 years) to study maize production and N leaching risks at different levels of precision
nitrogen (N) management. The value in using long weather
records could be expanded to discuss risk assessments of decision making and probabilities of success. Nitrogen was
applied uniformly in the spring; for each rate of application,
the eld was divided into 100 grid cells and the model was run
for each cell for 37 years. To maximize farmers net returns, an
average of 56.2 kg N ha1 overall grid cells was left in the soil
as residual N, which was subjected to leaching (Figure 7). To
achieve an average residual soil N at harvest under 40 kg ha1
in 80% of the growing seasons, the producers opportunity
341
Nitrate reduction
CSNTMat <VALUE>
<2
29
1015
213
1619
1424
2028
2536
3748
> 28
4960
6171
Figure 3 RZWQM2 model used to calculate annual nitrate reduction in tile water by cover crop in the US Midwest region (kg N ha1 year 1).
Reproduced with permission from Malone, R.W., Jaynes, D.B., Kaspar, T.C., et al., 2014. Cover crops in the upper Midwest USA: Simulated effect
on nitrate leaching with articial drainage. Journal of Soil and Water Conservation.
342
(a)
(b)
Interpolation
Sites
7.1 11.6
4.0 13.2
11.6 16.9
13.2 20.4
16.9 24.3
24.3 32.3
20.4 28.1
28.1 35.8
32.3 49.6
35.8 46.3
0
195
Interpolation
Sites
N
W
390
E
S
780
1170
33.3 41.0
39.4 45.1
41.0 46.2
15.1 50.1
46.2 51.9
50.1 54.1
51.9 55.2
54.1 58.0
55.2 6.09
58.0 64.9
1560
km
Figure 4 RZWQM2 used to calculate annual nitrate reduction in tile water by controlled drainage in the US Midwest region (kg N ha1 year 1).
Reproduced with permission from Thorp, K.R., Jaynes, D.B., Malone, R.W., 2008. Simulating the long-term performance of drainage water
management across the Midwestern United States. Transactions of the ASABE 51 (3), 961976.
343
1.0
Cumulative probability
0.8
0.6
0.4
00 kg N ha1
28 kg N ha1
56 kg N ha1
84 kg N ha1
112 kg N ha1
0.2
0.0
0
1000
2000
3000
(a)
4000
5000
ha1)
1.0
Cumulative probability
0.8
0.6
0.4
0.2
0.0
0
(b)
20
40
60
80
100
120
140
160
180
ha1)
Figure 5 Cumulative probability distribution function plots of winter wheat grain yields and residual soil N at harvest simulated by CERES-wheat
model under different N application rates. N was broadcast and the crop was planted every year. Reproduced with permission from Saseendran, S.
A., Nielsen, D.C., Ma, L., Ahuja, L.R., Halvorson, A.D., 2004. Modeling nitrogen management effects on a winter wheat cropping system using
RZWQM and CERES-wheat. Agronomy Journal 96, 615630.
4
2
0
9
6
3
0
Recharge: 40 50 60 70 80 50 60 70 80 60 70 80 70 80 80
40
50
60
70 80
Triggering:
% Field capacity
2
Maize (200 kg N ha1)
9
6
3
0
Recharge: 40 50 60 70 80 50 60 70 80 60 70 80 70 80 80
40
50
60
70 80
Triggering:
30
0
400
100
60
4
2
0
9
6
3
0
Recharge: 40 50 60 70 80 50 60 70 80 60 70 80 70 80 80
Triggering:
40
50
60
70 80
% Field capacity
30
0
400
200
100
0
Recharge: 40 50 60 70 80 50 60 70 80 60 70 80 70 80 80
40
50
60
70 80
Triggering:
% Field capacity
60
Nitrate-N leaching (kg N ha1)
200
% Field capacity
6
60
0
Recharge: 40 50 60 70 80 50 60 70 80 60 70 80 70 80 80
40
70 80
60
50
Triggering:
% Field capacity
90
Nitrate-N leaching (kg N ha1)
344
30
0
400
200
100
0
Recharge: 40 50 60 70 80 50 60 70 80 60 70 80 70 80 80
40
50
60
70 80
Triggering:
% Field capacity
Figure 6 Average grain yields and nitrate-N leaching across seasons under irrigations triggered at varying levels of % eld capacity (FC) and
stopped after root zone recharge to selected levels of %FC and at different N application rates (100, 200, 300 kg N ha1 per season) simulated by
RZWQM2 from 1961 to 1998. Bars indicate 1 standard derivation across 38 years of simulation (196198). Reproduced with permission from
Fang, Q., Ma, L., Yu, Q., et al., 2008. Modeling nitrogen and water management effects in a wheat-maize double-cropping system. Journal of
Environmental Quality 37, 22322242.
345
4643085
N Rate (kg ha1)
<180
200
4642857
220
240
260
4642629
N
W
4642400
45
45
90 m
4642172
411001
411139
346
4643085
4643085
Opportunity
cost (US $ ha1)
90130
030
130180
4642857
4642857
3070
210225
225240
4642629
N
W
140250
4642629
N
4642400
4642400
45
70140
Zone 15 UTMY (m)
180210
45
45
90 m
4642172
45
90 m
4642172
411139
411001
411001
411139
Figure 8 N rate and opportunity cost for leaving less than 40 kg N ha 1 of unused N in the soil 80% of the time. Opportunity cost is the
additional cost that reduces the maximum prot. Reproduced with permission from Thorp, K.R., Batchelor, W.D., Paz, J.O., Steward, B.L., Caragea,
P.C., 2006. Methodology to link production and environmental risks of precision nitrogen management strategies in corn. Agricultural Systems 89,
272298.
14 000
1:1 line
Rainfed (199397)
Irrigated (198486)
12 000
Calibration
10 000
8000
6000
4000
1997
2000
0
0
2000
4000
6000
8000
10 000
12 000
14 000
347
12 000
10 000
8000
6000
20% V, 80% R - with N stress
40% V, 60% R - with N stress
50% V, 50% R - with N stress
20% V, 80% R - No N stress
40% V, 60% R - No N stress
50% V, 50% R - No N stress
4000
2000
200
(a)
400
Irrigation (mm)
600
800
12 000
10 000
8000
6000
20% V, 80% R - with N stress
40% V, 60% R - with N stress
50% V, 50% R - with N stress
20% V, 80% R - No N stress
40% V, 60% R - No N stress
50% V, 50% R - No N stress
4000
2000
200
(b)
400
Irrigation (mm)
600
800
Figure 10 Simulated grain yield response to 100700 mm irrigations (gross irrigation), split between vegetative and reproductive stages at 20:80,
40:60, and 50:50 with (a) 22 June and (b) 15 July as cutoff dates differentiating between growth stages for corn grown at Akron, CO. Distribution
of average seasonal potential evapotranspiration demand between the vegetative and reproductive growth stages was (a) 38:62 and (b) 55:45.
Error bars represent one standard deviation from the mean. Deviations of grain yields from the mean value were due to variation in rainfall,
temperature, and solar irradiance during the crop growth period from 1912 to 2005. Average crop season rainfall was 284 mm. Reproduced with
permission from Saseendran, S.A., Ahuja, L.R., Nielsen, D.C., Trout, T., Ma, L., 2008. Use of crop simulation models to evaluate limited irrigation
management options for corn in a semiarid environment. Water Resources Research 44, W00E02. doi:10.1029/2007WR006181.
348
300
N kg ha1
200
150
100
50
0
100
(a)
200
300
400
500
600
700
300
N kg ha1
200
N leached
Residual N
N uptake
150
100
50
0
100
(b)
200
300
400
500
600
700
400
500
Irrigation (mm)
600
700
300
N kg ha1
200
150
100
(Figure 17). The biggest GHG emission was from the Central
Region that had the biggest area and more fertilizer applications. Results also showed higher N2O emission from corn
and soybean elds compared to cotton, alfalfa, and wheat.
Current management practices (19912000) produced much
more N2O than pre-1940 management (192130) or native
vegetation (15911600) (Figure 17). However, conversion
into no-tillage could mitigate 20% of agricultural GHG emissions in the United States (Del Grosso et al., 2005). In a later
study at the global scale, they found that nitrication inhibitors led to 10% reduction in N losses, but when combined
with no-till, it resulted in 50% reduction in GHG emissions
and 7% increase in crop yield (Del Grosso et al., 2009). In
Californias Central Valley, the model results showed that organic practices had the greatest potential for soil GHG ux
reduction, followed by cover cropping and conservation tillage
(De Gryze et al., 2010). In another similar simulation study
(De Gryze et al., 2011), the results showed that combining
various mitigation practices (conservation tillage, winter cover
cropping, manure application, and reduced N fertilizer input)
led to larger reductions in GHG emissions than the sum of the
reductions from individual practices. The combination of
winter cover cropping with manure application was particularly efcient in reducing GHG emissions.
These model applications showed complex effects of these
various alternative farming management practices across different climate and soil conditions. Process-based models
showed great potential for quantifying these complex effects of
alternative management on GHG emissions across different
soil and climate conditions. However, we need a better
understanding of the underlying factors that cause these variations across soils, climates, and management; and identify
strategies for mitigation under those conditions. There is a
particular need to quantify GHG emissions due to nitrication
and denitrication processes. In general, the soilwatercrop
management practices that increase crop biomass growth and
generate higher carbon residue can potentially increase soil
carbon storage to counteract the CO2 and CHG buildup in the
atmosphere (Smith et al., 2007).
50
0
100
(c)
200
300
349
Grain yield
(Mg ha1)
4
100 mm
150 mm
3
200 mm
250 mm
WUE
(kg m3)
1.0
0.8
0.6
Water drinage
(cm)
4
3
2
1
0
Nitrogen leaching
(kg N ha-1)
200
150
100
50
(a)
50:50
(b)
60:40
70:30
80:20
90:10
100:0
50:50
60:40
70:30
80:20
90:10
100:0
350
5000
Wheat biomass
WCM
WF (CT)
WF (NT)
WCF
12 000
Average
1 standard deviation
Wheat yield
WCM
WF (CT)
WF (NT)
WCF
Average
1 standard deviation
1 to 1 line
6000
3000
3000
2000
1 to 1 line
1000
12 000
Corn biomass
WCM
WCF
Average
1 standard deviation
9000
1 to 1 line
6000
3000
WCM
WCF
Corn yield
4000
Average
1 standard deviation
3000
2000
1 to 1 line
1000
5000
0
15 000
Simulated biomass (kg ha1)
4000
5000
0
15 000
12 000
9000
WCM
Millet biomass
WCM
Average
1 standard deviation
9000
1 to 1 line
6000
3000
15 000
Millet yield
4000
Average
1 standard deviation
3000
1 to 1 line
2000
1000
Circled points are
from calibration data set
0
0
3000
6000
9000
12 000 15 000
ha1)
1000
2000
3000
4000
5000
ha1)
Figure 13 RZWQM modeling of 1718 years data for biomass and grain yield for wheat, corn, and millet crops from four different rotations at
Akron, CO, USA. WCM, wheatcornmillet; WF, wheatfallow; and WCF, wheatcornfallow. Reproduced with permission from Saseendran, S.A.,
Nielsen, D.C., Ma, L., Ahuja, L.R., Vigil, M.F., 2010. Simulating alternative dryland rotational cropping systems in the central Great Plains with
RZWQM2. Agronomy Journal 102, 15211534.
351
Canola
Proso millet
*
*
Foxtail millet
Triticale
1000
750
500
*
*
250
250
500
1000
750
500
250
250
500
1000
750
500
250
25% PAW
50% PAW
75% PAW
100% PAW
Corn
250
500
1000
750
500
250
250
500
Figure 14 Validated RZWQM2 with long-term weather data generated this graph of Net Return for ve summer crops (corn, canola, proso millet,
foxtail millet, and triticale), as a guide for summer crop selection in a wheatsummer cropfallow rotation in Colorado and the Central Great Plains,
based on100, 75, 50, and 100% plant available water (PAW) at planting. Reproduced with permission from Saseendran, S.A., Nielsen, D.C., Ahuja,
L.R., Ma, L., Lyon, D.J., 2013. Simulated yield and protability of ve potential crops for intensifying the dryland wheat-fallow production system.
Agricultural Water Management 116, 175192.
14 000
ha1)
12 000
10 000
2008
2009
2010
2011
1:1 line
8000
6000
4000
2000
2000
4000
6000
8000
10 000
12 000
14 000
ha1)
Figure 15 Comparisons of simulated and measured corn grain yields in the limited irrigation trials conducted at Greeley, CO, from 2008 to 2010.
RMSE, root mean square error. Reproduced with permission from Saseendran, S.A., Nielsen, D.C., Ahuja, L.R., Ma, L., Lyon, D.J., 2013. Simulated
yield and protability of ve potential crops for intensifying the dryland wheat-fallow production system. Agricultural Water Management 116,
175192.
352
12 000
Yuma county
10 000
8000
6000
4000
2000
0
20
30
40
Weld county
12 000
Grain yield (kg ha1)
10
10 000
8000
6000
4000
2000
0
10
20
30
40
50
60
Washington county
12 000
10 000
8000
6000
4000
2000
0
10
20
30
40
50
Table 1
Major regions
Minor regions
Crop simulated
Northeast
Central
Southeast
Southwest
WI, MI, NY, VT, NH, ME, RI, CT, MA, NJ, and
DE
PA, WV, KY, TN, OH, IN, IL, IA, MO, and MN
VA, MD, NC, SC, GA, FL, AL, MS, LA, and AR
OK, TX, NM, AZ, UT, NV, and CA
Northwest
KS, NE, SD, ND, CO, WY, MT, ID, OR, and WA
30
353
EF
DAYCENT
25
Tg C yr1
20
15
10
5
0
Central
Northeast
Northwest
Southeast
Southwest
(a)
18
EF
DAYCENT
15
Tg C yr1
12
0
(b)
Com
Cotton
Central
Northeast
Alfalfa
Soybean
Northwest
Southeast
Wheat
0.5
Mg C ha1 yr1
0.4
0.3
0.2
0.1
0.0
Southwest
(c)
Figure 17 Simulated total N2O with IPCC emission factor (EF) and DAYCENT model for (a) ve regions in the United States, (b) ve major crops
in the United States, and (c) three management systems (from left to right, current management, pre-1940 management, and native vegetation).
Results are 10-year mean and standard deviation in units of CO2-C equivalents. Reproduced with permission from Del Grosso, S.J., Mosier, A.R.,
Parton, W.J., Ojima, D.S., 2005. DAYCENT model analysis of past and contemporary soil N2O and net greenhouse gas ux for major crops in the
USA. Soil And Tillage Research 83, 924.
354
climate-change studies in the literature. To overcome this uncertainty, the use of multimodel ensembles is better to project
future climate. In a recent study of irrigated corn in the Great
Plains of the USA, Islam et al. (2012) used an ensemble of 112
bias corrected and spatially disaggregated GCM projections at
1/81 spatial resolution for the period 19502099 and then ran
the RZWQM2 model for the prediction of corn production in
future climates. Simulation using the RZWQM2 model with
the ensembles showed decreases in irrigated corn yield during
2020, 2050, and 2080 with changes in temperature. As shown
in Figure 18, the changes in temperature (T) resulted in the
same probability distribution curve as that of with changes in
both temperature and precipitation (T P; one overlapping
the other in the gure.). Similarly, changes in precipitation (P)
resulted in the probability distribution curves similar to that of
the baseline (base) probability distribution curve. Thus, the
changes in precipitation had no effect on yield because with
full irrigation, 100% consumptive use demand was met by
irrigation. When CO2 fertilization effect (T P CO2) was
considered, there was less reduction in yield (Figure 18).
1.0
0.9
2050
Cumulative probability
0.8
0.7
0.6
Base
0.5
T
P
0.4
T+P
0.3
T+P+CO2
0.2
0.1
0.0
4000
6000
8000
Yield (kg
10 000
12 000
14 000
ha1)
1.0
2080
0.9
Cumulative probability
0.8
0.7
0.6
Base
0.5
T
P
0.4
T+P
0.3
T+P+CO2
0.2
0.1
0.0
4000
6000
8000
Yield (kg
10 000
12 000
14 000
ha1)
Figure 18 Cumulative distribution function (CDF) of corn yield in response to changes in temperature (T), precipitation (P), and CO2 in future
years over the baseline years for S1 (for an ensemble of 112 projections) scenario, at Greeley, CO, USA. Reproduced with permission from Islam,
A., Ahuja, L.R., Garcia, L.A., et al., 2012. Modeling the impacts of climate change on irrigated corn production in the Central Great Plains.
Agricultural Water Management 110, 94108.
355
1.0
100ET
0.9
0.8
0.7
Base
CDF
0.6
2020
0.5
2050
0.4
2080
0.3
0.2
0.1
0.0
1500
3500
5500
7500
9500
11500
13500
35
y = 5.3507x + 5.8635
R2 = 0.9926
30
25
20
15
10
5
0
35
30
y = 1.2619x 5.1459
R2 = 0.9956
Without CO2
With CO2
25
20
y = 0.8268x 0.5496
R2 = 0.9323
15
10
5
0
15
20
25
30
35
356
Conclusions
Achieving environmental protection and food security are two
somewhat conicting goals in agriculture. With increasing
demand on food due to escalating population, the society
requires high yield from farmland, which calls for high N,
water, and pesticide inputs. The latter will denitely increase
the risk of environmental pollution. The key to this complex
issue is to balance and optimize and assess risks, impacts, and
tradeoffs. Agricultural system models have the unique capability to provide a balanced solution to this dilemma. This
article has demonstrated some promising examples of model
applications in the areas of water and N management, and
climate-change effects on crop production. These applications
can be extended to other environmental and food security
issues, such as pesticides and phosphorus in runoff and soil
erosion.
References
Ahuja, L.R., Ma, L., Howell, T.A., 2002. Whole system integration and modeling
Essential to agricultural science and technology in the 21st century. In: Ahuja, L.
R., Ma, L., Howell, T.A. (Eds.), Agricultural System Models in Field Research
and Technology Transfer. Boca Raton, FL: CRC Press, pp. 19.
Andales, A.A., Ahuja, L.R., Peterson, G.A., 2003. Evaluation of GPFARM for
dryland cropping systems in Eastern Colorado. Agronomy Journal 95 (6),
15101524.
Bassu, S., Asseng, S., Richards, R., 2011. Yield benets of triticale traits for wheat
under current and future climates. Field Crops Research 124, 1424.
Bennett, K.E., Werner, A.T., Schnorbus, M., 2012. Uncertainty in hydrologic and
climate change impact analyses in Headwater basins of British Columbia. Journal
of Climate 25, 57115730. doi:10.1175/JCLI-D-11-00417.1.
CGIAR Science Council, 2005. System Priorities for CGIAR Research 20052015.
Rome: Science Council Secretariat, p. 16.
Chavas, D.R., Izaurralde, R.C., Thomson, A.M., Gao, X., 2009. Long-term climate
change impacts on agricultural productivity in eastern China. Agricultural and
Forest Meteorology 149, 11181128.
Chen, D., Li, Y., Grace, P., Mosier, A.R., 2008. N2O emissions from agricultural
lands: A synthesis of simulation approaches. Plant and Soil 309, 169189.
Crabbe, P.D., Lapen, R., Clark, H., Sunohara, M., Liu, Y., 2012. Economic benets
of controlled tile drainage: Watershed evaluation of benecial management
practices, South Nation River basin, Ontario. Water Quality Research Journal of
Canada 47, 3041.
Daccache, A., Weatherhead, E.K., Stalham, M.A., Knox, J.W., 2011. Impacts of
climate change on irrigated potato production in a humid climate. Agricultural
and Forest Meteorology 151, 16411653.
De Gryze, S., Lee, J., Ogle, S., Paustian, K., Six, J., 2011. Assessing the
potential for greenhouse gas mitigation in intensively managed annual cropping
systems at the regional scale. Agriculture, Ecosystem and Environment 144,
150158.
De Gryze, S., Wolf, A., Kaffka, S.R., et al., 2010. Simulating greenhouse gas budgets
of four California cropping systems under conventional and alternative
management. Ecological Applications 20, 18051819.
Del Grosso, S.J., Mosier, A.R., Parton, W.J., Ojima, D.S., 2005. DAYCENT model
analysis of past and contemporary soil N2O and net gas ux for major crops in
the USA. Soil and Tillage Research 83, 924.
Del Grosso, S.J., Ojima, D.S., Parton, W.J., et al., 2002. Simulated effects of
dryland cropping intensication on soil organic matter and greenhouse gas
exchanges using the DAYCENT ecosystem model. Environmental Pollution 116,
S75S83.
Del Grosso, S.J., Ojima, D.S., Parton, W.J., et al., 2009. Global scale DAYCENT
model analysis of greenhouse gas emissions and mitigation strategies for
cropped soils. Global Planet Change 67, 4450.
Fang, Q., Ma, L., Yu, Q., et al., 2008. Modeling nitrogen and water management
effects in a wheat-maize double-cropping system. Journal of Environmental
Quality 37, 22322242.
Fang, Q.X., Ma, L., Yu, Q., et al., 2010. Irrigation strategies to improve the water
use efciency of wheat-maize double cropping systems in North China Plain.
Agricultural Water Management 97, 11651174.
Farahbakhshazad, N., Dinnes, D., Li, C., Jaynes, D., Salas, W., 2008. Modeling
biogeochemical impacts of alternative management practices for a row-crop eld
in Iowa. Agriculture, Ecosystems and Environment 123, 3048.
Gouache, D., Bris, X.L., Bogard, M., et al., 2012. Evaluating agronomic adaptation
options to increasing heat stress under climate change during wheat grain lling
in France. European Journal of Agronomy 39, 6270.
Green, T.R., Taniguchi, M., Kooi, H., et al., 2011. Beneath the surface of global
change: Impacts of climate change on groundwater. Journal of Hydrology 405,
532560.
Hartmann, A., Lange, J., Aguado, A.V., et al., 2012. A muti-model approach for
improved simulations of future water availability at a large Eastern Mediterranean
karst spring. Journal of Hydrology 468469, 130138.
Hillel, D., Rosenzweig, C., 2011. Handbook of climate change and
agroecosystems. Impact, Adaptation, and Mitigation, vol. 1. London:
Imperial College Press.
357
Hillel, D., Rosenzweig, C., 2012. Handbook of climate change and agroecosystems.
Global and Regional Aspects and Implications, vol. 2. London: Imperial College
Press.
Intergovernmental Panel on Climate Change (IPCC), 2007. Climate change 2007:
The physical science basis. Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on Climate Change (IPCC).
Cambridge: Cambridge University Press, p. 881.
International Service for National Agricultural Research (ISNAR), 2004. Method in
Our Madness: Making Sense of Ecoregional Research with Modeling Tools and
Processes. The Netherlands: The Hague, p. 68.
Islam, A., Ahuja, L.R., Garcia, L.A., et al., 2012. Modeling the impacts of climate
change on irrigated corn production in the Central Great Plains. Agricultural
Water Management 110, 94108.
Jones, J.W., Hoogenboom, G., Porter, C.H., et al., 2003. The DSSAT cropping
system model. European Journal of Agronomy 18, 235265.
Kaspar, T.C., Jaynes, D.B., Parkin, T.B., Moorman, T.B., 2007. Rye cover crop and
garnagrass strip effects on NO3 concentration and load in tile drainage. Journal
of Environmental Quality 36, 15031511.
Khoi, D.N., Suetsugi, T., 2012. Uncertainty in climate change impacts on stream
ow in Be River catchment, Vietnam. Water and Environmental Journal 26,
530539.
Kimball, B.A., Kobayashi, K., Bindi, M., 2002. Responses of agricultural crops to
free-air CO2 enrichment. Advances in Agronomy 77, 293368.
Kimball, B.A., LaMorte, R.L., Pinter Jr., P.J., et al., 1999. Free-air CO2 enrichment
(FACE) and soil nitrogen effects on energy balance and evapotranspiration of
wheat. Water Resources Research 35, 11791190.
Ko, J., Ahuja, L.R., Kimball, B., et al., 2010. Simulation of free air CO2 enriched
wheat growth and interactions with water,nitrogen, and temperature. Agricultural
and Forest Meteorology 150, 13311346.
Ko, J., Ahuja, L.R., Saseendran, S.A., et al., 2012. Climate change impacts on
dryland cropping systems in the Central Great Plains, USA. Climatic Change
111, 445472.
Li, C., Frolking, S., Frolking, T.A., 1992. A model of nitrous oxide evolution from
soil driven by rainfall events: I. model structure and sensitivity. Journal of
Geophysical Research 97, 97599776.
Li, C.S., Narayanan, V., Harriss, R.C., 1996. Model estimates of nitrous oxide
emissions from agricultural lands in the United States. Global Biogeochemical
Cycle 10, 297306.
Li, H., Qiu, J.J., Wang, L.G., et al., 2010. Modeling impacts of alternative
farming management practices on greenhouse gas emissions from a winter
wheatmaize rotation system in China. Agriculture, Ecosystems and Environment
135, 2433.
Li, Y., White, R.E., Chen, D.L., et al., 2007. A spatially referenced water and
nitrogen management model (WNMM) for (irrigated) intensive cropping systems
in the North China Plain. Ecological Modeling 203, 395423.
Liebig, M.A., Morgan, J.A., Reeder, J.D., et al., 2005. Greenhouse gas contributions
and mitigation potential of agricultural practices in northwestern USA and
western Canada. Soil and Tillage Research 83, 2552.
Long, S.P., Ainsworth, E.A., Leakey, A.D.B., Nosberger, J., Ort, D.R., 2006. Food for
thought: Lower-than-expected crop yield stimulation with rising CO2
concentrations. Science 312, 19181921.
Lugato, E., Zuliani, M., Alberti, G., et al., 2010. Application of DNDC
biogeochemistry model to estimate greenhouse gas emissions from Italian
agricultural areas at high spatial resolution. Agriculture, Ecosystems and
Environment 139 (4), 546556.
Ma, L., Ahuja, L.R., Ascough II, J.C., et al., 2000. Integrating system modeling with
eld research in agriculture: Applications of the Root Zone Water Quality Model
(RZWQM). Advances in Agronomy 71, 233292.
Ma, L., Malone, R.W., Heilman, P., et al., 2007. RZWQM simulation of long-term
crop production, water and nitrogen balances in Northeast Iowa. Geoderma 140,
247259.
MacDonald, R.J., Byrne, J.M., Boon, S., Klenzle, S.W., 2012. Modeling the potential
impacts of climate change on snowpack in the north Saskatchewan River
watershed, Alberta. Water Resources Management 26, 30533076.
Matthews, R.B., Stephens, W. (Eds.), 2002. Crop-Soil Simulation Models
Applications in Developing Countries. Wallingford: CABI.
Mo, X., Liu, S., Lin, Z.H., Guo, R.P., 2009. Regional crop yield, water
consumption and water use efciency and their responses to climate
change in the North China Plain. Agriculture, Ecosystems and Environment
134, 6778.
Morgan, J., Mosier, A., Milchunas, D., et al., 2004. CO2 enhances productivity,
alters species composition and reduces digestibility of shortgrass steppe
vegetation. Ecological Applications 14, 208219.
358
Ouyang, W., Qi, S., Hao, F., et al., 2012. Impact of crop patterns and cultivation on
carbon sequestration and global warming potential in an agricultural freeze zone.
Ecological Modeling 252, 228237.
Parton, W.J., Hartman, M.D., Ojima, D.S., Schimel, D.S., 1998. DAYCENT: Its land
surface submodel Description and testing. Global and Planetary Change 19,
3548.
Pattey, E.G., Edwards, C., Desjardins, R.L., et al., 2007. Tools for quantifying N2O
emissions from agroecosystems. Agricultural and Forest Meteorology 24,
103119.
Payne, J.T., Wood, A.W., Hamlet, A.F., Palmer, R.N., Lettenmaier, D.P., 2004.
Mitigating the effects of climate change on the water resources of the Columbia
River basin. Climatic Change 62, 233256.
Probert, M.E., Dimes, J.P., Keating, B.A., Dalal, R.C., Strong, W.M., 1998. APSIMs
water and nitrogen modules and simulation of the dynamics of water and
nitrogen in fallow systems. Agricultural Systems 56, 128.
Raque, R., Peichl, M., Hennessy, D., Kiely, G., 2011. Evaluating management
effects on nitrous oxide emissions from grasslands using the process-based
denitrication-decomposition (DNDC) model. Atmospheric Environment 45,
60296039.
Saseendran, S.A., Ahuja, L.R., Nielsen, D.C., Trout, T., Ma, L., 2008. Use of crop
simulation models to evaluate limited irrigation management options for corn in
a semiarid environment. Water Resources Research 44, W00E02. doi:10.1029/
2007WR006181.
Saseendran, S.A., Nielsen, D.C., Ma, L., Ahuja, L.R., Halvorson, A.D., 2004.
Modeling nitrogen management effects on a winter wheat cropping system using
RZWQM and CERES-wheat. Agronomy Journal 96, 615630.
Saseendran, S.A., Nielsen, D.C., Ma, L., et al., 2005. Effectiveness of RZWQM for
simulating alternative Great Plains cropping systems. Agronomy Journal 97,
11831193.
Smith, P., Martino, D., Cai, Z., et al., 2007. Agriculture. In: Metz, B., Davidson, O.
R., Bosch, P.R., Dave, R., Meyer, L.A. (Eds.), Climate Change Mitigation.
Contribution of Working Group III to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge and New York, NY:
Cambridge University Press, pp. 497540.
Snyder, C.S., Bruulsema, T.W., Jensen, T.L., Fixen, P.E., 2009. Review of
greenhouse gas emissions from crop production systems and fertilizer
management effects. Agriculture, Ecosystems and Environment 133, 247266.
Tanaka, S.K., Zhu, T., Lund, J.R., et al., 2006. Climate warming and water
management adaptation for California. Climatic Change 76 (34), 361387.
Thorp, K.R., Batchelor, W.D., Paz, J.O., Steward, B.L., Caragea, P.C., 2006.
Methodology to link production and environmental risks of precision nitrogen
management strategies in corn. Agricultural Systems 89, 272298.
Wang, G., Sun, J., Zhang, F., et al., 2011. Modeling impacts of farming
management practices on greenhouse gas emissions in the oasis region of
China. Biogeosciences 8, 23772390.
Wang, Z., Ficklin, D.L., Zhang, Y., Zhang, M., 2012. Impact of climate change on
streamow in the arid Shiyang River basin of northwest China. Hydrological
Processes 26, 27332744.
Relevant Website
http://www.ars.usda.gov/main/site_main.htm?modecode=54-02-15-00
United States Department of Agriculture.
Glossary
Cumulative distribution function (CDF) Probability
distribution with the possible value for the random value
sorted from minimum to maximum.
Multivariate distribution A probability distribution with
more than one random variable and they are related linearly
(or nonlinearly) to each other so that their correlation is not
zero.
Probability density function A schedule of probabilities
associated with alternative values of a random variable, for
example, a histogram or a bell-shaped curve.
Introduction
Simulation has existed since man rst started thinking through
alternative ways for doing things. Thinking logically through
solutions to problems is the most fundamental form of
simulation. The modern computer greatly advanced simulation by allowing us to use machines to rapidly crunch
through many different scenarios and provide summaries of
the possible outcomes. Until the advent of the microcomputer,
simulation models were relegated to universities and large
corporations that had access to mainframe computers and
programmers who developed simulation models using complex languages. With the introduction of Microsoft Excel
spreadsheets, the simulation world has changed and anyone
can now develop and utilize the power of simulation. Excel
has become the language that businesses and researchers use
to organize and process data. Simulation add-ins to Excel
made the art of simulation more accessible to the business
world, to students, and to researchers.
The purpose of this article is to introduce simulation as a
tool for analyzing data and making probabilistic forecasts of
variables that are not published or have risk about their forecasts. It is assumed that the reader is familiar with Microsoft
Excel as this is fast becoming the language for developing
simulation models and addressing risk in decision making.
Decision making in business and agriculture implies that
management has a choice among alternative actions. The alternative actions could be different combinations of crops to
produce, alternative production systems for crops or livestock,
or different marketing or nancial strategies for an agribusiness. If the decisions are to be made in a risk-free setting,
the manager can easily determine which strategy is the best
the one with the greatest economic return. When decisions are
made in a risky environment, the manager cannot use such a
simple rule because the economic return for each alternative is
a probability distribution of returns rather than a single value.
One approach to decision making under risk is to simulate
alternative strategies to estimate the distribution for each
1
2
3
To simulate Y, a simulation software package randomly samples the probability distribution for e many times (iterations)
doi:10.1016/B978-0-444-52512-3.00127-3
359
360
and each time it adds the stochastic value for e to the deterministic part of Y, which is a+bX. After each iteration, the Y
value is recorded and after many hundreds of iterations the
values for Y provide an estimate of the shape of the empirical
probability distribution for Y. By recalling, estimating the
shape of the empirical distribution for Y is the objective of
simulation.
Most simulation models are much more complex than
eqn [2]. The equations frequently have more than one
exogenous variable, the exogenous variables themselves may
be stochastic in addition to the stochastic error term, and there
may be hundreds of equations necessary to dene the system
being modeled.
KOVs
Intermediate results
tables and reports
Equations and calculations to
get values for reports
Exogenous and control variables
Identify all stochastic variables
Figure 1 Steps for designing a simulation model. KOVs, key output
variables.
4
361
150
50
50
150
250
350
5
6
8
9
where all variables in italics become stochastic variables because they are functions of the random variables that are in
bold.
The stochastic variables for the model are prices and yields
but by including them in eqns [5] and [8] it makes all of the
other variables stochastic as well. It is through this process that
the simulation model is able to forecast the probability distribution for prot. Note that the exogenous variables in the
model are acres, variable costs per unit, and xed costs. The
exogenous variables are control variables set by the analyst and
can be used for testing alternative scenarios.
The next step in model building is to assemble the calculated variables into reports and tables that are useful for
summarizing the models results. The receipts and expenses for
a business model logically are summarized in an income
statement which is followed by a cash ow statement and a
balance sheet. An example of these summary tables is provided
in the Appendix.
The nal step in programming a simulation model is to
develop reports using the KOVs. Reports can include tables
with the summary statistics (means, standard deviation, coefcient of variation, minimum, and maximum) for all of
the KOVs, and charts of the KOVs. Probability density charts
are very useful as they show that the KOVs are stochastic
(Figure 3). Cumulative distribution charts are frequently more
useful as we can read the probabilities of alternative outcomes
directly from the chart, for example, the probability that the
KOV is less than zero is 10% (Figure 4). The two gures depict
the results for the same output variable but the CDF is easier to
interpret.
Model verication of the completed simulation model
must be undertaken as soon as the model is completed.
Verication is the process used to test that every equation in
the model is functioning as intended. This means that testing
each equation to ensure that its independent variables come
from the appropriate cells in the worksheet, i.e., that crop
production is actually calculated using the cells that have acres
and yields for the correct crop and that the model does not
multiply sorghum yield and wheat acres. Each equation must
be checked to ensure that the variables are using the correct
time period (months, years, etc.) and that the equations are
not using crossing periods, i.e., yields in 2013 are used to
calculate production in 2013. After verifying all equations it is
recommended that a series of verication tests be used to
further verify the models ability to forecast the system being
analyzed.
362
0.6
0.5
0.4
0.3
0.2
0.1
0
150
50
50
150
Profit
250
350
10
11
Because the USD is always between zero and one, Y has to lie
between 10 and 20 on the number line and there is an equal
probability that Y will be in the interval of 12 and 14 or 16 and
18. The uniform distribution itself is not used to simulate a
random variable unless the shape of the distribution is completely unknown and we only know the minimum and
maximum.
The most popular distribution for simulating random variables is the normal distribution because it is easy to estimate the
parameters. For that reason many modelers take the easy route
and just assume the random variables are distributed normal.
Before making this assumption, tests for normality should be
applied to the random variables. The parameters for the normal
distribution are its mean and standard deviation and we denote
that a random variable Y is distributed normal as: Y~N(mean,
standard deviation). A normal distribution can be simulated
with the following equation:
Y~ Mean Standard Deviation SND
12
363
Y^ a b T
Y~ Y^ i 1 EMPS; F x; USD
13
14
15
17
18
364
19
365
0.9
0.8
0.7
Prob
0.6
0.5
0.4
0.3
0.2
0.1
0
200 000
100 000
100 000
200 000
300 000
NPV: 1
NPV: 2
400 000
NPV: 3
500 000
600 000
700 000
800 000
NPV: 4
Figure 5 CDFs of NPV for four scenarios. NPV, net present value.
Certainty equivalent
NPV: 3
NPV: 1
NPV: 2
NPV: 4
0.5
1
NPV: 1
1.5
2
RRAC
NPV: 2
2.5
NPV: 3
3.5
NPV: 4
366
0.02
90%
0.30
80%
0.37
0.41
70%
0.63
60%
50%
40%
30%
0.65
0.59
0.57
20%
0.35
10%
0%
0.04
0.05
0.03
NPV: 1
NPV: 2
NPV: 3
NPV: 4
Ball. All three have been on the market for some time and
have their faults and positive features. More information on
the three add-ins is available on their web sites.
In selecting a simulation add-in for Excel, the author recommends to seek out a package that meets your needs and is
easy (preferable intuitive) to use based on your mode of
working. The following is a checklist of features to look for in
selecting a simulation add-in for Excel:
Pseudorandom number generator: user-dened seed to
start the random number generator at the same place each
time so that every time a model is run it can return the
same stochastic results.
A nondegenerative random number generator: test the
random number generator by simulating 100 000 or more
USDs to make sure that the last 1000 are indeed distributed
U(0,1).
Random numbers simulated with a Latin hypercube procedure: the alternative sampling procedure is a Monte Carlo
procedure, which tends to under- and oversample the USD
and thus force one to simulate an obscenely large number
of iterations to achieve stable stochastic distributions.
Owing to a more efcient sampling procedure the Latin
hypercube can generate stable stochastic distributions with
less than 2000 iterations instead of tens of thousands with
a Monte Carlo procedure.
Large number of available probability distributions: analysts need not be limited to a small number of probability
distributions from which to simulate random variables.
The more distributions included in the software, the better.
Multivariate distribution capabilities: for reasons described
above, the add-in must have the capability to simulate
correlated USDs so that the model can simulate multivariate distributions without variance bias.
Copulas to simulate concordance between random variables: when random variables are related in a nonlinear
fashion, the model must have the capability to simulate
their concordance.
Regression and forecasting options included in the package:
it is more accurate and efcient to estimate OLS coefcients
and residuals in the simulation packages than to do it in a
second Excel add-in. In addition, forecasting packages
such as times series, exponential smoothing, seasonal indices, and moving averages are frequently needed in
simulation to estimate the residuals about the forecast for a
stochastic variable and to forecast means for the random
variables.
Parameter estimation capabilities for parametric and nonparametric distributions: parameter estimation for other
than the uniform and normal distributions requires the use
of method of moments or maximum likelihood estimators.
These parameter estimation procedures are beyond the
capabilities of most simulation modelers so they need to be
included in the simulation add-in.
Statistical tests for validating simulated variables: until the
random variables generated by a simulation model are
validated, the model should not be used for decision
making. Student-t and F or Chi-square tests as well as
multivariate validation tests must be included in the add-in
for ease of validating the stochastic variables.
Risk ranking tools: stochastic dominance, stochastic efciency, and StopLight charts are essential features in a
simulation add-in if the modeler wants to help the decision
maker select the best scenario.
Graphing capabilities that complement Excel: specialized
charts such as PDFs, CDFs, and Fan Graphs are helpful to
display the shapes of the simulated KOVs and for testing
the model.
367
Scenarios Analyzed
Both the US Congress, Senate and House Farm Bills discussed
previously were analyzed using the representative farms for the
following scenarios:
Senate Farm Bill assuming individual-level coverage selected in the Acreage Risk Coverage (ARC) program along
with Supplemental Coverage Option (SCO) analyzed with
the Food and Agricultural Policy Research Institutes
(FAPRI) January 2012 Baseline projections of sector-level
prices.
Senate Farm Bill assuming county-level coverage selected in
the ARC program along with SCO analyzed with FAPRI
sector-level prices.
House Farm Bill assuming Revenue Loss Coverage (RLC)
selected and analyzed with FAPRI sector-level prices.
368
Simulation Results
Results were presented in terms of which types of farms preferred which farm program option. For example, the results for
ranking the Senate bill are summarized in Table 1 in terms of
Table 1
Number of representative farms that would prefer
individual versus county-level coverage based on NCFI in the Senate
ARC Farm Bill package assuming FAPRI-projected prices
Total by Preferencea
Feedgrain/Oilseed
Wheat
Cotton
Rice
Investment Analysis
Individual coverage
County coverage
22
7
3
8
4
40
16
8
6
10
Two farms, the small Texas southern plains cotton farm TXSP2500 and the
Arkansas cotton farm ARNC5000, are 100% cotton and would only be enrolled in
STAX. Therefore, there would be no difference between the alternatives.
Abbreviations: ARC, Acreage Risk Coverage; FAPRI, Food and Agricultural Policy
Research Institute; NCFI, net cash farm incomes.
The numbers represent the benefit in terms of average 20132017 annual NCFI in ($1000)
from choosing the house PLC program over the most perferred plan from the
senate farm bill package. The house PLC program was preferred in all instances.
18.4
54.3
19.0
26.2
11.8
12.7
15.8
12.6
10.4
36.9
28.8
90.2
43.2
21.4
12.3
12.2
20.9
95.3
11.5
28.5
79.9
96.4
104.0
173.2
60.9
88.4
173.1
54.5
29.1
31.2
87.1
44.7
68.0
80.2
10.5
11.5
60.1
Farm type
Wheat
Legend
Cotton
Feedgrain
Rice
113.4
6.6
15.0
21.6
81.8
38.7
19.6
18.9
83.4
60.9
35.4
30.9
59.2
33.8
Red = House
Yellow = Senate
8.2
16.3
14.7
8.6
77.4
88.2
40.3
41.8
68.2
98.6 145.8
254.6
169.3
Figure 8 Results indicating the representative farms preference for the House over the Senate safety net package.
369
0.6
0.5
0.4
0.3
0.2
0.1
0
800 000
600 000
400 000
200 000
200 000
400 000
Figure 9 CDF of NPV for a ranch investment to demonstrate the probability of economic success.
balance sheet that would make up the majority of the equations for an investment model.) The stochastic variables are
often a bit more challenging as they are distributions for prices
of outputs, volume of sales, and costs of inputs or services
provided.
The rst investment simulation model developed by the
author was for an ice plant (Richardson and Mapp, 1976). It
was an early application for simulation of investments to appear in the agricultural economics literature and was the rst
to report a probability of economic success and a probabilistic
cash ow. The probability of success was dened to be the
probability of NPV being positive. The logic behind probability of success is that if NPV is positive, the investment
generates a return greater than the discount rate, which is the
investors opportunity cost of capital. The investor in this case
was concerned about the probability that cash ow from the
business would be large enough to provide a minimum cash
withdrawal, so the probability of positive cash ows was used
by the decision maker for evaluating the investment.
A simple investment decision model is presented in this
section to demonstrate how simulation can be used to
evaluate a risky investment. The investment is a beef cattle
ranch that has been in operation and the owner is considering
selling the ranch and investing in a business that has an internal rate of return of 5%, so the discount rate is 10% for the
problem. The ranch runs 500 mother cows and has an initial
herd of 90 replacement heifers and 25 bulls. The ranch raises
its own replacements by keeping 43% of the heifers each year.
Risks on the ranch include: prices for cattle (culled cows, heifer
calves, steer calves, culled replacement heifers, and culled
bulls); price for surplus hay; and prices for buying decit hay
and soybean meal. Production risks include: hay yields, calving rate; death rates for calves, replacement heifers; and sale
weights for heifers, steers, and culled replacement heifers.
The ranch has an initial net worth of $4.4 million and
an expected NPV of minus $47 000. The probability of
success from the stochastic analysis is 29% which can be read
from the CDF for NPV in Figure 9. The summary statistics
from simulating the ranch for 7 years are summarized in
Table 2. The probability of NCFI being negative grows over the
planning horizon as does the probability that EC is negative.
Insurance Analysis
Each year, crop farmers face with the problem of deciding
whether to purchase crop insurance or not, and if they purchase an insurance, then what level of coverage to purchase.
Crop insurance is quite complicated because it comes in many
different levels of yield protection and the cost is associated
with the level of coverage elected, and the premium subsidy
decreases as the level of coverage increases. By denition, crop
yields are risky, otherwise farmers would not be interested in
purchasing insurance against low yields. In addition to crop
yield insurance, farmers can also purchase a revenue insurance
policy that insures against low yields and low prices.
A farm simulation model can be used to analyze the economic benets of purchasing different levels of crop insurance.
The model can be a simple model that just compares the
economic returns for different insurance programs by simulating stochastic yields and indemnities and comparing the
indemnities to the premiums for alternative policies. Or a
complete farm simulation model can be used that has stochastic prices and yields for all crops and uses an income
statement, cash ow statement, and balance sheet to show the
economic consequences of alternative insurance policies on
the economic viability of the farm. If a whole farm simulation
model is available (see the Appendix), it is a simple task to add
the formulas to calculate premiums and indemnities for crop
insurance. The alternative policies being considered are simply
programmed as scenarios and the model is run once for each
insurance policy.
The results for simulating ve alternative crop insurance
options for a farm growing three crops are presented in this
section. The NPV CDFs for the ve insurance options are
370
Table 2
Mean
StDev
CV
Min
Max
Mean
StDev
CV
Min
Max
P(NCFIo0)
Mean
StDev
CV
Min
Max
P(ECo0)
NPV
(77 462)
133 646
(173)
(574 180)
338 152
4 165 828
131 643
3
3 678 634
4 571 859
NCFl 1
NCFl 2
NCFl 3
NCFl 4
NCFl 5
NCFl 6
NCFl 7
58 031
55 649
96
(84 133)
260 081
5%
61 271
54 481
89
(70 730)
192 390
14%
48 916
54 497
111
(90 462)
200 285
30%
24 893
57 743
232
(179 039)
186 790
48%
(15 953)
51 520
(323)
(170 604)
131 123
73%
(55 028)
53 380
(97)
(201 765)
89 865
93%
(101 906)
52 041
(51)
(237 800)
51 242
100%
EC 1
EC 2
EC 3
EC 4
EC 5
EC 6
EC 7
82 031
45 324
55
(50 043)
213 127
16%
68 848
62 784
91
(140 261)
215 082
15%
42 683
79 948
187
(209 254)
254 661
21%
2 515
100 278
3 988
(320 486)
268 987
34%
(77 482)
115 424
(149)
(447 128)
206 268
59%
(198 781)
138 797
(70)
(666 364)
151 167
84%
(369 909)
163 072
(44)
(949 746)
129 618
98%
1
0.9
0.8
0.7
Prob
0.6
0.5
0.4
0.3
0.2
0.1
0
600 000
400 000
NPV: 1
200 000
NPV: 2
200 000
NPV: 3
NPV: 4
400 000
600 000
NPV: 5
371
60 000.00
40 000.00
Certainty equivalent
20 000.00
NPV: 2
0.00
0
0.5
1.5
2.5
20 000.00
3.5
NPV: 4
4
4.5
NPV: 1
NPV: 3
40 000.00
60 000.00
80 000.00
100 000.00
NPV: 5
120 000.00
RRAC
NPV: 1
NPV: 2
NPV: 3
NPV: 4
NPV: 5
Figure 11 Stochastic efciency rankings of ve alternative crop insurance policies for a crop farm.
Technology Assessment
Technology assessment is another application of Monte Carlo
simulation. In the case of technology assessment the task is
two-fold: (a) prove that the technology is better than the
existing technology and (b) calculating the value of the technology to the adopter so that the technology can be priced to
extract the maximum rent to the technology owner. Technology assessments using simulation are not common in agriculture but can easily be done using simulation because
technology is often introduced to reduce risk and reduce costs
of production. If a technology is designed to reduce risk, then
simulation that explicitly incorporates risk is the appropriate
tool for assessing the benets of the technology. Examples of
risk-reducing technologies are: irrigation, drought-tolerant
plant varieties, salt-tolerant crops, GMO crops, fertilization,
and pest-control chemicals.
The example used here to demonstrate a simulation model
to assess alternative technologies was developed at Texas A&M
University for assessing the benets of alternative technologies
for small holder farms in developing countries. The economics
model is part of the Integrated Data Support System which
includes SWAT and APEX, which are biological models. APEX
is a daily plant growth model capable of simulating a crop
under alternative technologies using 30 years of weather data.
The resulting output is 30 years of yields for a crop with an
assumed technology/cultivation system. APEXs 30 years of
yields are used to estimate probability distributions of yields
for the base and alternative technologies that are used in the
economics model.
The economics model, FARMSIM, simulates a small holder
farm for 5 years using stochastic yields for the technologies
being analyzed and stochastic prices for crops and livestock.
Stochastic crop yields affect the quantity of feedstocks and
pasture conditions for the livestock to the extent that forage
from the crops are fed to livestock and pasture conditions are
stochastic based on weather variability. Family consumption is
restricted to raised crops and livestock products plus nutrients
purchased using available cash. If cash is limited and raised
nutrients are not available, the farm family suffers nutrient
deciencies. The KOVs in the FARMSIM model include the
normal variables for NPV, NCFI, ending cash, and nutrient
consumption for six nutrients. So, the FARMSIM model can
show the economic and nutritional benets of technology
adoption for a family.
The results from simulating a small holder farm in Ethiopia
are summarized in this section. The two technologies analyzed
are: (a) use of irrigation and fertilizer and (b) use of irrigation
plus adoption of fertilizer and improved seed varieties. A
StopLight chart in Figure 12 shows the probabilities that the
farm would have a cash ow shortage. There is a 34% chance
of ending cash being less than 20 000 Birr in the Baseline and
a zero chance of low ending cash under the two irrigation
scenarios. Under the Baseline, the familys average daily consumption of energy is less than a minimum 11% of the time
(Figure 13). This probability drops to zero for the alternative
technologies due to increased production of food.
The value of the alternative technologies can be estimated
using a risk ranking method called risk premiums. A risk
premium is the difference in the certainty equivalents for the
Baseline and an alternative technology. The certainty equivalents are calculated assuming a power utility function for all
RRACs between risk neutral and extremely risk averse in
Figure 14. The value of the irrigation and fertilizer technology
is slightly over 30 000 Birr and by adding improved seed,
the value of the technology is approximately 42 000 Birr over a
5-year planning horizon or almost 9000 Birr per year. The risk
premiums are constant across the risk-aversion levels so that
all risk-averse farmers would benet equally from adoption of
the two technologies.
372
0.00
90%
0.22
80%
70%
0.61
0.66
60%
50%
40%
0.78
30%
20%
0.39
0.34
10%
0%
Baseline
0.00
Baseline+N
0.00
Baseline+N+V
Figure 12 StopLight chart for comparing ending cash reserves under the base and two alternative technologies for a small holder farm in
Ethiopia. Birr (Ethiopian Birr Currency). N indicates the addition of fertilizer to its optimal level and V indicates the addition of improved seed
technology through selective breeding for varieties adapted to the local conditions.
0.01
0.28
80%
70%
60%
50%
40%
0.99
1.00
0.00
Baseline+N
0.00
Baseline+N+V
0.61
30%
20%
10%
0.11
0%
Baseline
Figure 13 StopLight chart for comparing average daily consumption of energy for an adult equivalent assuming the base technology and two
alternative technologies for a small holder farm in Ethiopia. N indicates the addition of fertilizer to its optimal level and V indicates the addition of
improved seed technology through selective breeding for varieties adapted to the local conditions.
Summary
Simulation is best suited for quantifying what if questions
and comparing probable outcomes for alternative actions. The
brief description and examples of simulation analyses presented in this article should serve as a starting point for students and researchers interested in applying simulation to
agricultural and natural resource issues. As demonstrated in
this article, the introduction of risk into a simulation model is
quite easily done and can be easily added to existing simulation models.
Agricultural and natural resource issues are particularly
suitable for analysis with Monte Carlo simulation because of
the strong inuence of weather and price risks on agriculture. If
one ignores risk in analyzing agricultural and natural resource
issues, decision makers do not have a complete picture of the
base situation or the projected consequences of actions they
may undertake. Many decision makers are surprised when the
outcomes they observe are different from the projections.
Simply including risk in simulation models used for analyzing
alternatives and making projection so that one can provide
373
45 000
Baseline+N+V
40 000
35 000
Baseline+N
30 000
25 000
20 000
15 000
10 000
5000
Baseline
0.5
1.5
2.5
3.5
4.5
RRAC
Baseline
Baseline+N
Baseline+N+V
References
Anderson, J.R., Dillon, J.L., 1992. Planning and managing farm systems under
uncertainty. In: FAO Farm Systems Management Series, Farm Management for
Asia: A Systems Approach. Rome: Food and Agriculture Organization of the
United Nations.
Clements, Jr., A.M., Mapp, Jr., H.P., Eidman, V.R. A Procedure for Correlating
Events in Farm Firm Simulation Models. Technical Bulletin T-131, Oklahoma
Agricultural Experiment Station, August 1971.
Food and Agricultural Policy Research Institute (FAPRI), 2012. U.S. Baseline Brieng
Book. Available at: http://www.fapri.missouri.edu/outreach/publications/2013/
FAPRI_MU_Report_01_13.pdf (accessed 01.10.13).
Hardaker, J.B., Richardson, J.W., Lien, G., Schumann, K.D., 2004. Stochastic
efciency analysis with risk aversion bounds: A simplied approach.
374
Appendix
Sample pro forma nancial tables for a simulation model
Income statement
Receipts
Corn market receipts
SB market receipts
Corn indemnity
SB indemnity
Total receipts
Expenses
Corn variable cost
SB variable cost
Corn harvest cost
SB harvest cost
Crop insurance premium
Land rent
Fixed costs
Operating interest
Land debt interest
Carryover debt interest
Total expense
Net cash farm income
2007
2008
2009
2010
2011
376 393
159 369
535 762
327 837
177 957
505 794
347 442
177 294
524 736
457 512
203 825
661 337
489 057
196 145
685 202
140 250
38 500
53 366
6 606
142 500
63 360
21 718
34 702
501 003
34 760
146 842
40 310
45 460
6 913
145 357
66 338
22 674
33 627
507 519
(1 725)
149 823
41 128
51 587
7 196
147 962
67 685
24 293
32 470
1 236
523 379
1 357
151 875
41 691
68 979
8 122
150 562
68 612
25 864
31 227
7 250
554 182
107 155
153 622
42 171
76 926
8 712
153 330
69 401
26 847
29 891
4 448
565 347
119 855
2008
2009
2010
2011
Cash ow statement
2007
65 000
34 760
1 950
101 710
44 764
(1 725)
1 343
44 382
1 357
1 357
107 155
107 155
119 855
119 855
14 344
40 000
1 738
864
56 946
44 764
15 419
40 802
56 221
(11 840)
16 576
11 840
41 533
68
70 017
(68 660)
17 819
68 660
42 263
5 358
14 823
148 922
(41 768)
19 156
41 768
43 040
5 993
19 141
129 097
(9 242)
Balance sheet
2007
2008
2009
2010
2011
44 764
1 050 000
1 094 764
1 102 500
1 102 500
1 157 625
1 157 625
1 215 506
1 215 506
1 276 282
1 276 282
448 355
448 355
646 409
432 936
11 840
444 775
657 725
416 360
68 660
485 020
672 605
398 541
41 768
440 308
775 198
379 385
9 242
388 627
887 655
Land debt
Cash ow decits
Total liabilities
Net worth
Introduction
For most companies, the introduction of successful new
products is critical to the achievement of the short- and longterm corporate strategic goals of protability, growth, and
continuity. As an illustration, more than 25% of the current
retail food sales in the US have been reported to consist of
products introduced within the past 5 years (Hughes, 1994).
Similarly, US marketing managers indicated that they expect
40% of the company prot made in 5 years time would come
from products not currently on the market (Booz et al., 1982).
Within the well-established product-market expansion matrix
for growth (Ansoff, 1957), new product development (NPD)
is identied as one of the important growth strategies of the
rm.
Despite the fact that successful NPD is crucial to protability and growth ambitions, the actual success rates of new
product introductions are fairly disappointing. Although there
is a lack of reliable data on actual success and failure rates,
reported failure rates are ranging anywhere between 40% (e.g.,
Barczak et al., 2009) and as high as 90% (e.g., Gourville,
2006). One reason for this lack of insight into actual success
and failure rates stems from how success rates are being dened (Castellion and Markham, 2013). Success rates have
been expressed as the percentage of commercialized new
products that not only meet their marketing (e.g., market share
and prot contribution) objectives, but also relative to the
number of initial ideas that have entered the NPD selection
process. Research on the 2003 the Product Development and
Management Association best practices study (Barczak et al.,
2009) suggests that approximately 15% of the new product
ideas and approximately 60% of the new products actually
introduced into the market place make it to a commercial
success in the market.
Whatever the exact metric and the exact percentage be,
failure rates of new product introduction are an important
concern to academics and practitioners alike, as new product
introductions require substantial up-front investments that are
not necessarily recouped from the new products nancial
returns.
Bottom-line, NPD is an activity that is both necessary in
light of market turbulence, but at the same time quite uncertain and risky in terms of potential failure. Not surprisingly,
the NPD process has received a lot of attention in the marketing and management literatures (see Hart, 1996 for an
overview).
Market turbulence
The need for NPD essentially arises from market turbulence on
both the demand and the supply side (Van Trijp and Steenkamp, 2005). Consumer needs are subject to change over
time, as are the specic ways in which consumers seek to
satisfy these needs through the purchase and consumption of
specic products (demand). Such changes may occur as a
result of demographic, socio-economic, and cultural changes
in society.
Turbulence also occurs at the supply side of the market.
Changes in the political and legal environment trigger NPD
through new requirements from (food) laws and regulations
(e.g., increased minimal levels of animal welfare). Changes in
the economic environment, such as increased or reduced
purchasing power of consumers, will trigger innovation and
development of new products that will deliver similar consumer benets, but at a lower cost. Business strategies in terms
of internal resources and business objectives also trigger innovation and predetermine in which categories and directions
such innovation is to be found. Importantly, breakthroughs in
(food) technology may provide new and unprecedented opportunities to both deliver new product-related benets to the
consumer and deliver existing benets more effectively and
efciently. Finally, much of innovation activity is triggered by
changes in the competitive environment, as new products
introduced by competitors may change consumers value
perception of existing products in the market place. Together
these developments create a highly dynamic context in which
companies operate and compete for consumer loyalty.
doi:10.1016/B978-0-444-52512-3.00062-0
375
376
Sales and
profits ($)
Sales
Profits
Time
Product
development
Losses/
investment ($)
Figure 1 The product life cycle.
Introduction
Growth
Maturity
Decline
377
There has been a lot of research into the success and failure
factors of NPD. Much of this research is generic in nature with
only a limited number of studies focusing specically on NPD
success factors in food (see Stewart-Knox and Mitchell, 2003;
Kristensen et al., 1998 for exceptions). Research on success and
failure factors has essentially progressed along three dominant
approaches.
378
Technology
(R&D)
Yellow colour
Superior
value
fulfilment
Superior
benefit
delivery
Unique
attribute
perception
Pleasure in life
Nice taste
Creamy
Communication
(Marketing)
Packaging
End
Consumer
Means
Product
Figure 2 Products as a means to an end. Adapted from Van Trijp, J.C.M., Steenkamp, J.E.B.M., 2005. Consumer-oriented new product
development: Principles and practice. In: Jongen, W.M.F., Meulenberg, M.T.G. (Eds.), Innovation in Agri-Food Systems: Product Quality and
Consumer Acceptance. Wageningen: Wageningen Academic Press, pp. 87124.
Want formation
Inference formation
Personality
Values
Technology
features
Desired
product
benefits
Goals
379
Inferred
product
benefits
Attribute
perceptions
Product
features
Marketing
features
Situations
Trial/
choice preference
Experienced
product benefits
Repeat
Purchase
Formation of trial and repeat intentions
Figure 3 A simplied framework of how consumers decide on new products.
values) and situational factors (e.g., goals). Inference formation deals with how the consumer forms expectations
about which attributes the product has and which benets
these attributes are believed to bring about for him/her inferred from available cues. Finally, formation of intentions for
trial and repeat deals with how the comparison of wanted and
inferred benets leads, in comparison to the price of the
product, to an intention to make a rst-time purchase of the
product, and how the subsequent experience with the product
will affect intentions to keep on buying the product or not.
380
human beings, but people will differ in the relative weight they
attach to these values. Values have been used widely to explain
consumer choices (e.g., Beatty et al., 1985; Kahle, 1986;
Kamakura and Mazzon, 1991), but their main advantage,
namely that they are stable across situations and time, is also a
disadvantage: abstract values, while often related to specic
product choices, are relatively weak predictors of such specic
behaviors, which are inuenced by a host of other likewise
more specic factors. Values provide the enduring motivational aspects of consumer wants, but to explain consumer
choice, they will usually have to be supplemented by other
factors taking into account situational factors.
Goals have a higher degree of specicity than values, and
they have a situational component. When buying food, a
consumer can have a goal of pleasing the family, of rewarding
himself, of losing weight, or a host of other things. A goal of
pleasing the family will be linked to underlying values, like
benevolence and security, but will also have a situational
component, as pleasing the family is not relevant, for example,
when buying food in the canteen of ones workplace. Several
goals can and mostly will be salient with regard to any particular food choice, and they can be in conict with each other,
such as when a goal of losing weight conicts with a goal of
rewarding oneself with a pleasurable experience. Developing
products that solve goal conicts is one important avenue to
pursue in NPD in the food sector.
People differ in which goals are usually dominant when they
choose food, and instruments have been developed to measure
these differences and segment consumers accordingly. The foodrelated lifestyle approach has been a popular approach to this
end (Bruns et al., 2004; Grunert et al., 2001). Food-related
lifestyle designates different ways in which people use food to
attain life values and leads to generic consumer types that differ
with regard to dominant goals and ways of shopping, meal
preparation, and eating. The generic types identied are the
uninvolved consumers, who are really not very interested in
food, the careless consumers, who emphasize novelty and
convenience, the conservative consumer, who puts priority on
traditional meals and generally uses eating to establish a sense
of security, the adventurous consumer, with an emphasis on
social and innovative goals in preparing and eating meals, and
nally the rational consumer, who has a reasoned approach to
food choice and values healthfulness highly. This instrument
has been popular in Europe and has even been applied in
China (Grunert et al., 2011).
Goals thus point at desired benets that the consumer
wants to get out of the product to be bought. Desired benets
can be many things, but from social dilemma theory (Van
Lange et al. (2013) and Construal Level Theory (CTL) (Trope
et al., 2007), it is suggested that they can meaningfully be
classied as to whether they deliver benet to the self or to
others, and whether they deliver direct gratication or delayed
gratication (e.g., Van Trijp and Fischer, 2011). Directly
gratifying self-oriented benets include the sensory properties
of the food, its convenience, and its price. Self-oriented
delayed benets include the health value of products. Otherdirected benets with relatively direct reinforcement value
include motivations of local production to stimulate regional
economic development and animal welfare motivations.
Delayed, other-directed benets include sustainability
381
382
Market orientation
The importance of market orientation as a driver of company
performance and success in the market place is one of the best
established ndings within the marketing literature (see Kirca
et al., 2005 for a review). Market orientation involves the organizational norms and values to behave consistent with market orientation, as evidenced in closely monitoring customers
and competitors with a focus on inter-functional coordination
within the company (Narver and Slater, 1990). The behavioral
perspective on market orientation (e.g., Kohli and Jaworski,
1990) emphasizes the activities of generation of information
about customers and the market place, the dissemination of this
information across different functional disciplines within the
company, and use of this information as a basis for a coordinated and responsive marketing approach and market offering. Market orientation enhances a companys performance
through a higher level of innovativeness, which serves as a basis
for customer loyalty and perceived product quality delivered to
the market place (Kirca et al., 2005). Market orientation has
both a responsive (aligning with existing consumer needs and
wants) and a proactive (addressing latent and emerging consumer needs) component to it (Narver et al., 2004), and hence
forms a strong basis for NPD.
(6)
Relations
among
product features
Consumer
needs and
desires
(1)
Rel. importance
(2)
Relations
between
Consumer
consumer needs/desires
perception
and
technical product features
(4)
(6)
(3)
Technical specifications
(5)
Figure 4 The House of Quality within Quality Function Deployment. Adapted from Van Trijp, J.C.M., Steenkamp, J.E.B.M., 2005. Consumeroriented new product development: Principles and practice. In: Jongen, W.M.F., Meulenberg, M.T.G. (Eds.), Innovation in Agri-Food Systems:
Product Quality and Consumer Acceptance. Wageningen: Wageningen Academic Press, pp. 87124.
2.
3.
4.
5.
383
384
Opportunity identification
Development
Optimization
Launch
Technological
opportunity
Concept
generation
Concept
development
Product
design
Productconcept design
Full marketing
design
Launch
to market
Customer
needs
Fuzzy
front-end
methods
Idea
screening
Concept
testing
Product
testing
ProductConcept
testing
Test
market
Performance
monitoring
Concluding Remarks
As started off this article by stating that NPD is a necessary yet
high risk activity for the rm. However, throughout this article
it has been argued that this risk can, at least to some extent be
managed. Authors provided evidence that consumer relevance
of the product advantage and market orientation throughout
the process are key identied factors for NPD process. Authors
developed a simplied model of how consumers make decisions regarding (new) product decisions, and used this as a
basis for consumer-oriented NPD. Incorporating this consumer perspective throughout a structured and well-executed
NPD process enhances the changes of NPD success.
References
Ansoff, H.I., 1957. Strategies for diversication. Harvard Business Review 35,
113124.
Atuahene, G., Evangelista, F., 2000. Cross-functional inuence in new product
development: An exploratory study of marketing and R&D perspectives.
Management Science 46, 12691284.
Barczak, G., Grifn, A., Kahn, K.B., 2009. Perspective: Trends and drivers of success
in NPD practices: Results of the 2003 PDMA best practice study. Journal of
Product Innovation Management 26, 323.
Beatty, S.E., Kahle, L.R., Homer, P., Misra, S., 1985. Alternative measurement
approaches to consumer values: The list of values and the Rokeach value survey.
Psychology and Marketing 2, 181200.
Berkhout, A.J., Van der Duin, P.A., 2007. New ways of innovation: An application of
the cyclic innovation model to the mobile telecom industry. International Journal
of Technology Management 40 (4), 294309.
Booz, Allen, and Hamilton, 1982. New Product Management for the 1980s. New
York: Booz, Allen, and Hamilton.
Bruns, K., Bredahl, L., Grunert, K.G., Scholderer, J., 2005. Consumer perception of
the quality of beef resulting from various fattening regimes. Livestock Production
Science 94, 8393.
Bruns, K., Scholderer, J., Grunert, K.G., 2004. Closing the gap between values and
behavior a means-end theory of lifestyle. Journal of Business Research 57,
665670.
385
Castellion, G., Markham, S.K., 2013. New product failure rates: inuence
of Argumentum ad Populum and self-interest. Journal of Product Innovation
Management 30 (5), 976979.
Cooper, R.G., 1999. From experience the invisible success factors in new product
innovation. Journal of Product Innovation Management 16 (2), 115133.
Cooper, R.G., Kleinschmidt, E.J., 1995. Benchmarking the rms critical success
factors in new product development. Journal of Product Innovation Management
16, 115133.
Costa, A.I.A., Dekker, M., Jongen, W.M.F., 2001. Quality function deployment in
the food industry: A review. Trends in Food Science and Technology 11,
306314.
Costa, A.I.A., Jongen, W.M.F., 2006. New insights into consumer-led food product
development. Trends in Food Science and Technology 17, 457465.
Darby, M.R., Karni, E., 1973. Free competition and the optimal amount of fraud.
Journal of Law and Economics 16, 7388.
Eliashberg, J., Lilien, G.L., Rao, V.R., 1997. Minimizing technological oversight: A
marketing research perspective. In: Garud, R., Nayyar, P.R., Shapira, Z.R. (Eds.),
Technological Innovation: Oversights and Foresights. New York: Cambridge
University Press, pp. 214230.
Evanschinsky, H., Eisend, M., Calantone, R.J., Jiang, Y., 2012. Success factors of
product innovation: An updated meta-analysis. Journal of Product Innovation
Management 29 (S1), 2137.
Fishbein, M., Ajzen, I., 1975. Belief, Attitude, Intention and Behavior. Reading, MA:
Addison-Wesley.
Frewer, L.F., Lassen, J., Kettlitz, B., et al., 2004. Societal aspects of genetically
modied foods. Food and Chemical Toxicology 42, 11811193.
Gatignon, H., Robertson, T., 1991. Innovative decision processes. In: Robertson, T.,
Kassarjian, H. (Eds.), Handbook of Consumer Behavior. Englewood Cliffs, NJ:
Prentice Hall, pp. 316348.
Gielens, K., Steenkamp, J.B.E.M., 2007. Drivers of consumer acceptance of new
packaged goods: An investigation across products and countries. International
Journal of Research in Marketing 24, 97111.
Gourville, J.T., 2006. Eager sellers and stony buyers: Understanding the psychology
of new product adoption. Harvard Business Review 84 (6), 98106.
Grifn, A., Hauser, J.R., 1993. The voice of the customer. Marketing Science 12 (1),
127.
Grunert, K.G., 2005. Food quality and safety: Consumer perception and demand.
European Review of Agricultural Economics 32, 369391.
Grunert, K.G., 2010. Means-end chains a means to which end? Marketing
Journal of Research and Management 6, 3038.
Grunert, K.G., Baadsgaard, H., Larsen, H., Masden, T.K., 1996. Market Orientation in
Food and Agriculture. Boston, MA: Kluwer Academic Publishers.
Grunert, K.G., Bruns, K., Bredahl, L., Bech, A.C., 2001. Food-related lifestyle: A
segmentation approach to European food consumers. In: Frewer, L.J., Risvik, E.,
Schifferstein, H.N.J. (Eds.), Food, People and Society: A European Perspective of
Consumers Food Choices. London: Springer, pp. 211230.
Grunert, K.G., Harmsen, H., Larsen, H.H., Sorensen, E., Bisp, S., 1997. New areas
in agricultural and food marketing. In: Wierenga, B., Van Tilburg, A.,
Grunert, K.G., Steenkamp, J.B.E.M., Wedel, M. (Eds.), Agricultural Marketing and
Consumer Behavior in a Changing World. Boston, MA: Kluwer Academic
Publishers, pp. 330.
Grunert, K., Perrea, T., Zhou, Y., et al., 2011. Is food-related lifestyle (FRL) able to
reveal food consumption patterns in nonWestern cultural environments? Its
adaptation and application in urban China. Appetite 56, 357367.
Gutman, J., 1982. A means-end chain model based on consumer categorization
processes. Journal of Marketing 46, 6072.
Gutman, J., 1997. Means-end chains as goal hierarchies. Psychology & Marketing
14, 545560.
Hart, S., 1996. New Product Development: A Reader. London: The Dryden Press.
Hauser, J.R., Clausing, D., 1988. The house of quality. Harvard Business Review 66
(3), 6373.
Henard, D.H., Szymanski, D.M., 2001. Why some new products are more successful
than others. Journal of Marketing Research 38, 362375.
Hofmeister, K.R., 1991. Quality function deployment: Market success through
customer-driven products. In: Graf, E., Saguy, I.S. (Eds.), Food Product
Development. New York: Van Nostrand Reinhold, pp. 189210.
Hughes, D., 1994. Breaking with Tradition: Building Partnerships and Alliances in
the European Food Industry. Wye: Wye College Press.
Kahle, L.R., 1986. The nine nations of North America and the value basis of
geographic segmentation. Journal of Marketing 50, 3747.
Kamakura, W.A., Mazzon, J.A., 1991. Value segmentation: A model for the
measurement of values and value systems. Journal of Consumer Research 18,
208218.
386
Kardes, F.R., Posavac, S.S., Cronley, M.L., 2004. Consumer inference: A review of
processes, bases, and judgment contexts. Journal of Consumer Psychology 14
(3), 230256.
Kaul, A., Rao, V., 1995. Research for product positioning and design decisions: An
integrative review. International Journal of Research in Marketing 12 (4),
293320.
Kirca, A.H., Jayachandran, S., Bearden, W.O., 2005. Market orientation: A metaanalytic review and assessment of its antecedents and impact on performance.
Journal of Marketing 69 (April), 2441.
Kohli, A., Jaworski, B., 1990. Market orientation: The construct, research
propositions, and managerial implications. Journal of Marketing 54 (2), 118.
Kristensen, K., Ostergaard, P., Juhl, H.J., 1998. Success and failure of product
development in the Danish food sector. Food Quality and Preference 9,
333342.
Lancaster, K., 1966. A new approach to consumer theory. Journal of Political
Economy 74, 567585.
Lilien, G.L., Morrison, P.D., Searls, K., Sonnack, M., Von Hippel, E., 2002.
Performance assessment of the lead user idea-generation process for new
product development. Management Science 48 (8), 10421059.
MacFie, H. (Ed.), 2007. Consumer-led Food Product Development. Cambridge:
Woodhead Publishing Limited.
Miller, K.M., Hofstetter, R., Krohmer, H., Zhang, J., 2011. How should consumers
willingness to pay be measured? An empirical comparison of state-of-the-art
approaches. Journal of Marketing Research 48 (1), 172184.
Narver, J.C., Slater, S.F., 1990. The effect of market orientation on business
protability. Journal of Marketing 54 (3), 2035.
Narver, J.C., Slater, S.F., MacLachlan, D.L., 2004. Responsive and proactive market
orientation and new product success. Journal of Product Innovation Management
21, 334347.
Ozer, M., 1999. A survey of new product evaluation models. Journal of Product
Innovation Management 16, 7794.
Padel, S., Foster, C., 2005. Exploring the gap between attitudes and behavior:
Understanding why consumers buy or do not buy organic food. British Food
Journal 107, 606625.
Reynolds, T.J., Gutman, J., 1988. Laddering theory, method, analysis and
interpretation. Journal of Advertising Research 28 (1), 1131.
Rogers, E.M., 1995. Diffusion of Innovations. New York: The Free Press.
Ronteltap, A., Van Trijp, H.C.M., Renes, R.J., Frewer, L.J., 2007. Consumer
acceptance of technology-based food innovations: Lessons for the future of
nutrigenomics. Appetite 49, 117.
Rozin, P., 1976. The selection of foods by rats, humans, and other animals. In:
Lehrman, D., Hinde, R.A., Shaw, E. (Eds.), Advances in the Study of Behavior,
vol. 6. New York: Academic Press, pp. 2176.
Scholderer, J., Frewer, L.J., 2003. The biotechnology communication paradox:
Experimental evidence and the need for a new strategy. Journal of Consumer
Policy 26, 125157.
Schwartz, S.H., 1992. Universals in the content and structure of values: Theoretical
advances and empirical tests in 20 countries. In: Zanna, M.P. (Ed.), Advances in
Experimental Social Psychology, vol. 25. San Diego, CA: Academic Press,
pp. 165.
Schwartz, S.H., Bilsky, W., 1987. Toward a universal psychological structure of
human values. Journal of Personality and Social Psychology 53, 550562.
Selnes, F., Troye, S.V., 1989. Buying expertise, information search, and problem
solving. Journal of Economic Psychology 10, 411428.
Siegrist, M., 2008. Factors inuencing public acceptance of innovative food
technologies and products. Trends in Food Science and Technology 19,
603608.
Souder, W.E., Chakrabarti, A.K., 1978. The R&D/Marketing Interface: Results from an
empirical study of innovation projects. IEEE Transactions on Engineering
Management, EM 25, 8893.
Steenkamp, J.B.E.M., 1990. A conceptual model of the quality perception process.
Journal of Business Research 21, 309333.
Steenkamp, J.B.E.M., Gielens, K., 2003. Consumer and market drivers of the trial
probability of new consumer packaged goods. Journal of Consumer Research 30,
368384.
Steenkamp, J.B.E.M., Van Trijp, H.C.M., Ten Berge, J.M.F., 1994. Perceptual
mapping based on idiosyncratic sets of attributes. Journal of Marketing Research
31 (February), 1527.
Steenkamp, J.B.E.M., Van Trijp, H.C.M., 1996a. Quality guidance: A consumer-based
approach to food quality improvement using partial least squares. European
Review of Agricultural Economics 23, 195215.
Steenkamp, J.B.E.M., Van Trijp, H.C.M., 1996b. Task experience and validity in
perceptual mapping: A comparison of two consumer adaptive techniques.
International Journal of Research in Marketing 13 (3), 265276.
Steenkamp, J.B.E.M., Van Trijp, H.C.M., 1997. Attribute elicitation in consumer
research: A comparison of three methods. Marketing Letters 8 (2), 153165.
Stewart-Knox, B., Mitchell, P., 2003. What separates the winners from the losers in
new product development. Trends in Food Science and Technology 14, 5864.
Szymanski, D.M., Kroff, M.W., Troy, L.C., 2007. Innovativeness and new product
success: Insights from the cumulative evidence. Journal of the Academy of
Marketing Science 35, 3552.
Trope, Y., Liberman, N., Wakslak, C., 2007. Construal levels and psychological
distance: Effects on representation, prediction, evaluation, and behavior. Journal
of Consumer Psychology 17, 8395.
Trott, P., 2008. Innovation Management and New Product Development, fourth ed.
Harlow: Prentice Hall.
Urban, G.L., Hauser, J.R., 1993. Design and Marketing of New Products, second ed.
Englewood Cliffs, NJ: Prentice Hall.
Van Ittersum, K., Pennings, J.M.E., Wansink, B., Van Trijp, H.C.M., 2007. The
validity of attribute-importance measurement: A review. Journal of Business
Research 60, 11771190.
Van Kleef, E., Van Trijp, H.C.M., Luning, P., 2005. Consumer research in the early
stages of new product development: A critical review of methods and techniques.
Food Quality and Preference 16, 181201.
Van Lange, P.A.M., Joireman, J.A., Parks, C.D., Van Dijk, E., 2013. The psychology
of social dilemmas: A review. Organizational Behavior and Human Decision
Processes 120, 125141.
Van Trijp, H.C.M., Fischer, A.R.H., 2011. Mobilizing consumer demand for
sustainable development. In: Van Latesteijn, H., Andeweg, K. (Eds.), The
TransForum Model: Transforming Agro Innovation Toward Sustainable
Development. Dordrecht, Heidelberg, London, New York: Springer Science
+Business Media B.V., pp. 7397.
Van Trijp, J.C.M., Steenkamp, J.E.B.M., 2005. Consumer-oriented new product
development: Principles and practice. In: Jongen, W.M.F., Meulenberg, M.T.G.
(Eds.), Innovation in Agri-Food Systems: Product Quality and Consumer
Acceptance. Wageningen: Wageningen Academic Press, pp. 87124.
Van Trijp, H.C.M., Van Kleef, E., 2008. Newness, value and new product
performance. Trends in Food Science and Technology 19, 562573.
Venkatesh, V., Morris, M.G., Davis, G.B., Davis, F.D., 2003. User acceptance of
information technology: Toward a unied view. MIS Quarterly 27 (3), 425478.
Walker, B.A., Olson, J.C., 1991. Means-end chains: Connecting products with self.
Journal of Business Research 22, 111118.
Glossary
Case of illness An individual person who acquires a
disease or illness associated with an epidemiologically
signicant exposure.
Critical Tracking Event A physical point in the food
supply chain where an operator identies a minimum set of
event data to systematically collect, typically consisting of
three basic data items: unique location/Event ID, unique
Item ID, and date/time.
Food supply chain A sequence of processes involved in
the production and distribution of food.
Global Trade Identication Number (GTIN) An identier
for trade items used to lookup product information in a
database or between databases.
Introduction
Foodborne outbreaks represent a signicant burden of illness
in the United States and internationally causing signicant
morbidity and mortality (Scallan et al., 2011; Kuchenmller
et al., 2009). Although the majority of these illnesses are of an
unknown etiology, a signicant number are associated with
commercially distributed foods. As the complexity and speed
of the food supply increases, private industry, government
regulators, and public health ofcials have been challenged in
tracing potentially implicated foods during and after foodborne illness outbreaks. Notable examples include outbreaks
associated with spinach, peanut butter, shell eggs, fresh produce, and pet food (Wendel, 2009; Medus et al., 2009;
Cavallaro et al., 2011; Braden, 2006; Anonymous, 2010).
As a result of these outbreaks, improved recordkeeping and
traceability requirements were included in the landmark passage of the Food Safety Modernization Act in January of 2011.
This Act specically required the Food and Drug Administration to establish pilot projects to explore and evaluate
methods to rapidly and effectively identify recipients of food
to prevent or control a foodborne illness outbreak.
Surprisingly to many, the primary goal of food traceability
is not food safety. The primary goal of food traceability is to
improve investigational efciency. Specically, the goal of
improving food traceability is to improve the speed of investigations as well as the accuracy of results. Therefore, the
problem of food traceability requires a mindset that is rst
rooted in logistics rather than food safety. Certainly, achieving
improvements in food traceability will more likely result in
fewer cases of foodborne illness, reduction in the amounts of
otherwise wholesome foods discarded, as well as added protection of industry segments and/or product brands from erroneous implication in outbreaks. Also, increasing the number
of successful outbreak investigations will lead to more
doi:10.1016/B978-0-444-52512-3.00047-4
387
388
External traceability
Distributor/
wholesaler
Food
manufacturer
Product
Retail
location
Figure 1 Example of external traceability. A food manufacturer produces a product and tracks the distribution of that product to a distribution
and retail location.
Internal traceability
Ingredient
A
Ingredient
B
Manufacturing
process
Product
lot A
Ingredient
C
An Example Investigation
Traceability, in order to protect public health, should encompass all aspects of the food system, starting at the point of
harvest and continuing to retailers. Animal feed, as well as
food packaging, should also be included in a robust food
chain traceability system.
Numerous foodborne outbreaks over the past several years
have demonstrated the importance and need for rapid traceability of food products sold to consumers. More rapid traceability can aid and clarify foodborne illness investigations by
aligning product distribution data with epidemiological exposure data. These investigations could be completed more
rapidly and with a greater degree of accuracy if current data
389
Traditional epidemiology
Hypothesis supporting traceback
Figure 3 Conceptual diagram of a hypothesis supporting traceback investigation. PFGE, pulse eld gel electrophoresis.
regulatory agency based on record collection and in-eld investigations. An investigation of the invoices and bills-oflading from each restaurant location where a case of illness
was reported shows that each restaurant received their sprouts
from a different supplier. Further investigation of the records
from the suppliers shows that they received their sprouts from
a number of different growers. A review of the grow logs, seed
sources, and invoices at each of the sprout grower locations
shows that all of the seed in implicated time frame would have
come from a single seed-supply company. A review of the lot
codes for the implicated seeds shows that a common lot-code
of seed was used at each grower in the implicated time frame
and further investigation shows that the lot-code corresponds
to a single farm that produced all of the questionable seed.
It is not until all of these data are collected and analyzed
that a truly meaningful public health intervention, in the form
of seed and sprout recalls and a market withdrawal of the
implicated lot-code, can be made. As might be imagined, such
an investigation is complicated and time- and resourceintensive. Outbreaks often subside before investigators are
able to pinpoint a cause resulting in wasted time and effort of
both doing the investigating and those being investigated.
Traceforward Investigations
Traceforward, sometime called tracking, is the capability to
nd a product based on specic criteria while it is handled
along each point of the supply chain. This is a critical feature
of any traceability system because companies must be able to
identify and locate their products within the supply chain in
order to withdraw or recall them whenever necessary. Once a
food item or ingredient has been associated with illness, improving forward traceability through the channels of
390
distribution can prevent further consumer exposure and additional cases of illness. Additionally, labeling on consumer
packaging for manufactured foods with information containing lot or batch codes will allow consumers to easily
identify products in their homes that may be associated with a
recall or outbreak.
One-Forward-One-Back
Currently, food traceability revolves around the concept of
OFOB, which is often also referred to as one-up and onedown. This approach is popular because it does not require
operators to do anything other than to maintain customary
business records that virtually all responsible operators already
maintain without the additional consideration of food traceability. The concept of OFOB requires that each operator be
able to determine, within a reasonable amount of time and
typically within 24 h, the identities and locations of immediate suppliers and customers. Production records, purchase
orders, sales orders and invoices, as well as shipping and receiving records substantially satisfy the basic food traceability
requirements of OFOB. From the perspective of the operator,
OFOB works and requires little if any additional investment
other than what might normally enhance business productivity in terms of improving efciency of data storage and retrieval. Without even considering traceability, responsible
operators already maintain a variety of important business
process records such as payroll, production, receiving, shipping, sales orders, invoices, purchase orders, inventory, and
quality-control data. As mentioned, most of these data are
only useful to food outbreak investigators after likely sources
of contamination have been identied.
Indeed, OFOB does work, but the problem is that it is slow,
inefcient, and often ineffective for investigators, resulting in
too many unsolved outbreaks, implication of incorrect products, unnecessary damage to industries and brands, and waste
of enormous quantities of otherwise wholesome foods. A
better understanding of the investigative and recall processes
helps to expose why OFOB is more likely to be incapable
391
392
provides a basis for exibility, scalability, adaptability, efciency, and interconnectivity with little requirement for enforcing specic standards on any operator. CTE promises to do
for food traceability what hazard analysis critical control point
(HACCP) has done for food safety. The key concept is that
each operator knows their operation best and operators are in
the best position to identify those events that are critical to the
overall goal of food traceability. The CTE concept simplies
the large, complex, and seemingly intractable problem into a
local and familiar series of events that are deemed critical to
tracking items through an operation. Each operator properly
identies their own CTEs and commits to collecting a minimum set of event data for each CTE, typically consisting of a
three basic data items including unique location/event ID
(e.g., Receiving Door #2 at a given physical address), unique
item ID, and date/time stamp. Each operator would collect
event data from all of their CTEs and store them as they see t
in secure databases that may be accessed for query by properly
authorized personnel. This simple structure leads directly to
the possibility of authorized investigators being capable of
generating reports showing locations, dates, and times,
throughout the entire supply chain, of suspect food items and
ingredients, virtually instantaneously and with minimal intrusion and bother to operators. When multiple traceback
queries expose points of convergence in the supply chain, investigators can then focus their attention on the broader process and handling data of the implicated operator in order to
attempt to identify the source of contamination.
As with HACCP, the CTE framework does not prescribe any
particular method or technology for doing so. Operators are
free to choose the methods and/or technologies that best suit
their purposes. The beauty of the CTE framework is that it is
simple, exible, scalable, secure, and efcient and does not
require immediate universal participation in order to benet
from the system. As operators adopt the CTE concept into their
operations, the food supply chains will become increasingly
traceable. Additionally, modern distributed data networks
preclude any requirement for pushing or uploading CTE data
to any central repository, government, database, or authority.
The CTE concept permits operators to maintain ownership and
control of their own CTE data. As unique traceability codes can
only be linked to proprietary production-related data such a
lot/batch codes, CTE offers a level of security through data
abstraction. This means that unique traceability codes have
no inherent meaning. They simply point to a richer set of
meaningful data in properly secured databases. Table 1 depicts
the conceptual relationship between HACCP and CTE.
Data Security
Generally, supply chain participants do not wish to expose
proprietary data to competitors and most prefer to not be put
in a position that requires trust of government agencies and/or
third parties to secure such data on their behalf. It is, therefore,
unlikely that the vision of a central data repository controlled
and/or accessible by FDA or another government entity, to
which all food traceability data must be pushed, represents a
sound solution. A similar effort was envisioned in the 2000s
by the USDA to create a national database with all farm
Table 1
Comparison of hazard analysis and critical control points
(HACCP) and critical tracking events (CTEs)
HACCP
Data mining /
traceability
algorithms (web
crawling)
CTE server
registration
CTE
server
1
CTE
server
2
Operator 1
Operator 2
CTE
server
3
Operator 3
393
Table 2
Four categories of critical tracking events (CTEs); terminal, transfers, aggregations/disaggregations, and commingling
CTEs category
Description
Terminals
1. Creation, origination
2. Disposition
Transfers
1. Shipping
2. Receiving
Aggregation/disaggregation
1.
2.
3.
4.
Item case
Cases pallet
Pallet container, trunk, etc.
Container ship, rail, etc.
Commingling
1.
2.
3.
4.
Blend
Formulate
Bulk commingling
Rework
394
Terminal CTE
product is put into a case
Transfer CTE
pallets are loaded onto
truck for shipping
Aggregation CTE
cases are palletized
Figure 5 Example of CTEs in a simplied produce-packing facility (terminal, aggregation, and transfer CTEs).
packinghouse has identied an aggregation CTE in their process. As cases of product are palletized, an aggregation CTE
exists and captures data identifying which cases comprise an
individual pallet.
When pallets are broken down, the process works in reverse
in that one incoming object (pallet) results in many outgoing
objects (cases).
those operators will have their own denitions for their own
lots that make sense to their own operations. Clearly, the term
lot is more of an idea than a universally dened term. Although this alone should provide a sufcient argument against
the choice of lot numbers as the core data for traceability, at
least two additional arguments might be made against use of
lot numbers. First, lot numbers are currently elusive when
dealing with an unpackaged food or an ingredient. Lot codes
are often inconsistent and change meaning throughout the
supply chain and therefore represent limited utility when conducting a traceback. Lot codes are generally more useful when
conducting a recall and therefore targeting specic production
units in the supply chain. When the source of an outbreak or
point of convergence is identied, investigators and operators
need to know the size of the lot or lots associated with the
implicated product in order to commence the subsequent investigative process and initiate the recalling of food. Using
CTEs, until the source or point of convergence is identied,
investigators have no need for every operator's denition of
their own lots. They simply need an effective means to nd
points of convergence. Another issue with using lot numbers is
that they tend to unnecessarily expose intelligence about production volumes and inventory turnover to competitors and
customers and present food defense risks. This may or may not
be deemed important to any given operator, but operators
should be free to choose whether or not they wish to expose
those data without being forced to do so by regulation.
Therefore, although lot numbers currently are critical to the
investigative process, lot numbers do not represent an ideal
means for tracing items through the supply chain. Implementation of the CTE concept throughout the supply chain will
obviate the need for investigators to focus primarily on lot code
information as a proxy for internal traceability because case
level traceability may be more widely available.
received considerable attention was developed as a consequence of advances in RFID technology is the electronic
product code (EPC). Through standardization efforts, the EPC
is widely referred to as a serialized global trade identication
number (sGTIN). The GTIN has been in use for a long time
and is most recognizable as the Universal Product Code (UPC)
printed on most food packages (Figure 6).
As with the lot number, the GTIN or UPC code does not
identify a specic item, but rather a type of product in general.
The sGTIN is a simple modication that adds a serial number
to the GTIN to provide unique identication of items in the
supply chain. GTIN codes and therefore sGTIN codes are
managed globally through GS1, a non-prot international
standards organization, on a subscription basis. Although GS1
is widely recognized and respected, there may be reason for an
operator to wish to use another coding system now or in the
future. The CTE framework simply requires uniqueness while
the code exists within the supply chain. Therefore, the only
practical limitation on coding systems is ensuring that others
in the supply chain can also read codes. It is worth noting that
the GTIN was established before development of modern
computing technologies and practices. GTIN and sGTIN codes
inherently deliver meaningful data within the code, such as
manufacturer identication. Serialized code data may also
provide insight into production volumes and rates. Exposing
such data may or may not be desirable to operators, especially
when exposing such information is not necessary under the
CTE food traceability framework. Therefore, the authors recommend that operators consider alternative coding schemes
that simply satisfy the basic CTE requirements.
Contrary to an apparently common tendency to seek enforcement of compliance with data standards and structures,
readability is the only important requirement for achieving
Globally unique.
Least amount of data/bits as possible and practical.
Simple to print, write, and/or encode.
Simple to read.
Contains no meaningful information about the product or
operator (i.e., does not carry decodable information such as
Julian date, etc.)
1 4 1 4 1
395
9 9 9 9 9
U.P.C.
Item reference Check
company prefix
number
digit
Figure 6 Universal Product Code (UPC) code including company
prex, item reference number, and mathematically calculated check digit.
Examples of traceability codes: The codes are represented by the Unique IDs created for each combination of CTE type, name, and
Name
Location
Unique ID
Terminal creation
Aggregation Palletizing
Transfer Shipping
Washing/sorting/packaging machine
End of conveyor
Shipping dock door 2
XYZ123
ABC321
DEF456
396
What?
When?
XYZ123
789
397
Restaurant
state A
Distribution
center
state A
Manufacturer
state A
Farm
state A
Restaurant
state B
Farm
state B
Grocery store
state C
Distribution
center
state E
Manufacturer
state D
Farm
state D
Grocery store
state D
Figure 7 Simple conceptual diagram of traceback investigation. In this investigation, product is traced back to a point of convergence at Farm A.
CTE server
registration
Data mining/
traceability
algorithms
CTE
server
Business
1 data
CTE
server
Business
2 data
CTE
server
Business
3 data
Conclusion
Past outbreaks have demonstrated the need for more rapid and
accurate food traceability. Using existing standards and technologies, and adopting the CTE concept of traceability, would
allow industry and regulators to intervene in outbreaks and
prevent additional cases of foodborne illness. CTE allows for
more targeted food recalls, potentially limiting the amount of
References
Anonymous, 2010. Melamine Pet Food Recall of 2007, last update on 29 November
2010. US Food and Drug Administration. Available at: http://www.fda.gov/
AnimalVeterinary/%20SafetyHealth/RecallsWithdrawals/ucm129575.htm (accessed
02.04.13).
Anonymous, 2002. Bioterrorism Act 21 U.S.C. 350(c)(b) 2002. US Food and
Drug Administration.
Braden, C.R., 2006. Salmonella enterica serotype Enteritidis and eggs: A
national epidemic in the United States. Clinical Infectious Diseases 43 (4),
512517.
Cavallaro, E., Date, K., Medus, C., et al., 2011. Salmonella typhimurium infections
associated with peanut products. New England Journal of Medicine 365 (7),
601610.
Kuchenmller, T., Hird, S., Stein, C., et al., 2009. Estimating the global burden
of foodborne diseases a collaborative effort. Eurosurveillance 14 (18),
1922.
McEntire, J., 2009. Institute of Food Technologists Task Order No.7 Final Report:
Revised Tracing Systems: An Exercise Exploring Data Needs and Design.
Chicago, IL: Institute of Food Technologists.
398
McEntire, J., Bhatt, T., 2013. Pilot Projects for Improving Product Tracing along the
Food Supply System Final Report. Chicago, IL: Institute of Food Technologists.
Medus, C., Meyer, S., Smith, K., et al., 2009. Multistate outbreak of salmonella
infections associated with peanut butter and peanut butter containing products
United States, 20082009. Journal of the American Medical Association 301
(11), 11191122.
Miller, B.D., 2012. Use of traceback methods to conrm the source of a multistate
Escherichia coli O157: H7 outbreak due to in-shell hazelnuts. Journal of Food
Protection 75 (2), 320327.
Pendell, D.L., Brester, G.W., Schroeder, T.C., Dhuyvetter, K.C., Tonsor, G.T., 2010.
Animal identication and tracing in the United States. American Journal of
Agricultural Economics 92 (4), 927940.
Scallan, E., Hoekstra, R.M., Angulo, F.J., et al., 2011. Foodborne illness acquired in
the United States Major pathogens. Emerging Infectious Diseases 17 (1), 715.
Welt, B., Blancheld, R., 2012. IUSFoST Scientic Information Bulletin: Food
Traceability. Oakville, Ontario, Canada: International Union of Food Science and
Technology.
Relevant Websites
http://www.fda.gov/Food/GuidanceRegulation/FSMA/default.htm
Food Safety Modernization Act.
www.gs1.org
GS1.
www.producetraceability.org
Produce Traceability Initiative.
Crop Insurance
G Schnitkey and B Sherrick, University of Illinois, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Actuarially fair Means that premiums on policies equal
the expected payments from the policy.
Adverse selection Occurs because of asymmetric
information. After insurance premiums are set, potential
insurance purchases evaluate premiums. Individuals with
more risk will purchase crop insurance and those with less
risk will not purchase insurance.
Introduction
Crop insurance is a contractual agreement between a farmer and
an insurer under which the farmer pays a premium to the insurer and the insurer agrees to make insurance payments contingent on events occurring in the future that trigger losses as
dened in the crop insurance contract. Crop insurance payments are intended to reduce risk by making payments when a
farm is under nancial stress. Under better than average outcomes, a farmer pays a premium but does not receive a payment, so the intended net effect of insurance is to reduce the
range of possible outcomes that farmers can experience.
Most insurance markets are regulated to assure that insurance companies can make the insurance payments stipulated
in insurance contracts. Conceivably, this regulatory function
could be the only governmental involvement in crop insurance. In the United States, however, the federal government is
much more heavily involved in crop insurance. The federal
government determines the specications of federal crop insurance contracts that are sold to farmers, sets premiums that
farmers pay on crop insurance policies, subsidizes the costs of
premiums and program delivery, and acts as a reinsurer to
crop insurance companies offering crop insurance contracts. It
is thus important to understand the role of the federal government in crop insurance markets and how crop insurance
differs from other more common forms of insurance. Although each country is unique, many countries are involved in
crop insurance and face many of the same issues as in the
United States, as noted in the nal section of this article.
In the materials that follow, features of the crop insurance
market are delineated rst by types of crop insurance products
available to farmers. Then the history of the involvement of
government in crop insurance is discussed, with particular emphasis given to increases in subsidies that have occurred through
time. Finally, major issues that have caused difculties and
concerns in crop insurance delivery are outlined and described,
along with implications for performance of crop insurance.
doi:10.1016/B978-0-444-52512-3.00115-7
399
400
Crop Insurance
Crop Insurance
401
Total premiums
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
26
26
26
26
27
58
53
51
50
60
53
60
60
60
59
59
59
58
58
61
62
62
63
402
Crop Insurance
the federal governments share of total premiums has increased as well. In 1990, 26% of the total premiums were paid
by the federal government. In 2012, 63% were paid by the
federal government (see Table 1).
The current size of the crop insurance program may have
accomplished a major policy goal: replacing disaster assistance
programs with crop insurance. Since passage of the Federal
Crop Insurance Act of 1980 that eliminated the standing disaster assistance program, Congress has implemented ad hoc
disaster assistance programs throughout the 1980s, 1990s,
and 2000s. In 2012, however, there was major drought that
impacted much of the Midwest and Great Plains, yet no ad hoc
disaster assistance program was passed. A major reason given
for no disaster assistance program was the size and coverage of
the crop insurance program.
Federal
government
Reinsurance
company
Provides risk
coverage to crop
insurance
companies
Crop insurance
company
Crop insurance
agent
Farmer
Crop Insurance
companies and is periodically renegotiated to maintain performance targets through time. The negotiations around the
SRA can be very controversial, as crop insurance companies
and the federal government are often at direct odds about the
terms of the agreement. Crop insurance companies prefer to
retain a higher share of the gains and a lower share of losses,
whereas the federal government wants to provide incentives
for greatest coverage at lowest net cost. As policy terms and
premium determination are set outside a companys control,
the terms of the SRA have a large impact on the ultimate
nancial performance of crop insurance for companies.
Under the terms of the SRA, two funds of policies exist in
each state into which each policy may be committed. These are
termed (1) assigned risk fund and (2) commercial fund (Risk
Management Agency, 2013b). Within specied limits, a crop
insurance company must place each policy into either an assigned risk or a commercial fund before determining the loss
experience of the policy. Risk sharing differs dramatically
across these pools with the ability to retain exposure to policy
risk greater within the commercial fund.
For polices placed in the assigned risk fund, the companies
cede 80% of the premiums to the federal government. On this
ceded premium, the crop insurance company does not receive
any gains or losses regardless of the outcome of the underlying
policy. On the 20% of retained premium, gains and losses are
shared on the basis of a prescribed schedule, with the majority
share accruing to the FCIC. To illustrate, suppose that the loss
ratio, or indemnity payments divided by premiums, equaled
1.5 at a state level. In this case, losses are 50% greater than
premium, and for each dollar of premium, an additional US
$0.50 has to be paid, resulting in a loss of equal magnitude.
Under the Assigned Risk fund, at this level of loss ratio, the
company will have a US$0.04 loss, whereas the FCIC will bear
US$0.46 of the loss. As shown in Table 2, the losses increase as
loss ratios increase, but not proportionately with loss levels.
The companys losses go up with loss ratio to US$0.08 for a
2.5 loss ratio, US$0.11 for a 3.5 loss ratio, US$0.14 for a 4.5
loss ratio, and losses are then capped at US$0.15 for a 5.5 and
higher loss ratios.
For policies placed in the commercial fund, the company
can retain between 35% and 100% of the total premium in 5%
increments. The amount of premium to retain is a companys
decision. In the commercial fund, a company bears more
Table 2
Loss ratio
Total loss
FCIC
Insurance company
FCIC
Insurance company
0.46
1.42
2.39
3.36
4.35
5.35
0.30
0.65
0.74
0.83
0.88
0.88
0.20
0.85
1.76
2.67
3.62
4.62
0.20
0.38
0.47
0.57
0.61
0.61
Assigned risk
Loss sharing for different funds under the 2012 Standard Reinsurance Agreement, dollars of loss per dollar of retained premium
Insurance company
1.5
2.5
3.5
4.5
5.5
6.5
403
0.50
1.50
2.50
3.50
4.50
5.50
0.04
0.08
0.11
0.14
0.15
0.15
FCIC
404
Crop Insurance
Table 3
Unit
Basic optional
Enterprise (%)
67
64
64
59
59
55
48
38
Table 4
Year
80
80
80
80
80
77
68
53
Gross indemnity
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
Total
a
2 909
3 434
4 185
3 945
4 709
6 547
9 833
8 950
7 595
11 967
11 112
75 186
4 058
3 259
3 290
2 341
3 551
3 465
8 422
5 214
4 253
10 838
17 361
66 052
Million dollars
(1149)
175
895
1604
1158
3082
1411
3736
3342
1129
(6249)
9134
Insurance companyb
(47)
377
691
915
821
1571
1094
2298
1916
1663
(1312)
9987
(1102)
(202)
204
689
337
1511
317
1438
1426
(534)
(4937)
(853)
Crop Insurance
405
Systemic Risk
Crop insurance has all the problems associated with any other
form of privately offered insurance: ratings difculties, adverse
selection, and moral hazard. As crop insurance is also publically subsidized, it faces policies concerns, including the
perennial question of why to subsidize crop insurance in the
rst place. The following four subsections cover issues associated with crop insurance beginning with ratings issues and
moving to more public policy concerns. This progression of
issues is not without overlap, as many of the issues are intertwined with one another.
406
Crop Insurance
Crop Insurance
insurances and area-based contracts in developing crop insurance contracts in developing countries (Skees et al., 1999).
Of course, use of weather or index contracts introduces issues
of correlation between the index on which crop insurance is
based and actual yield. Whether or not these contracts will be
successful is an open question.
Summary
Crop insurance provides important risk management protection to farmers. Over time, this risk management protection
has been provided with heavy government involvement, including standardization and rating of products, pricing crop
insurance policies, and reinsurance of crop insurance companies. Issues common to all insurance markets occur in crop
insurance, and issues related to the systemic risk further
complicate the provision through private markets alone. It has
unique features that reset each year with annual prices of the
underlying insured commodities and due to the single-price
feature across participants and delivery channels. The degree
of subsidy involved in its provision seems to be a key point
of contention, but this issue should also be viewed in the
context of the political environment that includes considerations of ad hoc disaster assistance and its use to motivate
other desirable policy outcomes as well. In any case, it has
become the primary cornerstone for many farmers risk management activities and has also become one of the main features of farm program legislation debate. It is expected that
crop insurance markets and products will continue to become
more sophisticated through time and that innovations will
continue, but some form of public participation will also
continue for the foreseeable future due to the underlying
nature of crop revenue risk.
References
Chite, R.M., 1988. A federal crop insurance: Background and current issues.
Congressional Research Service Report No. 88-739 ENR. Washington, DC:
Congressional Service Reports.
407
Coble, K.H., Dismukes, R., Glauber, J.W., 2007. Private crop insurers and the
reinsurance fund allocation decision. American Journal of Agricultural Economics
89 (3), 582595.
Gardner, B.L., Kramer, R.A., 1986. Experience with crop insurance programs in the
United States. In: Hazell, P., Promenade, C., Valdez, A. (Eds.), Crop Insurance
for Agricultural Development: Issues and Experience. Baltimore, MD: John
Hopkins University Press, pp. 195222.
Glauber, J.W., 2004. Crop insurance reconsidered. American Journal of Agricultural
Economics 86 (5), 11791195.
Goodwin, B.K., 1993. An empirical analysis of the demand for multiple peril crop
insurance. American Journal of Agricultural Economics 75 (2), 425434.
Goodwin, B.K., Vandeveer, M.L., Deal, J., 2004. An empirical analysis of acreage
effects on participation in the federal crop insurance program. American Journal
of Agricultural Economics 86, 10581077.
Hazell, P.B.R., 1992. The appropriate role of agricultural insurance in developing
countries. Journal of International Development 4, 567581.
Horowitz, J.K., Lichtenberg, E., 1993. Insurance, moral hazard, and chemical use in
agriculture. American Journal of Agricultural Economics 75 (4), 926935.
Miranda, M.J., 1991. Area-yield crop insurance reconsidered. American journal of
Agricultural Economics 73 (2), 233242.
Miranda, M.J., Glauber, J.W., 1997. Systemic risk, reinsurance, and the failure of
crop insurance markets. American Journal of Agricultural Economics 79 (1),
206215.
Nelson, C.H., Loehmann, E.T., 1987. Further toward a theory of agricultural
insurance. American Journal of Agricultural Economics 69, 523531.
Risk Management Agency, 2012. United States Department of Agriculture. Summary of
Business. Available at: http://www.rma.usda.gov/data/sob.html (accessed 15.01.14).
Risk Management Agency, 2013a. United States Department of Agriculture. 2013
Crop Insurance Handbook. FCIC 18010, (06-2013). Washington, DC: Risk
Management Agency.
Risk Management Agency, 2013b. United States Department of Agriculture.
Reinsurance Reports Online. Available at: http://www.rma.usda.gov/tools/
reinsurance.html (accessed 15.01.14).
Skees, J., Hazell, P., Miranda, M., 1999. New approaches to crop yield insurance in
developing countries. Environment and Production Technology Division Discussion
Paper No 55. Washington, DC: International Food Policy Research Institute.
Skees, J.R., Reed, M.R., 1986. Rate making for farm-level crop insurance:
Implications for adverse selection. American Journal of Agricultural Economics
68 (3), 654659.
Smith, V.H., Goodwin, B.K., 1996. Crop insurance, moral hazard, and agricultural
chemical use. American Journal of Agricultural Economics 78 (2), 428438.
Valgren, V.N., 1922. Crop insurance: Risks, losses, and principles of protection.
U.S. Department of Agriculture, Bulletin NO. 1043. Washington, DC: U.S.
Department of Agriculture.
Woodard, J.D., Schnitkey, G.D., Sherrick, B.J., Lozano-Gracia, N., Anselin, L.u.c.,
2012. A spatial econometric analysis of loss experience in the U.S. crop
insurance program. The Journal of Risk and Insurance 79 (1), 261285.
Wu, J., 1999. Crop insurance, acreage decisions, and nonpoint Source pollution.
American Journal of Agricultural Economics 81 (2), 305320.
Crop Pollination
SG Potts and T Breeze, University of Reading, Reading, UK
B Gemmill-Herren, Food and Agricultural Organization of the United Nations, Rome, Italy
r 2014 Elsevier Inc. All rights reserved.
Glossary
Biotic-pollination When pollen is delivered to stigmas by
animal vectors such as insects.
Cross-pollination The transfer of pollen from an anther of
the ower of one plant to a stigma of the ower of another
plant.
Pollination The main mode of sexual reproduction in
plants, which occurs when the transfer of pollen (male)
from the anther of a ower to a stigma (female) results
Introduction
Pollination is the main mode of sexual reproduction in plants,
which occurs when the transfer of pollen (male) from the
anther of a ower to a stigma (female) results in fertilization
which produces seeds and, in some cases, fruits. Pollination is,
therefore, an important input in the production of the
marketable goods of many crops and can have a substantial
impact on production. Pollination by animals in particular is a
vital component in global agricultural economies by increasing crop productivity and prots. However, some of the main
animal pollinators, such as bees, hoveries, and butteries, are
in a state of long-term decline in some regions of the world,
thereby threatening the stability and security of this ecosystem
service. This article presents a brief overview of the main
modes of pollination in globally important crops, highlighting
the yield and economic benets of animal pollination in
particular. The main drivers of animal pollination service declines are then reviewed along with possible measures to
mitigate these declines.
Modes of Pollination
Within crops there are several widely observed modes of pollination. Self-pollination whereby owers of the plant are
capable of fertilizing themselves is the most simplistic and
often occurs in plants such as peas with enclosed owers.
However, most crops require pollen transfer between different
owers to successfully fertilize or benet from external agents
increasing their rate of self-pollination. In many crops pollen
grains are light enough to be transferred effectively by wind
with some crops, such as wheat, relying largely on wind pollination to successfully pollinate. Approximately 75% of
globally important crops benet from biotic pollination
whereby animals transfer pollen between owers or increase
the rate of self-fertilization that occurs (Klein et al., 2007). In
some crops, biotic pollination by particular animals is essential to the production of marketable output. This is especially
important to crops where the pollen is too heavy or sticky to
408
move via the wind (e.g., almond Prunus dulcis), where there are
separate male and female owers (e.g., kiwifruit) and where
pollen must come from a different cultivar (pollinizer) to
produce fruit (e.g., rabbiteye blueberries, Vaccinium virgatum)
(Free, 1993). Biotic pollination is usually performed by bees
and ies, many of which have evolved to feed exclusively on
oral pollen and nectar, but butteries, beetles, birds, bats,
and even some terrestrial mammals (e.g., palm squirrel;
Chakravarthy and Thyagaraj, 2012) can provide pollination
services to commercial crops (Klein et al., 2007).
Globally, domesticated honeybees (Apis spp.) are widely
utilized to provide pollination services to a wide variety of
crops, particularly in large-scale systems (e.g., rapeseed) where
abundant pollinators are required. However, some studies
have demonstrated that honeybees are not always the most
effective pollinators of crops, either by collecting nectar from
owers without contacting the anthers (e.g., apples, Malus
domestica; Thompson and Goodall, 2001), displaying foraging
preference for noncrop plants over some crops or simply
nding some unattractive (e.g., pears, Stern et al., 2004). Another widely observed group of pollinators are bumblebees
(Bombus spp.), which are effective pollinators of many small
fruits (e.g., raspberries, Rubus idaeus; Willmer et al., 1994) and
are widely domesticated to provide pollination services to
crops that honeybees cannot effectively pollinate (e.g., tomatoes, Solanum lycopersicum; Banda and Paxton, 1991). Other
pollinators have also been domesticated to provide more
specialist pollination services to certain crops. These include
alfalfa leafcutter bees (Megachile rotundata) that are used to
pollinate alfalfa and mason bees (Osmia spp.), which have
recently been domesticated to provide pollination services to
some fruit crops (Bosch and Kemp, 2002).
Although domesticated pollinators can be readily managed
to provide pollination services to a wide range of crops, pollination services by wild insects are increasingly thought to be
important to crop production even in intensive cropping systems, such as muskmelon (Cucumis melo) production in
Pennsylvania, USA (Winfree et al., 2008). In many tropical
countries feral honeybees, stingless bees (Meliponina sp.), and
solitary bees are important contributors to crop pollination in
doi:10.1016/B978-0-444-52512-3.00020-6
Crop Pollination
Benets of Pollination
It is estimated that 75% of globally important crops benet
from biotic pollination in various ways, from directly increased yields to greater crop quality or other agronomic
benets (Klein et al., 2007). Most overtly, biotic pollination
directly increases fruit seed set in many crops compared with
other modes of pollination alone (e.g., pears, Pyrus communis;
Nyeki and Stolesz, 2003), resulting in greater overall production. This is especially important to crops that cannot
self-pollinate, many of which require biotic pollination to
effectively transfer pollen between neighboring plants (Free,
1993). Similarly, in many crops, biotic pollination produces
fruits with greater weight compared with those produced by
wind and self-pollination alone, increasing the total market
output per hectare. Recent studies have demonstrated that
pollination by insects can increase the proportion of
marketable oil content in rapeseed (Brassica napus; Bommarco
et al., 2012). Biotic pollination can also increase the speed and
synchronization of fruit maturity, resulting in easier, more
efcient harvesting (e.g., linseed, Linum usitatissimum; Williams
et al., 1991). In some highly productive crops, such as sweet
peppers (Capsicum annum) grown in glasshouses, this increased maturity can even result in additional harvests per year
(Shipp et al., 1994).
Beyond direct increases in output, biotic pollination can
also signicantly improve fruit quality in certain crops. For
instance in strawberries (Fragaria ananassa), pollination of
all anthers by insects is required to produce fruit of an
acceptable shape (Chagnon et al., 1993). Besides economically
signicant quality factors, biotic pollination can improve the
nutrient content (e.g., apples; M. domestica; Volz et al., 1996),
and taste quality (e.g., tomatoes, S. lycopersicum; Hogendoorn
et al., 2010) in some crops. Biotic pollination can also provide
more long-term agronomic benets to crop producers. By
transferring pollen between different plants, crop pollination
can reduce inbreeding effects within crops, which may help
improve disease resistance (Free, 1993) and reduce crop
abortion rate (e.g., almond, P. dulcis; Martinez-Garcia et al.,
409
2012). A study on persimmon (Diospyros kaki) tree productivity found that trees receiving ample pollination from insects
also grew at a quicker rate, probably because the plant was
forced to increase its nutrient uptake to support greater yields
(George et al., 1995).
Although pollination can benet many plants, it is possible
that biotic pollination may negatively impact productivity in
some crops. For instance, if excessively pollinated, crop trees
may become overburdened with fruits, requiring costly thinning by hand or chemical induction to prevent damage to the
tree or excessive nutrient use. In other crops, notably pineapples and some varieties of citrus fruit (Citrus sp.) and cucumber (Cucumis sativus), biotic pollination can result in seed
production which can leave the product unmarketable (Free,
1993). As most noncrop owering plants also benet from
biotic pollination (Ollerton et al., 2011), the prevalence of
abundant pollinators can also encourage the propagation of
many weeds.
Fruit Crops
As a group, the majority of fruit crops are dependent on pollination to produce marketable yields. Several tree fruit crops,
notably apple (M. domestica), plum (Prunus domestica), and gs
(Ficus carica), are largely self-incompatible and very highly
dependent on animal pollinators to transfer pollen between
owers from different trees. Yields of most other tree fruits,
including avocado, peach, pear, plum, and sour cherry, can
increase by 500900% by animal pollinators transferring
pollen between plants and owers as wind pollination is often
insufcient to successfully transfer enough pollen. By contrast,
the benets of biotic pollination to persimmon trees (D. kaki)
can vary substantially with some varieties being able to set
fruit entirely through self and wind pollination, whereas other
cultivars can double yields with ample biotic pollination
(George et al., 1995; Free, 1993). Citrus fruits (Citrus sp.) also
vary in their need for biotic pollination; although some species, such as mandarin produce more and larger fruits when
cross-pollinated by insects (Schneider et al., 2009), varieties of
other citrus crops can set more desirable seedless fruits with
parthenocarpy, making biotic pollination largely undesirable
(Free, 1993).
Small fruits largely benet from biotic pollination to more
moderate extents than other fruits as many are self-compatible,
have small, light pollen grains, require fewer grains per stigma
to fertilize, and produce multiple anthers per ower allowing
them to set fruit even if not all stigmas are fertilized.
410
Crop Pollination
Table 1
Crop
Effective pollinatorsb
Almond
Apple
Buckwheat
Citrus fruits
Cocoa
Coffee
Faba bean
Mango
Raspberry
Rapeseed
Seed cotton
Soybean
Strawberry
65
65
65
5
95
25
25
65
25
25
25
25
25
Sunower
Tomato
25
25
a
Adapted from Gallai, N., Vaissire, B.E., 2009. Guidelines for the economic value of pollination services at a national scale. Available at: http://www.
internationalpollinatorsinitiative.org/uploads/POLL%20VALUE%20NATIONAL%20MANUAL.pdf
b
Adapted from Klein, A.M., Vaissiere, B.E., Cane, J.H., et al. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B
Biological Sciences 274 (1608), 303313.
Crop Pollination
globally (FAO, 2013). Sunowers have one of the two pollination systems, in most oil producing cultivars the ower
switches between the male and female phases, whereas in
hybrid production, specically bred male and female lines are
planted within the same eld. Both benet from insect visitation to optimize pollen transfer to female plants (Free, 1993).
Rapeseed and canola are highly self-compatible and readily set
pods with wind and self-pollination; however, their high
nectar concentration makes them attractive to insects which
can increase pollen transfer, thereby increasing the total
marketable yield by 20% (Bommarco et al., 2012). Rapeseed is
attractive to a wide diversity of pollinating insects and although wild insects can be signicant, managed honeybees are
thought to provide a more reliable and stable service to larger
elds (Rader et al., 2009 but see Rader et al., 2011; Woodcock
et al., 2013). Pollination in coconut, which has separate male
and female owers, produces similar increases in yield through
greater drupe set (Melndez-Ramrez et al., 2004). Some edible
oil crops gain very little benet from pollination, such as linseed (L. usitatissimum) (Williams et al., 1991), whereas olive
(Olea europaea), is entirely wind pollinated (Klein et al., 2007)
and some, specially bred cultivars of rapeseed can also set
ample yield from wind pollination alone (Free, 1993). In seed
cotton, biotic pollination benets production of both utilized
outputs, resulting in a 20% increase in total seed weight and a
16% increase in lint production (Rhodes, 2002).
Stimulant Crops
Both the major stimulant crops, cocoa (Theobroma cacao) and
coffee (Coffea arabica and C. canephora), benet from biotic
cross-pollination between plants to produce good quality
yields. In cocoa, although bees have been observed to provide
pollination services in some regions, the majority of pollination services are provided by midges (Cecido myiid and
Ceratopogonid spp.). Both species of coffee benet from insect
visitation, however, despite their lighter pollen grains;
C. canephora is thought to be slightly more dependent on insect pollination than C. arabica due to greater self-incompatibility (Free, 1993; Klein et al., 2003). Field studies have
indicated that pollination produces both greater bean set and
weight by ~20% and reduces the occurrence of misshapen pea
berries by 27% (Ricketts et al., 2004; Klein et al., 2003).
411
Pulse Crops
Several pulse crops, notably soybean (Glycine max) and faba
bean (Vicia faba), are often primarily self-pollinated due to
their tightly enclosed owers which place the anthers in direct
contact with the stigma. Pollination of soybeans by Africanized honeybees has been observed to increase yields by 50%
under experimental conditions, with bee-pollinated owers
producing more and heavier pods than enclosed plants (Chiari
et al., 2005). In faba beans, cross-pollination by insects has
also been demonstrated to improve both yield and disease
resistance (Suso, 2012). By contrast, biotic pollination has no
effect on the yields of peas (Pisum sativum), lentils (Lens
esculenta), and chickpeas (Cicer arietinum) and very little in
cowpea (Vigna unguiculata). Other pulses such as runner beans
(Phaseolus coccineus) have more open owers that directly
benet from biotic pollination (abuda, 2010).
Spice Crops
Among the crops grown for condiment or spice products are
several species of the plant family Umbelliferae, notably fennel
(Foeniculum vulgare), caraway (Carum carvi), and coriander
(Coriandrum sativum), which are characterized by numerous
small owers with each ower producing multiple seeds.
Visitation of these owers by foraging insects helps transfer
pollen among the many owers, resulting in substantial increases in seed set (Free, 1993). Owing to the arrangement of
its anthers making self-pollination impossible, vanilla (Vanilla
planifolia) relies entirely on biotic pollination for pod set, although in many regions this must be done via hand pollination (Free, 1993).
Cereal Crops
Most arable grain crops, including the global staples of wheat,
rice, and maize do not benet from biotic pollination, instead
relying entirely on self and wind pollination to produce seeds
(Klein et al., 2007). The only exception is the pseudocereal
Buckwheat (Fagopyrum esculentum), which is self-incompatible
and benets greatly from insect pollination to set seed (Taki
et al., 2011).
Sugar Crops
Although visited by several insects, sugar beet (Beta vulgaris) is
not known to benet from biotic pollination as their owers
are highly self-compatible and effectively pollinated by self
412
Crop Pollination
Table 2
Region
Africa
Asia
Europe
North America
South America
Oceania
Total
Value of pollination
services (bn)
137.5
881
216.7
176.8
187.7
18.8
11.9
88.1
22
17.9
11.6
1.3
1618.5
152.8
Pollination services as a
% of total value
Regional % of global
pollination service value
9
10
10
10
6
7
8
58
14
12
8
1
9.5
Source: Adapted from Gallai, N., Vaissire, B.E., 2009. Guidelines for the economic value of pollination services at a national scale. Available at: http://www.
internationalpollinatorsinitiative.org/uploads/POLL%20VALUE%20NATIONAL%20MANUAL.pdf
Other Crops
Apart from edible crops, yields of several important plants
grown for commercial seed production benet to a great extent
from insect pollination, often by specialist insects. Lucerne seed
(Medicago sativa) yields, in particular, are heavily dependent
on insect pollination by specialist alfalfa leafcutter bees
(M. rotundata), which are better able to access the nectaries and
pollen of lucerne owers (Delaplane and Mayer, 2000). Similarly, several species of clover (Trifolium sp.) are widely bred for
planting as nitrogen xing cover crops or hay and require insect
visitation to effectively cross-pollinate. Red clovers (Trifolium
pratense), among other species, have long, deep owers that
cannot be accessed by most short-tongued bees and instead
require longer-tongued species such as the bumblebee Bombus
hortorum (Bommarco et al. 2011).
Crop Pollination
413
0.050
0.045
Percentage of GDP
0.040
0.035
0.030
0.025
0.020
0.015
0.010
0.005
0.000
Global
US
UK
Nepal
China
Egypt
Country
Figure 1 Proportion of total national GDP arising from insect-pollinated crops for selected countries and global average. Compiled by H. Ngo
from FAO data.
Table 3
Crop group
Vegetables
Fruits
Edible oil crops
Stimulants
Nuts
Pulses
Spices
Cereals
Sugar crops
Roots and tubers
Total
Value of pollination
services (bn)
418
219
240
19
13
24.1
7
312
268
98
51
50
39
7
4
1
0.2
0
0
0
1618.5
152.8
Pollination services as a
% of total value
Regional % of global
pollination service value
12
23
16
39
31
4
3
0
0
0
33
33
25
5
3
1
0.1
0
0
0
9.5
Source: Adapted from Gallai, N., Vaissire, B.E., 2009. Guidelines for the economic value of pollination services at a national scale. Available at: http://www.
internationalpollinatorsinitiative.org/uploads/POLL%20VALUE%20NATIONAL%20MANUAL.pdf
$77m and $433m (US) annually. Furthermore articial pollination may not be viable for all crops, such as raspberry
where hand pollination produces lower quality fruits
compared with insect pollination (Kempler et al., 2002). Pollination services provided by wild animals can also reduce the
need to hire managed honeybees for crop pollination. For
example, hiring additional honeybees to replace pollination
services provided by wild pollinators in the watermelon
plantations in New Jersey would cost producers an estimated
$200 000, effectively doubling the expenditure on managed
pollination services (Winfree et al., 2011).
In addition to these economic benets, production added
by pollination services has a substantial impact on human
diets. Globally, animal-pollinated crops form 35% of the
total crop production (Klein et al., 2007) and a loss of pollination services would result in a reduction of total crop
production by 38% even if highly pollinator-dependent
crops were replaced with pollinator-independent ones (Aizan
et al., 2009). Although the majority of crop-based calories
and protein in the human diet derive from pollinatorindependent crops, animal-pollinated crops are the main
sources of vegetable fats and several major micronutrients.
Consequently, ~41% of vitamin A, 20% of vitamin C, 32% of
carotenoids, and 20% of uorides in global diets are thought
to derive from production added by insect pollination (Eilers
et al., 2011).
414
Crop Pollination
Crop Pollination
primary pollinators of several deep owered crops, notably
faba beans (Aouar-Sadli et al., 2008; Benachour et al., 2007)
and red clover (Bommarco et al., 2012). With their smaller
colony sizes, bumblebees are less vulnerable to overheating
and resource depletion when conned in enclosed systems
than honeybees (Delaplane and Mayer, 2000), making them
ideal glasshouse pollinators and highly effective on several
crops such as tomatoes (Banda and Paxton, 1991), strawberry
(Ji-Larn et al., 2006), and sweet pepper (Ercan and Onus,
2003).
Some solitary bee species have also been domesticated to
provide more specialist pollination services to certain crops.
Mason bees (Osmia sp.) in particular, have been demonstrated
to be several times more effective per individual than honeybees in apples, almonds (Vicens and Bosch, 2000a,b),
blueberries (Stubbs and Drummond, 1997), and sweet cherries (Bosch et al., 2006). Mason bees are primarily bought as
cocoons and incubated at different temperatures to ensure
emergence in time with peak crop owering (Shefeld et al.,
2008a); however, it is possible that introduced individuals
may nd or enhance wild populations if careful management to provide suitable nesting sites and postcrop forage is
provided (Stubbs and Drummond, 2001; Shefeld et al.,
2008b). For instance, Shefeld et al. (2008b) found that
sowing late owering bigleaf lupins (Lupinus polyphyllus) in
Nova Scotia apple orchards signicantly increased breeding
success of Osmia lignaria introduced to provide pollination.
Another domesticated solitary bee is the alfalfa leafcutter bee
(M. rotundata), which has been domesticated primarily to
pollinate lucerne, its preferred forage, but can also effectively
pollinate other crops such as blueberry (Stubbs and Drummond, 1997).
Although managed pollinators can provide ample pollination services to crops, in many cropping systems, wild insects
are often as or more important service providers (Winfree
et al., 2008; Garibaldi et al., 2011b; Holzschuh et al., 2012;
Garibaldi et al., 2013). In some crops, notably strawberries
(Chagnon et al., 1993) and sunowers (Carvalheiro et al.,
2011; Greenleaf and Kremen, 2006) a mix of wild pollinators
and managed honeybees has been demonstrated to provide
the highest yields as the two groups provide complementary
pollination of the same owers. Diverse wild pollinator
communities often provide insurance against losses of key
service providers as the remaining species become more able
to exploit crop resources (Winfree et al., 2010; Klein et al.,
2012) and produce more stable crop yields between years
(Garibaldi et al., 2011b). Recent studies have also demonstrated that honeybees are largely incapable of fully substituting for losses of wild insect pollination services in most
crop systems, intensive or small holder (Garibaldi et al., 2013).
Furthermore, diverse pollinator communities allow producers
to grow more diverse crops within their holdings or between
years as part of rotations by providing an array of pollinators
with different foraging habits and preferences.
There are a number of ways that producers can manage their
holding to maintain and encourage healthy wild pollinator
populations. Foremost, providing natural habitat in close
proximity to crops can provide foraging and nesting resources
to wild insects when crops are not in bloom. Morandin and
Winston (2006), for instance, recommend that ~30% of the
415
surrounding landscape is left uncultivated to optimize pollination services to mass owering crops. Ricketts et al. (2008) also
demonstrate that pollination services fall substantially at distances of more than 1000 m from a seminatural habitat. Where
maintaining large sections of habitat is not possible or practical,
including fallow land as part of crop rotations has been demonstrated to encourage pollinators even in intensive landscapes
(Kuussaari et al., 2011). Alternatively, many plants used as
unharvested cover crops, such as red clover, can add forage
diversity to the landscape. Pollinators can also be encouraged
within elds by planting diverse nectar ower margins or tussocky grasses at the edge of crops left untreated by pesticides
(Pywell et al., 2011; Potts et al., 2009; Lye et al., 2009). In several
developed nations many of these practices are subsidized as
part of national agri-environmental schemes, providing an
added incentive to adopt these practices (Kleijn et al., 2006),
and can provide additional on-farm benets such as soil quality
maintenance and erosion control (Wratten et al., 2012). A recent study in South Africa has also demonstrated that allowing
owering weeds to remain in sunower elds enhanced pollination service benets by a greater extent than the negative
effects of the weeds themselves and produced a more even
pollination throughout the eld (Carvalheiro et al., 2011). Reducing herbicide use and grazing intensity on grasslands can
also help promote pollinator diversity by allowing more diverse
ower communities to establish (Hateld and LeBuhn, 2007;
Scheper and Kleijn, 2011).
Conclusion
As the global population continues to grow and demand for
food production increases, the areas of owering crops needed
to meet this demand will continue to expand and so will the
reliance on pollination services. Pollinators provide a wide
range of production, economic, and health benets and they
will need to be increasingly considered as a legitimate agricultural input contributing to food security.
References
Aizen, M.A., Garibaldi, L.M., Cunningham, S.A., Klein, A.M., 2008. Long term trends
in crop yield and production reveal no current pollination shortage but increasing
pollinator dependency. Current Biology 18 (20), 14.
Aizan, M.A., Garibaldi, L.M., Cunningham, S.A., Klein, A.M., 2009. How much does
agriculture depend on pollinators? Lessons from long-term trends in crop
production. Annals of Botany 103 (9), 15791588.
Aizen, M.A., Harder, L.D., 2009. The global stock of domesticated honey bees is
growing slower than agricultural demand for pollination. Current Biology 19 (11),
915918.
Allsopp, M.H., de Lange, W.J., Veldtman, R., 2008. Valuing insect pollination
services with cost of replacement. PLoS One 3 (9), 8pp. doi: 10.1371/journal.
pone.0003128.
416
Crop Pollination
Aouar-sadli, M., Louadi, K., Doumandji, S.-E., 2008. Pollination of the broad bean
(Vicia faba L. var. major) (Fabaceae) by wild bees and honey bees (Hymenoptera:
Apoidea) and its impact on the seed production in the Tizi-Ouzou area (Algeria).
African Journal of Agricultural Research 3 (4), 266272.
Ashworth, L., Quesada, M., Casas, A., Aguilar, R., Oyama, K., 2009. Pollinatordependent food production in Mexico. Biological Conservation 142 (5), 10501057.
Banda, H.J., Paxton, R., 1991. Pollination of greenhouse tomatoes by Bees. Acta
Horticulturae 288, 194198.
Benachour, K., Louadi, K., Terzo, M., 2007. Rle des abeilles sauvages et
domestiques (Hymenoptera:Apoidea) dans la pollinisation de la fve (Vicia faba
L. var. major) (Fabaceae) en rgion de Constantine (Algrie). Annales De La
Societe Entomologique De France 43 (2), 213219.
Bommarco, R., Lundin, O., Smith, H.G., Rundolf, M., 2011. Drastic historic shifts in
bumble-bee community compositions in Sweden. Proceedings of the Royal
Society B Biological Sciences 279, 309315.
Bommarco, R., Marini, L., Vaissiere, B., 2012. Insect pollination enhances seed
yield, quality, and market value in oilseed rape. Oecologia 169 (4),
10251032.
Bos, M.M., Veddeler, D., Bogdanski, A.K., et al., 2007. Caveats to quantifying
ecosystem services: fruit abortion blurs benets from crop pollination. Ecological
Applications 17 (6), 18411849.
Bosch, J., Kemp, W.P., 2002. Developing and establishing bee species as crop
pollinators: the example of Osmia spp. (Hymenoptera: Megachilidae) and fruit
trees. Bulletin of Entomological Research 92 (1), 316.
Bosch, J., Kemp, W.P., Trostle, G.E., 2006. Bee population returns and cherry yields
in an orchard pollinated with Osmia lignaria (Hymenoptera: Megachilidae).
Journal of Economic Entomology 99 (2), 408413.
Brading, P., El-Gabbas, A., Zalat, S., Gilbert, F., 2009. Biodiversity Economics: The
Value of Pollination Services to Egypt. Egyptian Journal of Biology 11, 4551.
Brittan, C.A., Vighi, M., Bommarco, R., Settle, J., Potts, S.G., 2010. Impacts of a
pesticide on pollinator species richness at different spatial scales. Basic and
Applied Ecology 11 (2), 106115.
Carvalheiro, L., Buckley, Y.M., Memmott, J., 2010. Diet breadth inuences how the
impact of invasive plants is propagated through food-webs. Ecology 91 (4),
10631074.
Carvalheiro, L.G., Veldtman, R., Shenkute, A.G., et al., 2011. Natural and withinfarmland biodiversity enhances crop productivity. Ecology Letters 14 (3),
251259.
Cavalcante, M.C., Oliveira, F.F., Maus, M.M., Freitas, B.M., 2012. Pollination
requirements and the foraging behavior of potential pollinators of cultivated brazil
nut (Bertholletia excels Bonpl.) trees in central amazon rainforest. Psyche 2012
Article ID 978019, 9pp. doi: http://dx.doi.org/10.1155/2012/978019.
Chagnon, M., Gingras, J., de Oliveira, D., 1993. Complementary aspects of
strawberry pollination by honey bees and indigenous bees (Hymenoptera).
Journal of Economic Entomology 86 (2), 416420.
Chakravarthy, A.K., Thyagaraj, N.E., 2012. The palm squirrel in coconut plantations:
ecosystem services by therophily. Mammalia 76 (2), 193199.
Chiari, W.C., de Toledo, V.A.A., Ruvolo-Takasusuki, M.A.C., et al., 2005. Pollination
of soybean (Glycine max L. Merril) by honeybees (Apis mellifera L.). Brazilian
Archives of Biology and Technology 48 (1), 3136.
Cox-Foster, D.L., Conlan, S., Holmes, E.C., et al., 2007. A metagenomic survey
of microbes in honey bee colony collapse disorder. Science 318 (5848),
283287.
Delaplane, K.S., Mayer, D.E., 2000. Crop Pollination by Bees. Wallingford, CT: CABI
Publishing.
Denisow, B., 2004. The inuence of articial wind blow on the pollination and
fructication of blackcurrant (Ribes nigrum L.) cultivars. Acta Scientiarum
Polonorum, Hortorum Cultus 3 (1), 8996.
Diektter, T., Kadoya, T., Peter, F., Wolters, V., Jauker, F., 2010. Oilseed rape
crops distort plant-pollinator interactions. Journal of Applied Ecology 47 (1),
209214.
Eilers, E.J., Kremen, C., Greenleaf, S., Garber, A.K., Klein, A.-M., 2011. Contribution
of pollinator-mediated crops to nutrients in the human food supply. PLOS One 6,
e21363.
Ercan, N., Onus, A.N., 2003. The effects of bumblebees (Bombus terrestris L.) on
fruit quality and yield of pepper (Capsicum annuum L.) grown in an unheated
greenhouse. Israel Journal of Plant Science 51 (4), 275283.
FAO, 2013. Crops. Available at: http://faostat.fao.org/site/567/DesktopDefault.aspx?
PageID=567#ancor (accessed 16.01.13).
Feon, V., Schermann-Legionnet, A., Delettre, Y., et al., 2010. Intensication of
agriculture, landscape composition and wild bee communities: a large scale
study in four European countries. Agriculture Ecosystems and Environment 137,
143150.
Formato, G., Comini, A., Giacomelli, A., et al., 2010. Veterinary care of honey bees
in the UK. Practice 32, 418425.
Free, J., 1993. Crop Pollination by Insects, Second ed. London: Academic Press.
Gallai, N., Salles, J.M., Settele, J., Vaissiere, B.E., 2009. Economic valuation of the
vulnerability of world agriculture confronted with pollinator decline. Ecological
Economics 68 (3), 810821.
Gallai, N., Vaissire, B.E., 2009. Guidelines for the economic value of pollination
services at a national scale. Available at: http://www.internationalpollinators
initiative.org/uploads/POLL%20VALUE%20NATIONAL%20MANUAL.pdf
Garibaldi, L.A., Aizen, M.A., Klein, A.M., Cunningham, S.A., Harder, L.D., 2011b.
Global growth and stability of agricultural yield decrease with pollinator
dependence. Proceedings of the National Academy of Science of the United
States 108, 15811584.
Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., et al., 2011a. Stability of pollination
services decreases with isolation from natural areas despite honey bee visits.
Ecology Letters 14, 10621072.
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., et al., 2013. Wild pollinators
enhance fruit set of crops regardless of honey-bee abundance. Science 339,
16081611.
Gemmill-Herren, B., Ochieng, A., 2008. Role of native Bees and habitats in eggplant
(Solanum melongena) pollination in Kenya. Agriculture, Ecosystems and
Environment 127, 3136.
George, A.P., Nissen, R.J., Collins, R.J., Rasmussen, T.S., 1995. Effects of fruit
thinning, pollination and paclobutrazol on fruit set and size of persimmon
(Diospyros kaki) in subtropical Australia. Journal of Horticultural Science 70 (3),
477484.
Gill, R., Ramos-Rodriguez, O., Raine, N.E., 2012. Combined pesticide exposure
severely affects individual- and colony-level traits in bees. Nature 491, 105108.
Gonzalez, M., Baeza, E., Lao, J.L., Cuevas, J., 2006. Pollen load affects fruit set,
size, and shape in cherimoya. Scientia Horticulturae 110, 5156.
Goulson, D., Sparrow, K.R., 2009. Evidence for competition between honeybees and
bumblebees; effects on bumblebee worker size. Journal of Insect Conservation 13
(2), 177181.
Greenleaf, S., Kremen, C., 2006. Wild bees enhance honey bees pollination of
hybrid sunower. Proceedings of the National Academy of Sciences of the United
States of America 103 (37), 1389013895.
Groeneveld, J.H., Tscharntke, T., Moser, G., Clough, Y., 2010. Experimental evidence
for stronger cacao yield limitation by pollination than by plant resources.
Perspectives in Plant Ecology, Evolution and Systematics 12, 183191.
Hateld, R.G., LeBuhn, G., 2007. Patch and landscape factors shape community
assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane
meadows. Biological Conservation 139, 150158.
Hawthorne, D.J., Dively, G.P., 2011. Killing them with kindness? In-hive medications
may inhibit xenobiotic efux transporters and endanger honey bees. PLoS One 6,
e26796.
Henle, K., Alard, D., Clitherow, J., et al., 2008. Identifying and managing the
conicts between agriculture and biodiversity conservation in Europe A review.
Agriculture Ecosystems and Environment 124 (12), 6071.
Hogendoorn, K., Bartholomaeus, F., Keller, M.A., 2010. Chemical and sensory
comparison of tomatoes pollinated by bees and by a pollination wand. Journal of
Economic Entomology 103 (4), 12861292.
Holzschuh, A., Dudenhffer, J.H., Tscharntke, T., 2012. Landscapes with wild bee
habitats enhance pollination, fruit set and yield of sweet cherry. Biological
Conservation 153, 101107.
Isaacs, R., Kirk, A.K., 2010. Pollination services provided to small and large
highbush blueberry elds by wild and managed bees. Journal of Applied Ecology
47 (7), 841849.
Jaffe, R., Dietemann, V., Allsopp, M.H., et al., 2010. Estimating the density of
honeybee colonies across their natural range to ll the gap in pollinator decline
censuses. Conservation Biology 24 (2), 583593.
Ji-Lian, L., Wen-Jun, P., Jain-Dong, A., et al., 2006. Strawberry pollination by
Bombus lucorum and Apis mellifera in greenhouses. Acta Entomologica Sinica
49 (2), 342348.
Jian-Dong, A., Wen-Feng, C., 2011. Economic value of insect pollination for fruits
and vegetables in China. Acta Entomologica Sincia 54 (4), 443450.
Kasina, J.M., Mburu, J., Kraemer, M., Holm-Mueller, K., 2009. Economic benet of
crop pollination by bees: A case of Kakamega small-holder farming in Western
Kenya. Journal of Economic Entomology 102 (2), 467473.
Kempler, C., Harding, B., Ehert, D., 2002. Out-of-season raspberry production in
British Columbia, Canada. Acta Horticulturae 585, 629632.
Kleijn, D., Baquero, R.A., Clough, Y., et al., 2006. Mixed biodiversity benets of
agri-environment schemes in ve European countries. Ecology Letters 9,
243254.
Crop Pollination
Klein, A.M., Brittan, C., Hendrix, S.D., et al., 2012. Wild pollination services to
California almond rely on semi-natural habitat. Journal of Applied Ecology 49
(3), 723732.
Klein, A.-M., Steffan-Dewenter, I., Tscharntke, T., 2003. Bee pollination and fruit set
of Coffea arabica and C. canephora (Rubicacea). American Journal of Botany 90,
153157.
Klein, A.M., Vaissiere, B.E., Cane, J.H., et al., 2007. Importance of pollinators in
changing landscapes for world crops. Proceedings of the Royal Society B
Biological Sciences 274 (1608), 303313.
Kuussaari, M., Hyvnen, T., Hrm, O., 2011. Pollinator insects benet from
rotational fallows. Agriculture Ecosystems and Environment 143 (1), 2836.
abuda, H., 2010. Runner bean (Phaseolus coccineus L.) Biology and Use. Acta
Scientiarum Polonorum Hortum Cultus 9 (3), 117132.
Lautenbach, S., Seppelt, R., Liebscher, J., Dormann, C.F., 2012. Spatial and
temporal trends of global pollination benet. PLoS One 7, e35954.
Losey, J.E., Vaughn, M., 2006. The economic value of ecological services provided
by insects. Bioscience 56 (4), 311323.
Lu, C., Warchol, K.M., Callahan, R.A., 2012. In situ replication of honey bee colony
collapse disorder. Bulletin of Insectology 65 (1), 99106.
Lumpkin, T.A., Weinberger K., Moore, S., 2006. Increasing income through fruit and
vegetable production opportunities and challenges. CGIAR Science Council
paper. Available at: http://library.cgiar.org/handle/10947/3904
Lye, G., Park, K., Osborne, J., Holland, J., Goulson, D., 2009. Assessing the value
of rural stewardship schemes for providing foraging resources and nesting
habitat for bumblebee queens (Hymenoptera: Apidae). Biological Conservation
142, 20232032.
Marris, G., Brown, M., Cuthbertson, A.G., 2011. Pest risk assessment for vespa
velutinani grithorax. Available at: https://secure.fera.defra.gov.uk/nonnativespecies/
downloadDocument.cfm?id=643
Martinez-Garcia, P.J., Dicenta, F., Ortega, E., 2012. Anomalous embryo sac
development and fruit abortion caused by inbreeding depression in almond
(Prunus dulcis). Scientia Horticulturae 133, 2330.
Meeus, I., Brown, M.J.F., de Graaf, D.C., Smagghe, G., 2011. Effects of Invasive
parasites on bumble bee declines. Conservation Biology 25 (4), 662671.
Melndez-Ramrez, V., Parra-Tabla, V., Kevan, P., et al., 2004. Mixed mating
strategies and pollination by insects and wind in coconut palm (Cocos nucifera
L. (Arecaceae)): Importance in production and selection. Agricultural and Forest
Entomology 6 (2), 155163.
Morandin, L.A., Winston, M.L., 2006. Pollinators provide economic incentive to
preserve natural land in agroecosystems. Agriculture Ecosystems and
Environment 116, 289292.
Ngo, H.T., Gemmill-Herren, B., Packer, L., 2012. The valuation of pollinators for
Southeast Asia: The Philippines and Vietnam.
Nyeki, J., Stolesz, M., 2003. Pear (Pyrus communis L.). In: Kozma, P., Nyeki, J.,
Stolesz, M., Szabo, Z. (Eds.), Floral Biology, Pollination and Fertilisation in
Temperate Zone Fruit and Grape. Budapest: Akademiai Kiado, pp. 531582.
Ollerton, J., Winfree, R., Tarrant, S., 2011. How many owering plants are pollinated
by animals? Oikos 120 (3), 321326.
Olschewski, R., Tscharntke, T., Benitez, P.C., Schwarze, S., Klein, A.-M., 2006.
Economic evaluation of pollination services comparing coffee landscapes in
Ecuador and Indonesia. Ecology and Society 11 (1), 7.
Otterstatter, M.C., Thomson, J.D., 2011. Does pathogen spillover from commercially
reared bumble bees threaten wild pollinators? PLoS One 3 (7), e2771.
Partap, U., Ya, T., 2012. The human pollinators of fruit crops in Maoxian county,
Sichuan, China. Mountain Research and Development 32 (2), 176186.
Pinillos, V., Cuevas, J., 2008. Articial pollination in tree crop production.
Horticultural Reviews 34, 239276.
Potts, S.G., Biesmeijer, J.C., Kremen, C., et al., 2010a. Global pollinator declines;
trends, impacts and drivers. Trends in Ecology and Evolution 25, 345353.
Potts, S.G., Roberts, S.P.M., Dean, R., et al., 2010b. Declines of managed
honeybees and beekeepers in Europe. Journal of Apicultural Research 49, 1522.
Potts, S.G., Woodcock, B.A., Roberts, S.P.M., et al., 2009. Enhancing pollinator
biodiversity in intensive grasslands. Journal of Applied Ecology 46 (2), 369379.
Pywell, R.F., Meek, W.R., Loxton, R.G., et al., 2011. Ecological restoration on
farmland can drive benecial functional responses in plant and invertebrate
communities. Agriculture Ecosystems and Environment 140, 6267.
Rader, R., Howlett, B.G., Cunningham, S.A., Westcott, D.A., Edwards, W., 2011.
Spatial and temporal variation in pollinator effectiveness: Do unmanaged insects
provide consistent pollination services to mass owering crops? Journal of
Applied Ecology 46, 10801087.
Rader, R., Howlett, B.G., Cunningham, S.A., et al., 2009. Alternative pollinator taxa
are equally efcient but not as effective as the honeybee in a mass owering
crop. Journal of Applied Ecology 46 (5), 10801087.
417
418
Crop Pollination
Vicens, N., Bosch, J., 2000b. Pollinating efcacy of Osmia cornuta and Apis
mellifera (Hymenoptera: Megachilidae, Apidae) on red Delicious apple.
Environmental Entomology 29 (2), 235240.
Volz, R.K., Tustin, D.S., Ferguson, I.B., 1996. Pollination effects on fruit mineral
composition, seeds and cropping characteristics of Braeburn apple trees.
Scientia Horticulturae 66 (34), 169180.
Westphal, C., Steffan-Dewenter, I., Tscharntke, T., 2003. Mass owering crops
enhance pollinator densities at a landscape scale. Ecology letters 6 (11),
961965.
Williams, I.H., Simpkins, J.R., Martin, A.P., 1991. Effects of insect pollination on
seed production in linseed (Linum usitatissimum). Journal of Agricultural
Science 117 (1), 7579.
Willmer, P.G., Bataw, A.A.M., Hughes, J.P., 1994. The superiority of bumblebees to
honeybees as pollinators: insect visitors to raspberry owers. Ecological
Entomology 19 (3), 271284.
Winfree, R., Aguilar, R., Vazquez, D.P., LeBuhn, G., Aizen, M., 2010. A metaanalysis of bees' responses to anthropogenic disturbance. Ecology 90,
20682076.
Winfree, R., Gross, B.J., Kremen, C., 2011. Valuing pollination services to
agriculture. Ecological Economics 71, 8088.
Winfree, R., Williams, N.M., Gaines, H., Ascher, J.S., Kremen, C., 2008. Wild bee
pollinators provide the majority of crop visitation across land-use gradients in
New Jersey and Pennsylvania. Journal of Applied Ecology 45 (3), 793802.
World Bank 2012. Economic policy & external debt data. Available at: http://data.
worldbank.org/topic/economic-policy-and-external-debt (accessed on 07.11.12).
Woodcock, B., Edwards, M., Redhead, J., et al., 2013. Crop ower visitation by
honeybees, bumblebees and solitary bees: Behavioural differences and diversity
responses to landscape. Agriculture Ecosystems and Environment 171, 18.
Wratten, S.D., Gillespie, M., Decourtye, A., Mader, E., Desneux, N., 2012. Pollinator
habitat enhancement: benets to other ecosystem services. Agriculture
Ecosystems and Environment 159, 112122.
Yang, E.C., Chuang, Y.C., Chen, Y.L., Chang, L.H., 2008. Abnormal foraging
behavior induced by sublethal dosage of Imidacloprid in the honey bee
(Hymenoptera: Apidae). Journal of Economic Entomology 101 (6), 17431748.
D
Dairy Animals
J Gupta, ID Gupta, and MV Chaudhari, National Dairy Research Institute, Karnal, Haryana, India
r 2014 Elsevier Inc. All rights reserved.
Glossary
Age at rst calving The age from the date of birth to date
of rst calving.
Breed A group of animals related by descent and having
similar appearance, behavior, and most of the other
characteristics.
Crossbreeding The mating of animals of different breeds.
Crossbreeding is followed for breeding animals for milk and
meat production. In India, zebu nondescript cows are
crossed with exotic breeds, like Holstein Friesian, Brown
Swiss, and Jersey bulls or their semen, to enhance the milk
production potential of the progeny.
305-days milk yield Milk yield produced up to 305 days
of lactation.
Cattle
Dry period The period from the date of dry to the date of
next calving.
Gestation period The period from the date of conception
to the date of calving.
Lactation length The period from the date of calving to
the date of dry.
Lactation milk yield Total milk yield produced by a cow
or a buffalo in complete lactation.
Service period The period from the date of calving to the
date of conception.
Species A group of individuals that have certain common
characteristics, which distinguish them from other group of
individuals and are capable of interbreeding and producing
fertile offspring.
Body Weights
Animals belonging to the phylum Chordata (backbone animals), class Mammalia (milk giving), order Artiodactyla (even
toed and hoofed), suborder Ruminatia (cud-chewing), family
Bovidae (hollow unbranched horn), and genus Bos (ruminant
quadrupeds) are cattle.
Cattle can be broadly classied into dairy and beef cattle.
Dairy cattle are cows (adult females) that are bred for their
ability to produce milk. Beef cattle are bred for meat
production.
Utility
Milk, meat, draught, manure, and hide.
Domestication of Cattle
Time: 60006500 years BC.
Location: Old World.
Reason: Religious.
How: Aurochs.
Table 1
Kingdom
Phylum
Class
Order
Suborder
Family
Genus
Species
doi:10.1016/B978-0-444-52512-3.00131-5
Animalia
Chordata (backbone animals)
Mammalia (milk-giving)
Artiodactyla (even toed and hoofed)
Ruminatia (cud-chewing)
Bovidae (hollow unbranched horn)
Bos (ruminant quadrupeds)
1. Bos indicus (humped cattle)
2. Bos taurus (without any hump)
419
420
Dairy Animals
Table 2
Jersey
Origin: This breed was developed from the island of Jersey in
the English Channel off the coast of France.
Distinguishing characters:
Male
Female
Young
Group
Act of mating
Gestation/pregnancy period
Dairy cattle
Bull
Cow/heifer
Calf
Herd/drove
Serving
9 months
Calve
Table 3
S. No.
Native breed
Specic region
Remarks
1
2
3
4
5
Brown Swiss
Holstein Friesian
Jersey
Guernsey
Ayrshire
Switzerland
Holland
British Isles
Guernsey
Scotland
Dairy
Dairy
Dairy
Dairy
Dairy
Table 4
breed
breed
breed
breed
breed
Group
Particulars
Name of breeds
First
Lyre-horned gray cattle with white foreheads, prominent orbital arches, and faces with
at or dished proles
Second
Shorthorned, white or light gray with cofn-shaped skull, orbital arches, and faces with
convex proles
Third
Heavy body build, pendulous dewlap and sheath, prominent forehead, spotted red or
white, or various sheds of red and white
Fourth
Mysore-type cattle. Forehead is prominent and the horns emerge from the top of the poll
fairly close together in upward and backward direction
Fifth
Heterogeneous mixture small, black, red, or dun cattle often with large patches and
white markings. Found in Himalayan region and rugged terrain
Sixth
Dhanni (Pakistan)
Source: Reproduced from Banerjee, G.C., 2010. A Textbook of Animal Husbandry, eigth ed. New Delhi: Oxford and IBH publishing Co. Pvt. Ltd.
Dairy Animals
Holstein Friesian
Sahiwal
Gir
Red Sindhi
421
Table 5
S. No.
Native breed
1
2
Angus
Nellore
Scotland
India
Table 6
Deoni
Name
Inheritance
Taylor
Jersind
Karan Swiss
Karan Fries
Sunandini
Frieswal
Place
Local cows
Kankrej, Gir, Hariana, Sahiwal, and Red Sindhi
Sahiwal and Red Sindhi
Tharparkar
Local nondescript
Sahiwal
Ayrshire
Holstein Friesian, Brown-Swiss, Jersey, and Guernsey
Brown-Swiss
Holstein Friesian
Brown-Swiss
Holstein Friesian
Patna (Bihar)
Allahabad (Uttar Pradesh)
NDRI, Karnal (Haryana)
NDRI, Karnal (Haryana)
Kerala
Military Dairy Farm
Table 7
Breeds
Hariana
Sahiwal
Tharparkar
Red
Sindhi
Gir
Ongole
Deoni
4149
3848
3953
3949
434523
418473
418474
436562
136303
136189
130183
152158
7301170
15972125
13262139
13121694
257315
228330
268317
284345
4461
3642
4755
456541
529637
456472
135259
210241
173192
11251859
658999
8181041
230394
279
282302
Source: Reproduced from Indian Council of Agricultural Research, 2008. Handbook of Animal Husbandry. New Delhi: Indian Council of Agricultural Research.
422
Dairy Animals
Hariana
Cow Nutrition
Average rates of daily feeding of concentrates and green and
dry fodder assumed for different stages of life of cattle are
given in Table 8.
Tharparkar
Heifer
Heifer is a young female cow before she has had her rst calf.
Heifers are selected on the basis of progeny testing, i.e., the potential of the sire and milk production of the dam, their proper
growth, good health, and freeness from any genetic abnormality.
Kankrej
Bull
Bulls contribute 50% of the inheritance to the next generation.
Most of the genetic improvement in a population comes
through proper bull selection. It is not very practicable to have
intense selection of the females for breeding, i.e., almost
all the heifers will have to be reared and used for breeding
in a situation where age at rst calving and calving interval
are not optimum. Hence, most care is to be given for bull
selection.
Kangayam
Also known by other names of Kanganad and Kongu, although the name Kangayam is well known. These cattle are
bred in the southern and southeastern area of the Erode
district of Tamil Nadu in India.
Best suited for plowing and transport. Withstands hardy
conditions.
Amritmahal
Cattle Breeding
Hallikar
Umblacherry
Origin: Tanjore district in Tamil Nadu.
Distinguishing characters:
Table 8
Reproduction is an important consideration in the economics of cattle production. In the absence of regular
breeding and calving at the appropriate time, cattle rearing
will not be protable. A healthy calf each year is the usual
goal. This is possible only by increasing the reproductive
efciency of the animals.
Successful reproduction encompasses the ability to mate,
the capacity to conceive and to nourish the embryo, and
deliver the viable young ones at the end of a normal gestation period. In fact, interruption in this chain of events
Average rates of daily feeding of concentrates and green and dry fodder assumed for different age groups of cattle
Cattle
Crossbred (milch)
Females 43 years of age
Males 43 years of age
Males o3 years of age
Concentrate (kg)
2.75
1.20
0.125
0.17
1.50
0.016
20.0
10.00
3.5
4.96
10.00
1.58
6.00
6.00
3.16
5.65
2.00
1.47
Source: Reproduced from Banerjee, G.C., 2010. A Textbook of Animal Husbandry, eigth ed. New Delhi: Oxford and IBH publishing Co. Pvt. Ltd.
Dairy Animals
423
Cattle Population
According to the FAOSTAT in the year 2010, there were 1428.7
million cattle stock. Among those with approximately 210.2
million cattle stock, India is the country with the largest cattle
population, contributing approximately 14.7% to the world,
followed by Brazil (209.5 million), the United States (93.9
million), and China (83.8 million).
Housing Systems
In the UK, there are three main options available for housing
dairy cattle.
Cubicles
Straw (loose) yards
Kennels.
424
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Dairy Animals
Types of housing
In India except in some organized dairy farms- owned by
government, co-operatives or military- the prevalent practice
is to tie the cows with rope on a Katcha oor. It is quite easy
to understand that unless cattle are provided with good
Cattle shed
The entire shed should be surrounded by a boundary wall of
5 ft height from three sides and manger, etc. on one side. The
feeding area should be provided with 22.5 ft of manger space
per cow. All along the manger, there shall be a 10-in.-wide
water trough to provide clean drinking water. The water trough
thus constructed will also minimize the loss of fodders during
feeding. Near the manger, under the roofed house, 5-foot-wide
oor should be paved with bricks having a little slope.
Shed for calves
On one side of the main cattle shed there should be a fully
covered shed of 10 15 sq ft area to accommodate young
calves. Such sheds with suitable partitioning may also serve as
calving pen under adverse climatic conditions. Beyond this
covered area, there should be a 20 10 sq ft open area having
boundary wall so that calves may move there freely. In this
way, both calf and cattle sheds will need in all a 50 50 sq ft
area for 20 adult cows and followers. If one has limited resources, they can build ordinary, Katcha/semikatcha (mud/
semimud) boundary walls; however, feeding and water trough
should be cemented ones.
Conventional dairy barn
The conventional dairy barns are comparatively costly and are
now becoming less popular day by day. However, by this system, cattle are more protected from adverse climatic condition.
The following barns are generally needed for proper
housing of different classes:
Dairy Animals
Calving box
Isolation box
Sheds for young stocks
Bull or bullock sheds.
Cow sheds
Cow sheds can be arranged in a single row if the number of
cows is less say, less than 10 and in a double row if the
herd is a large one. Ordinarily, not more than 80100 cows
should be placed in one building. In double-row housing, the
stable should be so arranged that the cows face out (tail-to-tail
system) or face in (head-to-head system) as preferred.
Advantages of tail-to-tail system:
Floor
The inside oor of the barn should be of some impervious
material that can be easily kept clean and dry and is not
slippery. Paving with bricks can also serve ones purpose.
Grooved cement concrete oor is still better. The surface of the
cowshed should be laid with a gradient of 11 14 in. from
manger to excreta channel. An overall oor space of 6570 sq
ft per adult cow should be satisfactory.
Walls
The inside of the walls should have a smooth hard nish of
cement, which will not allow any lodgment of dust and
moisture. Corners should be round. For plains, dwarf walls,
approximately 45 ft in height, and roofs supported by masonry work or iron pillars are best or more suitable. The open
space in between supporting pillars serves for light and air
circulation.
425
Roof
Roof of the barn may be of asbestos sheet or tiles. Corrugated
iron sheets have the disadvantage of making extreme uctuations in the inside temperature of the barn in different seasons. However, iron sheets with aluminum-painted tops to
reect sunrays and bottoms provided with wooden-insulated
ceilings can also achieve the objective. A height of 8 ft at the
sides and 15 ft at the ridge is sufcient to give the necessary
air space to the cows. An adult cow requires at least approximately 800 cubic ft of air space under tropical conditions. To
make ventilation more effective, continuous ridge ventilation
is considered most desirable.
Manger
Cement concrete continuous manger with removable partitions is the best from the point of view of durability and
cleanliness. A height of 1 ft to 4 in. for a high-front manger
and 69 in. for a low-front manger is considered sufcient.
Low-front mangers are more comfortable for cattle, but highfront mangers prevent feed wastage. The height at the back of
the manger should be kept at 2 ft to 63 in. An overall width
of 22.5 ft is sufcient for a good manger.
Alleys
The central walk should have a width of 56 ft exclusive of
gutters when cows face out and 45 ft when they face in. The
feed alley, in case of a face out system, should be 4 ft wide, and
the central walk should show a slope of 1 in. from the center
toward the two gutters running parallel to each other, thus
forming a crown at the center.
Manure gutter
The manure gutter should be wide enough to hold all dung
without getting blocked and be easy to clean. Suitable dimensions are 2 in. width with a cross-fall of 1 in. away from
standing. The gutter should have a gradient of 1 in. for every
10 ft length. This will permit a free ow of liquid excreta.
Doors
The doors of a single-range cowshed should be 5 in. wide with
a height of 7 ft, and for double-row shed the width should not
be less than 8 in. to 9 ft. All doors of the barn should lie at
against the external wall when fully open.
Calving boxes
Allowing cows to calve in the milking cowshed is highly undesirable and objectionable. It leads to unsanitary conditions
in milk production and spread of disease, like contagious
abortion in the herd. Special accommodation in the form of
loose boxes enclosed from all sides and with a door should be
furnished to all parturient cows. It should have an area of
approximately 100150 sq ft. With ample soft bedding, it
should be provided with sufcient ventilation through windows and ridge vent.
Isolation boxes
Animals suffering from infectious disease must be segregated
soon from the rest of the herd. Loose boxes of approximately
150 sq ft are very suitable for this purpose. They should be
situated at some distance from the other barns. Every isolation
426
Dairy Animals
box should be self-contained and should have separate connection to the drainage disposal system.
Sheds for young stocks
Calves should never be accommodated with adults in the
cowshed. The calf house must have provision for daylight
ventilation and proper drainage. Damp and ill-drained oors
cause respiratory trouble in calves to which they are susceptible. For an efcient management and housing, the young
stock should be divided into three groups, viz., young calves
(aged up to one year), bull calves (the male calves over one
year) and the female calves (above one year). Each group
should be sheltered in a separate calf house or calf shed. As far
as possible, the shed for the young calves should be quite close
to the cow shed. Each calf shed should have an open paddock
or exercise yard. An area of 100 sq ft per head for a stock of 10
calves and an increase of 50 sq ft for every additional calf
will make a good paddock. It is useful to classify the calves
below 1 year into three age groups, viz., calves below the age
of 3 months, 36-month-old calves, and those more than
6 months of age, for a better allocation of the resting area. An
overall covered space of:
1. 2025 sq ft per calf below the age of 3 months,
2. 2530 sq ft per calf from the age of 36 months,
3. 3040 sq ft per calf from the age of 612 months and
more, and
4. 4045 sq ft for every calf above 1 year. Provision of water
troughs inside each calf shed and exercise yard should
never be neglected.
Bull or bullock shed
Safety and ease in handling a comfortable shed, protection
from weather, and a provision for exercise are the key points
while planning accommodation for bulls or bullocks. A bull
should never be kept in connement, particularly on hard
oors. Such a connement without adequate exercise leads to
overgrowth of the hoofs creating difculty in mounting and
loss in the breeding power of the bull. A loose box with rough
cement concrete oor approximately 15 10 ft in dimensions
having an adequate arrangement of light and ventilation
and an entrance 4 ft in width and 7 ft in height will make
a comfortable housing for a bull. The shed should have a
manger and a water trough.
If possible, the arrangement should be such that water and
feed can be served without actually entering the bull house.
The bull should have a free access to an exercise yard provided
with a strong fence or a boundary wall of approximately 2 ft
height, i.e., too high for the bull to jump over. From the bull
yard, the bull should be able to view the other animals of the
herd so that it does not feel isolated (Banerjee, 2010).
Diseases in Cattle
Performance of cattle in the form of milk, meat, or hide production or reproduction is affected by a number of diseases
that may be caused by bacteria, virus, or protozoa or may
be due metabolic cause and nutritional deciencies. A few
important diseases of cattle are anthrax, black quarter, bovine
abortions, bovine mastitis, cow pox, foot-and-mouth disease,
hemorrhagic septicemia, leptospirosis, rinderpest, vibrionic
abortion, and metabolic disorders.
Anthrax
The disease usually occurs in an acute form; affected animals die within 2448 h of the onset of symptoms.
There is high fever with a hot, tense, painful swelling,
usually in one of the quarters, more often a hindquarter;
however, such swelling may also occur in the other quarter
before death. The swelling becomes cold and painless and
crepitates on pressure due to the presence of gas in it.
Prevention and control:
Dairy Animals
Foot-and-mouth disease
Hemorrhagic septicemia
Leptospirosis
Leptospirosis occurs in animals and humans in almost all
parts of the world. Serological evidence indicates the prevalence of leptospires among domesticated animals in different
parts of the country. The damage done to animal industry
results from the death of animals in the acute stage of illness;
stillbirth; abortion; stunning; decrease in weight (loss of
meat); reduced milk production; and unthriftiness.
Causes and pathogenesis:
The causative organisms of leptospirosis belong to the
genus Leptospira.
Symptoms:
Bovine mastitis
Symptoms:
427
428
Dairy Animals
Rinderpest
Metabolic diseases
Milk fever
Buffalo
Animal belonging to the phylum Chordata (backbone animals), class Mammalia (milk giving), order Artiodactyla (even
toed and hoofed), suborder Ruminatia (cud-chewing), family
Bovidae (hollow unbranched horn), and genus Bubalus (ruminant quadrupeds) is buffalo.
Zoological Classication
Table 9 explains the zoological classication of buffalo.
Domestication
Time: 25002100 BC.
Table 9
Kingdom
Phylum
Class
Order
Suborder
Family
Genus
Species
Table 10
Female
Serving
Herd
10 months
Calve
Dairy Animals
Utility
Milk, meat, draught, and manure.
Domestication
It has been suggested that buffaloes were in service of humans
as early as 25002100 BC. The domesticated buffaloes can be
classied into two main categories, i.e., (1) The swamp buffalo
(chromosomes, 2n 48) and (2) The river buffalo (chromosomes, 2n 50). They belong to the same species, B. bubalis,
but have very different habits. The former is more or less
permanent inhabitant of marsh lands, where it wallows in
mud and feeds on coarse marsh grass, and is found principally
in Malaya, Singapore, the Philippines, Thailand, Indonesia,
southern China, and other counties in the Far East. In the
Philippines and some other countries, it is known as the
Carabao and in Malaysia as the Kerban. The river type is
the one found throughout India, Pakistan, Bangladesh, Nepal,
and Sri Lanka. These are primarily milch animals (Banerjee,
2010). Water buffaloes were domesticated in India approximately 5000 years ago and in China approximately 4000 years
ago. Two types are recognized on the basis of morphological
and behavioral criteria the river buffalo of the Indian subcontinent and further west to the Balkans and Italy and the
swamp buffalo, found from Assam in the west through
Southeast Asia to the Yangtze valley in China in the east.
Breeds
In India there are 13 well-dened breeds with standard qualities and with specic physical characters that differentiate
them unmistakably from other types as may be found in
various states of the country. On the basis of regions, the welldened buffalo breeds are listed in Table 11.
Out of all these breeds, six breeds, viz., Murrah, Nili-Ravi,
Jaffarabadi, Bhadawari, Surti, and Mehsana are high-quality
milch breeds of the country and they all come from the
northern and western parts of the country comprising the
states of Punjab, Rajasthan, and Gujarat. The breeds of central
and western parts are noted as draught purpose due to the fact
that they have swamp as well as river characteristics.
429
and is either being bred in pure form or being used as improver breed for grading up local buffaloes. Murrah breed has
even found an important place in the livestock industry of
many developing countries like Bulgaria, the Philippines,
Malaysia, Thailand, China, Indonesia, Bangladesh, Nepal, the
former USSR, Myanmar, Vietnam, Brazil, and Sri Lanka. Milk
yield varies from place to place depending on the management
practices and environmental conditions under which animals
are reared. Large herds have shown average yields as 1800 kg.
Housing In the breeding tract, these buffaloes are kept in
a mixed type of housing system. The buffaloes are tied to a tree
or a pole in the open, but shelter is provided during extreme
weather conditions. Houses are well ventilated and mostly
made up of pucca (solid) walls with katcha (mud) oor.
Feeding Animals are mostly stall fed. Berseem, oat, and
mustard are the green fodders fed in Rabi season and pearl
millet, sorghum, and cluster bean in Kharif season. In lean
season, Murrah animals are maintained on wheat and pulse
straws in conjunction with oilcakes and other concentrates.
Mostly, women are engaged in buffalo rearing (80%), and all
the activities pertaining to feeding, milking, cleaning, etc. are
looked after by them. Calves are not weaned. Very few farmers
rear bulls exclusively for breeding purpose. Natural service is
mostly practiced in eld.
Nili-Ravi
Nili and Ravi were two different breeds long before, but due to
the passage of time and with intensive crossbreeding, the two
breeds converted into a single breed named Nili-Ravi. NiliRavi buffaloes are found in almost all the districts, with major
concentration in Amritsar, Gurdaspur, and Ferozepur districts
of Punjab in India and in Lahore, Sheikhupura, Faizabad,
Okora, Sahiwal, Multan, Bohawalpur, and Bahwalnagar districts of Punjab in Pakistan. However, due to good dairy
characteristics of this breed in Pakistan, Nili-Ravi buffaloes are
found in whole of Pakistan with major concentration in
buffalo colony at Karachi. The average lactation yield in
Nili-Ravi buffaloes range from 16882317 kg.
Banni, Kalahandi, and Chilika are newly registered buffalo
breeds in India.
Murrah
Banni
Table 11
Murrah group
Gujarat group
1.
2.
3.
4.
1. Surti
2. Jaffarbadi
3. Mehsana
1. Bharawari
2. Tarai
1.
2.
3.
4.
5.
6.
1. Toda
2. South Kanara
Murrah
Nili-Ravi
Kundi
Godavari
Nagapuri
Pandharapuri
Manda
Jerangi
Kalhandi
Sambalpuri
Source: Reproduced from Banerjee, G.C., 2010. A Textbook of Animal Husbandry, eigth ed. New Delhi: Oxford and IBH publishing Co. Pvt. Ltd.
430
Dairy Animals
Kalahandi
Kalahandi buffaloes are dual type; they are used both for milk
and draught purpose in Kalahandi and Rayagada districts of
Odisha. Animals are medium sized; have long, strong, and
half-circled horns with broad base; and are excellent in heat
and drought tolerance.
Heat Tolerance
Although buffaloes are found in greatest numbers in the tropics, they have poor heat resistance and suffer real distress if
worked during the heat of the day or if they are left to stand in
the direct rays of the sun for long periods. Access to water or
shade is essential for the well-being of buffaloes. It is customary to rest working buffaloes for several hours in the
middle of the day and to allow them to wallow at that time
and again in the early evening when the days work is over. It is
thus to be noted that sudden changes of temperature, especially the effect of cold winds and drought, may be extremely
harmful to this species. Heat-regulating mechanism of buffaloes in comparison with cattle is less efcient. The difference
may be due in part to the heavy coat of the cow preventing
wetting of the skin but more probably to the fact that the
thyroidadrenal mechanism is less efcient in buffaloes
(Banerjee, 2010).
Wallowing
It means rolling or oundering in mud or in water. The river
breeds of Indian subcontinent prefer the clear water of streams
and pools, bunching close together, but the swamp buffalo of
China and southeast Asia likes to wallow in slime and mudhole, accommodating one animal or very few animals only. It
is seldom that buffaloes are found in areas where there is no
easy access to water. Although wallowing is not absolutely
necessary for buffaloes to maintain themselves, they apparently wallow for two main reasons: to regulate body temperature and to control parasites. Moreover, there is no
denite pattern of wallowing (Banerjee, 2010).
Buffalos Nutrition
Goat
Animal belonging to the phylum Chordata (backbone animals), class Mammalia (milk-giving), order Artiodactyla (even
toed and hoofed), suborder Ruminatia (cud-chewing), family
Bovidae (hollow unbranched horn), and genus Capra is goat.
Domestication of Goat
Time: 90007000 BC.
Number of chromosome pairs of goat: 30 (Capra hircus)
Body Weights
Body weight in goat ranges from 2.53.5 kg at birth to 26
102 kg at maturity.
Table 13
Kingdom
Phylum
Class
Order
Suborder
Family
Genus
Species
Animalia
Chordata (backbone animals)
Mammalia (milk-giving)
Artiodactyla (even toed and hoofed)
Ruminatia (cud-chewing)
Bovidae (hollow unbranched horn)
Capra
Capra hircus (True goat including Bezoar)
Capra falconeri (Markhor)
Capra ibex
Capra caucasica (Caucasian tur)
Capra pyrenaica (Spanish ibex)
Average rates of daily feeding of concentrates and green and dry fodder assumed for different age groups of buffalo
Improved buffalo
Other milch buffalo and not calved even once
Concentrate (kg)
1.50
0.41
0.109
0.01
10.00
5.72
6.51
1.59
6.00
5.08
5.43
1.64
Source: Reproduced from Banerjee, G.C., 2010. A Textbook of Animal Husbandry, eigth ed. New Delhi: Oxford and IBH publishing Co. Pvt. Ltd.
Dairy Animals
Table 14
431
Male
Female
Young
Group
Act of mating
Gestation/pregnancy period
Goat
Buck
Nanny
Kid
Trip
Serving
148156 days
Kidding
Utility
Milk, meat, ber, manure, and hide.
Dairy goats
Alpine
Alpine goats are known for their very good milking ability.
They are multicolored and have no set markings. They have
erect ears, horns, and have a dish face. The breed originated in
the French Alps. Mature animals weigh approximately 61 kg or
125 lbs and are approximately 0.8 m or 30 in. tall at the
shoulder. Alpine goats can range in color from white or gray to
brown and black. Alpine goats are heavy milkers; the milk can
be made into butter, cheese, soap, ice cream, or any other dairy
product that cows milk can produce. They are most often used
for commercial milking. The French-alpine is also referred to
as the Alpine Dairy goat and registration papers for this dairy
goat use both designations, which are synonymous. These are
hardy, adaptable animals that thrive in any climate while
maintaining good health and excellent production. Alpine
goats milk has an average butterfat of approximately 3.5%.
The face is straight.
Alpine colors are described by using the following terms:
Broken Chamoisee a solid chamoisee broken with another color by being banded or splashed, etc. Any variation
in the above patterns broken with white should be described as a broken pattern, such as a broken coublanc
(Briggs and Briggs, 1980; American Dairy Goat Association,
n.d.).
Anglo-Nubians
These goats were developed in England by crossing British
goats with bucks of African and Indian origin. The AngloNubian is an all-purpose goat, useful for meat, milk, and hide
production. It is not a heavy milk producer but its milk has a
high average butterfat content (between 4% and 5%). As it is
best suited, of the dairy goat breeds, to hot conditions, the
Anglo-Nubian has been used in grading up programs in many
tropical countries to increase the milk and meat production of
local breeds. The Anglo-Nubian is a relatively large, proud, and
graceful dairy goat. It is named after Nubia, in northeastern
Africa. The original goats imported from Africa, Arabia, and
India were long legged, hardy goats that had some characteristics desired by goat breeders in England. English breeders
crossed these imported bucks on the common short-haired
does of England before 1895 to develop the Anglo-Nubian
goat. In the United States, the breed is usually spoken of as the
Nubian. The Anglo-Nubian is regarded as an aristocraticappearing goat and has very long, pendulous ears that hang
close to the head. It carries a decidedly Roman nose and is
always short haired. Any solid or parti-colored coat is permitted in the Anglo-Nubian, but black, red, or tan are the most
common colors, any of which may be carried on combination
with white. Usually there is shorter hair on the Anglo-Nubian
males, particularly along the back and on the thigh, than is
commonly found on the Swiss breeds. Its udder is capacious
but is sometimes more pendulous than that of the Swiss
breeds. A mature doe should stand at least 30 in. at the withers
and weigh 135 lbs or more, whereas the males should stand at
least 35 in. at the withers and weigh at least 175 lbs. It usually
gives less milk than the Swiss breeds but produces a milk of
higher butterfat content. The head is the distinctive breed
characteristic, with the facial prole between the eyes and the
muzzle being strongly convex. The ears are long (extending at
least 1 in. beyond the muzzle when held at along the face),
wide, and pendulous. They lie close to the head at the temple
and are slightly out and well forward at the rounded tip,
forming a bell shape. The ears are not thick, with the cartilage
well dened. The hair is short, ne, and glossy (Briggs and
Briggs, 1980; Mason, 1988; Meat and Livestock Australia,
1989; American Dairy Goat Association, n.d.).
Meat goats
Black Bengal
The Black Bengal goat is a breed of goat found in West Bengal,
Bihar, and Odisha regions of northeastern India and
432
Dairy Animals
Fiber goat
Angora
The Angora goat originated in the district of Angora in Asia
Minor. The Angora dates back before early Biblical history.
Mention is made of the use of mohair at the time of Moses,
which would x the record of the Angora sometime between
1571 and 1451 BC, according to the Angora Goat Mohair
Industry publication from the United States Department of
Agriculture. Mohair became a valuable product in commerce
early in the nineteenth century. To increase the supply of
mohair available for export to the European countries, the
Turks crossed the Angora goat with common stock to increase
the poundage of salable hair. Probably there was no effort to
keep the original Angora separate, and the general increase in
size and vigor of the goats in the Angora area was, undoubtedly, partially the result of this infusion of other blood.
Angora stock was distributed to different countries, and a pair
of Angoras was imported to Europe by Charles V around 1554.
Mohair production The most valuable characteristic of
the Angora as compared with other goats is the value of the
mohair that is clipped. The average goat in the US shears approximately 5.3 lbs of mohair per shearing and is usually
sheared twice a year. They produce a ber with a staple length
between 12 and 15 cm. The mohair is very similar to wool in
chemical composition but differs from wool in that it has a
much smoother surface and very thin, smooth scale. Consequently, mohair lacks the felting properties of wool. Mohair
is very similar to coarse wool in the size of ber. It is a strong
ber that is elastic, has considerable luster, and takes dye very
well. Mohair has been considered very valuable as an upholstering material for the making of plushes and other covering
materials where strength, beauty, and durability are desired
(Briggs, 1969; Select Genes Ltd., 1675; Meat and Livestock
Australia, 1989).
Housing management
Concentrates: These are low in crude ber and high in digestible nutrients. Concentrates low in protein are maize,
rice, sorghum, bran, molasses, etc., whereas protein-rich
concentrates are groundnut cake, cottonseed cake, soyabean meal, etc.
Roughage: These are high in crude ber but low in digestible nutrients, such as sorghum fodder, bajra fodder, rice
and wheat straw, grasses like paragrass and young pasture
grasses, silage, and dry hay.
Feed additives: There are chemicals that are added to feed
for growth promotion or for disease prevention, for example, antibiotics aureomycin, and terramycin.
Minerals: Salt, oyster shell, lime stone, bone meal, wood
ash, etc. supply minerals to goats body.
Dairy Animals
433
Goatskin Production
Aggregate 1 138 100 tons goatskin was produced throughout
the world in the year 2011.
Feeding the dry doe Feed well during the pregnancy as the
unborn babies gain more weight during the last week of
pregnancy. The pregnant doe should be in good esh and
weight before giving birth. Nutritious grasses and legumes are
sufcient to support the doe. If the pregnant doe looks thin
then give approximately 0.51 kg of concentrate mixture.
Feeding the doe about to kid 35 days before giving
birth, give pregnant doe approximately 250500 g of concentrate. Then 12 days before kidding, replace this concentrate ration with just maize, bran, wheat bran, or rice
bran. The bran is known for its laxative property and will
help to clean the stomach. Clean stomach will assist the
doe in easy kidding.
Feeding the milking doe Milk does should be given as
much quality grasses and legumes as they can consume.
Concentrate grams for every liter of milk should be given
and fresh water and mineral lick-brick should be provided
to the does frequently.
Feeding the bucks Bucks used for breeding should be fed
properly. When not used for breeding, feed a buck at least
500 g of concentrate mixture plus green grass and legume,
like lucerne. See that the does do not become fat, aggressive, and sterile. During breeding period, increase its ration
from 500 g to 1 kg.
Feeding young kids The object should be not to fatten
them up but rather provide them enough nutrients for
growth and maintenance. Sufcient space for exercise plus
abundant quality grass and legumes are important for
yearlings. Feed 500 g of concentrate every day.
Feeding the baby goats Keep the kids with the mother for
the rst 23 days. This will ensure sufcient intake of colostrum needed for their good health. From the 3rd or 4th
day, allow the kid to be with the mother only during the day.
Continue this up to 45 months, i.e., till they are weaned.
You can feed the kid with the help of a bottle. For this you
must separate the kid from the doe after the 3rd or 4th day of
its birth. Take care to keep the milk warm around 103
105 1F. Keep the nipple and bottle clean after each feeding.
Sheep
Animal belonging to the phylum Chordata (backbone animals), class Mammalia (milk giving), order Artiodactyla (even
toed and hoofed), suborder Ruminatia (cud-chewing), family
Bovidae (hollow unbranched horn), and genus Ovis is sheep.
Domestication of Sheep
An archeological site in Iran produced a statuette of a wooled
sheep, which suggests that selection for woolly sheep had
begun to occur more than 6000 years ago. The common features of todays sheep already appeared in Mesopotamian and
Babylonian art and books by 3000 BC.
Number of chromosome pairs of sheep: 54 (Ovis aries).
Body Weights
Body weight in sheep ranges from 2.04.0 kg at birth to 34
80 kg at maturity.
Utility
Milk, meat, eece, manure, and hide.
Goats Population
In the year 2011, there were 875.53 million goats in the world.
Kingdom
Phylum
Class
Order
Suborder
Family
Genus
Species
434
Table 16
Dairy Animals
Male
Female
Young
Group
Act of mating
Gestation/pregnancy period
Sheep
Buck/ram
Ewe/dam
Lamb
Flock
Tupping
148156 days
Lambing
References
In the year 2011, there were 1 043 712 633 sheep in the world.
Relevant Websites
Sheep Population
Sheeepskin Production
Aggregate 1 741 333 tons sheepskin was produced throughout
the world in the year 2011.
Wool Production
1 985 797 tons of wool (greasy) was produced throughout the
world in the year 2011.
www.bieap.gov.in
Board of Intermediate Education Andhra Pradesh.
www.buffalopedia.cirb.res.in
Buffalopedia Central Institute for Research on Buffaloes, Indian Council of
Agricultural Research.
www.cirb.res.in
Central Institute for Research on Buffaloes.
www.dairyco.org.uk
Dairyco.
www.ansi.okstate.edu
Department of Animal Science, Oklahoma State University.
www.faostat.org
FAOSTAT production data.
www.nbagr.res.in
National Bureau of Animal Genetic Resources.
www.agritech.tnau.ac.in
Tamil Nadu Agricultural University agritech portal.
www.inseda.org
The Integrated Sustainable Energy and Ecological Development Association
(INSEDA).
www.wikipedia.org
Wikipedia, the free encyclopedia.
www.world-agriculture.com
World Agriculture.
Glossary
Bovine Cattle or closely related ruminants.
Enterotoxins Toxins elaborated by some strains of
Staphylococcus aureus that may cause gastrointestinal signs
(vomiting, diarrhea, etc.) when ingested by a person.
Mastitis Inammation of the mammary gland, usually
caused by microorganisms infecting the gland.
Staphylococcus aureus
Streptococcus spp. (Streptococcus agalactiae, Streptococcus dysgalactiae, Streptococcus uberis, etc.)
Trueperella pyogenes (formerly Arcanobacterium pyogenes)
Mycoplasma spp.
Escherichia coli
Klebsiella spp.
Many of these mastitis-causing pathogens and other possible mastitis-causing microorganisms can be present in the
dairy environment and can pose a threat to dairy cows.
doi:10.1016/B978-0-444-52512-3.00197-2
435
436
437
20
2002
18
16.4
15.0
2007
% of cows treated
16
14
12
10
7.4
8
4.9
6
4
7.0 7.1
2.2
2.8
2.0 1.9
0.2
0.5
0
Respiratory
Diarrhea or Reproductive
other
digestive
problems
Mastitis
Lameness
Other
Figure 1 Use of antibiotics at dairy farms in the United States during the previous 12 months of 2002 and 2007. Reproduced from United States
Department of Agriculture, Animal Plant Health Inspection Service National Animal Health Monitoring System (USDA APHIS, 2008). Antibiotic use
on U.S. dairy operations, 2002 and 2007. Available at: http://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_
AntibioticUse.pdf (accessed 05.05.13).
438
60
53.2
2002
% of antibiotics used
50
2007
36.8
40
33.8
30
19.1
20
21.3
19.4
4.9
1.9
10
2.9
NA
1.0 0.2
0.0 0
2.8
0.2
0.71.2
3.1 2
1.8
0.5
0
l
lito
yc
c
ino
Am
ino
Am
rin
po
s
alo
l
n
e
e
ide
ide
ico
lid
ori
tam
clin
sp
am
am
fen
cro
cy
r
s
o
n
l
a
a
o
o
o
r
l
a
t
c
M
lf
F
ph
Te
Su
Lin
Ce
ac
-l
eta
he
Ot
ep
nc
No
ide
os
c
gly
Figure 2 Percentage of primary antibiotic used for treatment of cows during the previous 12 months of 2002 and 2007. Reproduced from the
data presented in USDA APHIS United States Department of Agriculture, Animal Plant Health Inspection Service National Animal Health Monitoring
System, 2008. Antibiotic use on U.S. dairy operations, 2002 and 2007. Available at: http://www.aphis.usda.gov/animal_health/nahms/dairy/
downloads/dairy07/Dairy07_is_AntibioticUse.pdf (accessed 05.05.13).
References
Anderson, K.L., Lyman, R.L., 2006. Long-term persistence of specic genetic types
of mastitis-causing Staphylococcus aureus on three dairies. Journal of Dairy
Science 89, 45514556.
Anderson, K.L., Lyman, R.L., Bodeis-Jones, S.M., White, D.G., 2006. Genetic
diversity and antimicrobial susceptibility proles among mastitis-causing
Staphylococcus aureus isolated from bovine milk samples. American Journal of
Veterinary Research 67, 11851191.
Aquino, G.deV., Maluta, R.P., de vila, F.A., 2012. Prevalence of methicillin-resistant
Staphylococci on a farm: Staff can harbor MRS when animals do not. Zoonoses
and Public Health 59, 13.
Asao, T., Kumeda, Y., Kawai, T., et al., 2003. An extensive outbreak of
staphylococcal food poisoning due to low-fat milk in Japan: Estimation of
enterotoxin A in the incriminated milk and powdered skim milk. Epidemiology
and Infection 130, 3340.
Barkema, H.W., Green, M.J., Bradley, A.J., Zadoks, R.N., 2009. The role
of contagious disease in udder health. Journal of Dairy Science 92,
47174729.
Boerlin, P., Kuhnert, P., Hussy, D., Schaellibaum, M., 2003. Methods for
identication of Staphylococcus aureus isolates in cases of bovine mastitis.
Journal of Clinical Microbiology 41, 767771.
Bramley, A.J., Dodd, F.H., 1984. Reviews of the progress in dairy science:
Mastitis controlprogress and prospects. Journal of Dairy Research 51,
481512.
Capurro, A., Aspn, A., Unnerstad, H.E., Waller, K.P., Artursson, K., 2010.
Identication of potential sources of Staphylococcus aureus in herds with
mastitis problems. Journal of Dairy Science 93, 180191.
Cosgrove, S.E., 2006. The relationship between antimicrobial resistance and patient
outcomes: Mortality, length of hospital stay, and health care costs. Clinical
Infectious Diseases 42, S82S89.
Cuny, C., Nathaus, R., Layer, F., et al., 2009. Nasal colonization of humans with
methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without
exposure to pigs. PLos One 4, e6800.
Devriese, L.A., Van Damme, L.R., Famaree, L., 1972. Methicillin (cloxacillin)resistant Staphylococcus aureus strains isolated from bovine mastitis cases.
Zentralblatt fur Veterinarmedizin Reihe B 19, 598605.
Dosogne, H., Vangroenweghe, F., Mehrzad, J., Massart-Leen , A.M., Burvenich, C.,
2003. Differential leukocyte count method for bovine low somatic cell count milk.
Journal of Dairy Science 86, 828834.
Doyle, M.E., Hartmann, F.A., Wong, A.C.L., 2012. Methicillin-resistant staphylococci:
Implications for our food supply? Animal Health Research Reviews 13,
157180.
Erskine, R., Cullor, J., Schaellibaum, M., Yancey, B., Zecconi, A., 2004.
Subcommittee of the NMC Research Committee: Bovine mastitis pathogens and
trends in resistance to antibacterial drugs. NMC Annual Meeting Proceedings,
pp. 400414. Verona, WI: National Mastitis Council.
Erskine, R.J., Walker, R.D., Bolin, C.A., Bartlett, P.C., White, D.G., 2002. Trends in
antibacterial susceptibility of mastitis pathogens during a seven-year period.
Journal of Dairy Science 85, 11111118.
439
Ferreira, J.P., Correa, M.T., Lyman, R., Anderson, K.L., 2012. A review of
methicillin-resistant Staphylococcus aureus (MRSA) in dairy cattle. Bovine
Practitioner 46, 19.
Fessler, A., Scott, C., Kadlec, K., et al., 2010. Characterization of methicillinresistant Staphylococcus aureus ST398 from cases of bovine mastitis. Journal of
Antimicrobial Chemotherapy 65, 619625.
Garca-lvarez, L., Holden, M.T., Lindsay, H., et al., 2011. Methicillin-resistant
Staphylococcus aureus with a novel mecA homologue in human and bovine
populations in the UK and Denmark: A descriptive study. Lancet Infectious
Diseases 11, 595603.
Graveland, H., Duim, B., van Duijkeren, E., Heederik, D., Wagenaar, J.A., 2011.
Livestock-associated methicillin-resistant Staphylococcus aureus in animals and
humans. International Journal of Medical Microbiology 301, 630634.
Haran, K.P., Godden, S.M., Boxrud, D., et al., 2012. Prevalence and characterization
of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus,
isolated from bulk tank milk from Minnesota dairy farms. Journal of Clinical
Microbiology 50, 688695.
Hogan, J.S., Berry, E., Hillerton, E., et al., 2011. Current Concepts of Bovine
Mastitis, fth ed. Verona, WI: National Mastitis Council.
Huber, H., Koller, S., Giezendanner, N., Stephan, R., Zweifel, C., 2009. Prevalence
and characteristics of methicillin-resistant Staphylococcus aureus in humans in
contact with farm animals, in livestock, and in food of animal origin, Switzerland.
Euro Surveillance 15, 14.
Jayarao, B.M., Pillai, S.R., Sawant, A.A., Wolfgang, D.R., Hegde, N.V., 2004.
Guidelines for monitoring bulk tank milk somatic cell and bacterial counts.
Journal of Dairy Science 87, 35613573.
Jevons, M.P., 1961. Celbenin-resistant staphylococci. British Medical Journal 1,
124125.
Jones, T.F., Kellum, M.E., Porter, S.S., Bell, M., Schaffner, W., 2002. An outbreak of
community-acquired foodborne illness caused by methicillin-resistant
Staphylococcus aureus. Emerging Infectious Diseases 8, 8284.
Juhsz-Kaszanyitzky, E., Jnosi, S., Somogyi, P., et al., 2007. MRSA transmission
between cows and humans. Emerging Infectious Disease 13, 630632.
Kelly, A., Tiernan, D., OSullivan, C., Joyce, P., 2000. Correlation between bovine
milk somatic cell count and polymorphonuclear leukocyte level for samples of
bulk milk and milk from individual cows. Journal of Dairy Science 83,
300304.
Kitchen, B.J., 1981. Review of the progress of dairy science: Bovine mastitis: Milk
compositional changes and related diagnostic tests. Journal of Dairy Research
48, 167.
Kluytmans, J., van Leeuwen, W., Goessens, W., et al., 1995. Food-initiated outbreak
of methicillin-resistant Staphylococcus aureus analyzed by phenotyping and
genotyping. Journal of Clinical Microbiology 33, 11211128.
Kck, R., Loth, B., Kksal, M., et al., 2012. Persistence of nasal colonization with
livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers
after holidays from pig exposure. Applied and Environmental Microbiology 78,
40464047.
Kck, R., Schaumburg, F., Mellmann, A., et al., 2013. Livestock-associated
methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection
and colonization in Germany. Plos One 8, e55040.
Koess, C., Hamann, J., 2008. Detection of mastitis in the bovine mammary
gland by ow cytometry at early stages. Journal of Dairy Research 75,
225232.
Koskinen, M.T., Wellenberg, G.J., Sampimon, A.C., et al., 2010. Field comparison of
real-time polymerase chain reaction and bacterial culture for identication of
bovine mastitis bacteria. Journal of Dairy Science 93, 57075715.
Leitner, G., Shoshani, E., Krifucks, O., Chaffer, M., Saran, A., 2000. Milk leucocyte
population patterns in bovine udder infection of different aetiology. Journal of
Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 47,
581589.
Lievaart, J.J., Kremer, W.D.J., Barkema, H.W., 2007. Short communication:
Comparison of bulk milk, yield-corrected, and average somatic cell counts as
parameters to summarize the subclinical mastitis situation in dairy herd. Journal
of Dairy Science 90, 41454148.
Lindmark-Man sson, H., Bran ning, C., Alden , G., Paulson, M., 2006. Relationship
between somatic cell count, individual leukocyte populations and milk
components in bovine udder quarter milk. International Dairy Journal 16,
717727.
Marrack, P., Kappler, J., 1990. The staphylococcal enterotoxins and their relatives.
Science 248, 705711.
Matthews, K.R., Kumar, S.J., OConner, S.A., et al., 1994. Genetic ngerprints of
Staphylococcus aureus of bovine origin by polymerase chain-based DNA
ngerprinting. Epidemiology and Infection 112, 177186.
440
Merle, R., Schroder, A., Hamann, J., 2007. Cell function in the bovine mammary
gland: A preliminary study on interdependence of healthy and infected udder
quarters. Journal of Dairy Research 74, 174179.
Nielen, M., Deluyker, H., Schukken, Y.H., Brand, A., 1992. Electrical conductivity of
milk: Measurement, modiers, and meta analysis of mastitis detection
performance. Journal of Dairy Science 75, 606614.
Noskin, G.A., Rubin, R.J., Schentag, J.J., et al., 2005. The burden of Staphylococcus
aureus infections on hospitals in the United States: An analysis of the 2000 and
2001 nationwide inpatient sample database. Archives of Internal Medicine 165,
17561761.
Olechnowicz, J., Jakowski, J.M., 2012. Somatic cells count in cows bulk tank milk.
Journal of Veterinary Medical Science 74, 681686.
Oliver, S.P., Murinda, S.E., 2012. Antimicrobial resistance of mastitis pathogens.
Veterinary Clinics of North America: Food Animal Practice 28, 165185.
Oshima, M., 1977. Detection of abnormal quarter milk by the quarter difference of
the electrical conductivity and its theoretical basis. Japan Agricultural Research
Quarterly 11, 239.
Owens, W.E., Watts, J.L., 1988. Antimicrobial susceptibility and beta-lactamase
testing of staphylococci isolated from dairy herds. Journal of Dairy Science 71,
19341939.
Pantoja, J.C., Hulland, C., Ruegg, P.L., 2009. Dynamics of somatic cell counts and
intramammary infections across the dry period. Preventive Veterinary Medicine
90, 4354.
Piddock, L.J.V., 1996. Does the use of antimicrobial agents in veterinary medicine
and animal husbandry select antibiotic resistant bacteria that infect man and
compromise antimicrobial chemotherapy? Journal of Antimicrobial Chemotherapy
38, 13.
Pilla, R., Schwarz, D., Konig, S., Piccinini, R., 2012. Microscopic differential cell
counting to identify inammatory reactions in dairy cow quarter milk samples.
Journal of Dairy Science 95, 44104420.
Rivas, A.L., Quimby, F.W., Blue, J., Coksaygan, O., 2001. Longitudinal evaluation of
bovine mammary gland health status by somatic cell counting, ow cytometry,
and cytology. Journal of Veterinary Diagnostic Investigation 13, 399407.
Sarikaya, H., Schlamberger, G., Meyer, H.H., Bruckmaier, R.M., 2006. Leukocyte
populations and mRNA expression of inammatory factors in quarter milk
fractions at different somatic cell score levels in dairy cows. Journal of Dairy
Science 89, 24792486.
Scallan, E., Hoekstra, R.M., Angulo, F.J., et al., 2011. Foodborne illness acquired in
the United States-major pathogens. Emerging Infectious Disease 17, 715.
Schalm, O.W., Carroll, E.J., Jain, N.C., 1971. Bovine Mastitis. Philadelphia, PA: Lea
& Febiger.
Schwarz, D., Diesterbeck, U.S., Konig, S., et al., 2011. Microscopic differential cell
counts in milk for the evaluation of inammatory reactions in clinically healthy
and subclinically infected bovine mammary glands. Journal of Dairy Research 78,
448455.
Shore, A.C., Deasy, E.C., Slickers, P., et al., 2011. Detection of staphylococcal
cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1,
blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillinresistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 55,
37653773.
Sommerhuser, J., Kloppert, B., Wolter, W., et al., 2003. The epidemiology of
Staphylococcus aureus infections from subclinical mastitis in dairy cows during
a control programme. Veterinary Microbiology 96, 91102.
United States Department of Agriculture, Animal Plant Health Inspection Service
National Animal Health Monitoring System (USDA APHIS, 2008). Antibiotic use
on U.S. dairy operations, 2002 and 2007. Available at: http://www.aphis.usda.
gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_AntibioticUse.pdf
(accessed on 05.05.13).
Vanderhaegen, W., Cerpentier, T., Adriaensen, C., et al., 2010. Methicillin-resistant
Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical
mastitis in Belgian cows. Veterinary Microbiology 144, 166171.
Virgin, J.E., van Slyke, T.M., Lombard, J.E., Zadoks, R.N., 2009. Short
communication: Methicillin-resistant Staphylococcus aureus detection in US bulk
tank milk. Journal of Dairy Science 92, 49884991.
Weese, J.S., 2010. Methicillin-resistant Staphylococcus aureus in animals. ILAR
Journal 51, 233244.
Wulf, M.W., Sorum, M., van Nes, A., et al., 2008. Prevalence of methicillin-resistant
Staphylococcus aureus among veterinarians: An international study. Clinical
Microbiology and Infectious Diseases 14, 2934.
Relevant Websites
http://nmconline.org
National Mastitis Council.
http://www.cdc.gov/mrsa/
US Centers for Disease Control and Prevention.
Glossary
Gangliosides Glycolipids with negatively charged glycans
containing one or more sialic acid residues.
Glycoconjugate Molecule in which one or more glycan
units are covalently linked to a noncarbohydrate entity
(e.g., protein or lipid).
Glycolipids Lipids with one or more glycans attached.
Glycoprotein Protein with one or more covalently bound
glycans.
Mass spectrometry Analytical technique that measures the
charge-to-mass-ratios of molecules.
Oligosaccharides Carbohydrates consisting of between
2 and 20 monosaccharides, linear or branched connected by
doi:10.1016/B978-0-444-52512-3.00067-X
441
442
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
2
1
3
New
products
4
8
in vivo
6
in vitro
Figure 1 Functional ingredient development life cycle: (1) desired optimal physiological conditions are identied and associated with related
biological processes and biochemical pathways; (2) development of health targets; (3) provisioning of health targets enables the identication of
potential bioactive mediators; (4) lab separation techniques can deconstruct foods and their processing efuents to reveal classes of contained
bioactive molecules; (5) utilizing advanced instrumentation and analysis techniques, these classes of molecules can then be further characterized
and quantied to the molecular level; (6) lab-scale quantities of these molecules can be made available for in vitro and in vivo experiments that
validate target and molecule selection choices; (7) quantitation of these molecules within foods and food by products permits the development of
pilot-scale separation techniques; (8) when these techniques are scaled up to industrial levels, they can be leveraged to reduce pollution in food
processing efuents while providing functional ingredients for new food products; and (9) population health improvement.
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
443
444
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Main
product
Side streams
Cheese
Soybean
Wine
Coffee
Olive oil
Whey
Soybean processing waste (ber-rich spent solids)
Wine processing waste (wine-grape residues and pomace)
Residues from coffee processing (spent grounds)
Olive oil wastewaters
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
whey waste negatively alters the physical and chemical structure of soil, and a prolonged exposure can cause a decreased
crop yield, limiting possibilities for irrigation with whey. Untreated whole liquid whey is used as an animal feed, particularly for pigs, although transport of liquid whey over any
distance is both difcult and expensive (Schingoethe, 1976).
The amount of whey that can be incorporated into animal
diets is trivial compared to the volumes that need to be absorbed (Schingoethe, 1976). Therefore, greater utilization of
whey components is desirable to avoid these economic and
environmental costs. Recent advances in technology now
allow the separation of protein and lactose (Scott and
Krishnapillai, 2012).
Ultraltration is a type of ltration that uses hydrostatic
pressure to force liquid through a lter ne enough to retain
colloidal particles and high molecular weight molecules.
Though ultraltration systems have been in commercial use
for approximately 30 years, dairy processors have been slow to
adopt these systems for whey processing because of a high
price of implementation and difculties with large-scale
membrane processing, including membrane fouling (CuartasUribe et al., 2009). The major technological breakthrough in
the commercial production of whey proteins was the development of scalable ultraltration systems that yielded nondenatured whey protein concentrates (WPC). WPC and whey
protein isolates (WPI)were developed in the late 1990s and
produced mostly by membrane ltration (Morr and Ha,
1993). To obtain WPI, whey is passed through a membrane
lter (ultraltration) which, because of the structure of its
pores, retains the macromolecules while letting the water
containing the dissolved smaller molecules pass through. This
process allows whey proteins to be separated from lactose,
minerals, and other components. Ultraltration produces two
fractions: retentate (containing all retained molecules) and
permeate (containing molecules that permeate through the
membrane). The nal protein-enriched retentate can be dried
to a powder in a spray drying tower. The permeate fraction can
likewise be dried to make permeate powder. A protable
process for utilization of whey permeate compounds is still
lacking. More research and development is required to maximize whey utilization. Discovery of functional proteins such as
lactoferrin in WPC sparked growth in the whey protein market
(Smithers, 2008). Although manufacturers are increasingly
taking advantage of the bioactive benets of whey when designing new products, the full health-enhancing potential of
whey and whey components is still underdeveloped. Concentration of whey proteins in the retentate leaves behind
waste streams in the permeate that often contain functional
components like BMO and bioactive peptides.
445
and quantitation of all bioactive components in processing byproducts and side streams. Recently, detailed knowledge of
waste composition has grown steadily and is essential to the
assessment of all basic applications. Measurement of the
overall composition of products, including water content,
carbohydrates, proteins, and fats is simple and can be performed by all food industries as part of their routine analysis.
Greater analytical expertise and advanced instrumentation and
data analysis software are required for the unambiguous
characterization of complex chemicals in waste sources.
Functional compounds such oligosaccharides, glycolipids,
glycoproteins, and peptides, are found in relatively low concentrations, and are extremely heterogeneous and complex in
nature. Identication and detailed characterization of these
compounds, therefore, demand specic analytical expertise.
Even small differences in structure can cause signicant differences in function, so structural characterization is essential
to accurately distinguish molecular function. To identify their
biological functions through in vitro and in vivo studies, it is
necessary to measure those molecules with accurate and sensitive methods.
Many of milk's functional molecules could not be discovered until the right concordance of novel separation and
analytical technologies were developed and applied. Many
health-promoting components still await discovery due to
technical challenges in their identication, isolation, and testing. As analytical technologies advance in sophistication and
accuracy, new functional milk molecules are being discovered.
In whole milk, many components mask the analytical
signal of others, so some components cannot be detected.
Because milk is such a complex mixture, its compartments
need to be separated, and then fractioned into molecular
classes. Modern analytics allow for the discovery and characterization of hundreds of novel milk compounds with high
resolution and high accuracy. Liquid chromatography (LC)
paired with electrospray ionization allows the separation of
peptides, glycans, and glycolipids for improved mass spectrometric detection. Target proteins and glycoproteins can now be
puried from intact milk or other dairy streams by chromatography in order to better characterize these proteins for new
bioactivities. The combination of advanced analytics with the
new engineering capabilities will allow for high molecular
resolution and separation techniques that can be scaled up to
semiindustrial and industrial scale for translation of lab-based
discoveries.
Many technological breakthroughs have made discovery of
new milk molecules possible. These advances include improved separation science, high-resolution detection instrumentation, bioinformatic toolsets (like proteomic software),
and genomics (as a tool to guide proteomics). Currently,
toolsets exist for the detection of a wide array of free milk
oligosaccharides (glycomics), milk lipids (lipidomics), proteins (proteomics), and naturally occurring peptides in milk
(peptidomics).
Chemical characteristics: oligosaccharides, glycolipids,
glycoproteins, and peptides
Chemical characteristics of oligosaccharides
Milk oligosaccharides can have diverse and complicated
structures even though they commonly share a lactose core
446
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
consisting of a glucose and a galactose linked via a 1,4linkage (Kunz et al., 2000). These oligosaccharides are produced in the mammary gland where several monosaccharides
are added to a lactose core by action of specic enzymes called
glycosyltransferases (Urashima and Tauk, 2010). These glycosyltransferases elongate the core by repetitive attachment
of galactose (Gal) and N-acetylglucosamine (GlcNAc) in
-glycosidic linkage, which are further decorated by multiple
resides of sialic acid and fucose (Kunz et al., 2000). Neutral
oligosaccharides are composed of glucose and galactose (lactose core) extensively elongated by 1-3 or 1-6 linkages to
lactosamine units, and further decorated with fucose residues
in terminal positions connected with 1-2,3,4 possible
linkages. Acidic oligosaccharides can contain all these monosaccharides in addition to one or more molecules of Nacetyl-neuraminic acid (also known as sialic acid) connected
with 2-3,6 linkages. The possible arrangement of monosaccharide combinations and linkages results in a structurally
complex array of linear and branched oligosaccharide structures. In particular, the structural elements fucose and sialic
acid appear to be crucial to the ability of oligosaccharides to
act as bioactive components. These ve monosaccharides
(glucose, galactose, N-acetyl-glucosamine, fucose, and sialic
acid) are linked in various ways through at least 12 - and glycosidic linkages. The most abundant oligosaccharides in
human milk are fucosylated, whereas sialylation is more
abundant than fucosylation in bovine milk and cheese whey
(Morrow et al., 2005).
Chemical characteristics of glycolipids
Nearly all glycolipids in vertebrates are glycosphingolipids.
The glycolipids are composed of two parts: ceramide lipid
portion and carbohydrate moiety. The ceramide is formed by
attachment of a fatty acid in amide linkage to the long-chain
amino alcohol sphingoid base. Ceramide structures vary in
length, hydroxylation, and saturation of both the sphingoid
base and fatty acid moieties, resulting in lipid structural diversity that imparts the presentation of the attached glycan at
membrane surfaces.
In the complex glycolipids, the glucose moiety in head
group is typically substituted with -linked galactose on the
C-4 hydroxyl of glucose, to give lactosylceramide. Further the
glycans are extended by the addition of different monosaccharides.
Glycolipids are subclassied as neutral (no charged sugars or
ionic groups), sialylated (having one or more sialic acid residues), or sulfated according to the carbohydrate moieties. Traditionally, all sialylated glycolipids are known as gangliosides.
The most abundant human and bovine neutral glycolipids are
lactosylceramide, glucosylceramide, and galactosylceramide
(Newburg and Chaturvedi, 1992). GM3(NeuAc2-3 Gal14Glc-Cer) and GD3 (NeuAc2-8NeuAc2-3 Gal1-4Glc-Cer)
are the major gangliosdes in bovine milk and whey buttermilk
(Lee et al., 2011; Rueda, 2007).
Chemical characteristics of glycoproteins
Protein glycosylation, a common posttranslational modication, plays a key role in structural conformation and resultant bioactivity of proteins (Marth and Grewal, 2008;
Shental-Bechor and Levy, 2009). This posttranslational
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
447
However, for single protein isolation, each step of the chromatographic needs to be optimized for each glycoprotein. The
quality of the puried fraction can be monitored by gel electrophoresis and mass spectrometry. The identication of the
protein can be validated by Western blot and peptide mass
ngerprinting. Novel protocols are being developed to achieve
site-specic analysis of milk glycoproteins (Nwosu et al., 2012,
2011). These methods involve using aspecic proteases to
digest the proteins into short glycopeptide chains whose
structural elucidation is accomplished by using accurate mass
and tandem mass spectrometry.
Basic lab-scale separation methods of glycoproteins, N-glycan
purication
To identify the glycans, they can be released by a chemical
method or the use of a commercial enzyme, peptide-N-glycosidase F (PNGase F), which cleaves between the Asparagine
residue and the rst N-acetylglucosamine of the N-glycan core.
One of the advantages of the enzymatic method is the release
of a large variety of glycans, except those containing a fucose
(13) linked to the terminal N-acetylglucosamine residue of
the N-glycan core. PNGase F is not able to cleave the linkage
between the rst N-acetylglucosamine and the asparagine
residue due to steric hindrance. Glycans can be released from
the protein in solution or from the Coomassie-stained gel band
that contained the glycoprotein (Rendi et al., 2007). Specic
exoglycosidases can also be used to get more information
about the N-glycan structure. The deglycosylated protein can be
eliminated by ethanol purication and the released carbohydrates can be puried by graphitized carbon chromatography
and analyzed by sensitive methods like mass spectrometry.
Basic lab-scale separation methods of peptides
Peptidomic analysis of milk's naturally occurring peptides is
now possible only through a conuence of novel preparative
isolation, analytical separation, analytical detection, and
computational techniques. Milk peptides can be isolated by
rst removing cream by centrifugation, then removing the
large proteins via acid precipitation, and nally by removing
the salts, lactose, and oligosaccharides by preparative nonpolar
(C18) solid-phase extraction (SPE).
448
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
449
450
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Challenges for Stream Fractionation and Enrichment of
Functional Molecules
The quest for alternative sources The human milk
oligosaccharides example
The limited supply of HMOs precludes their use as an
industrial source for large-scale production of prebiotics.
Researchers are currently investigating alternative sources of
complex oligosaccharides in sufcient quantity for in vitro and
clinical studies. Various chemical and biological synthesis
strategies have attempted to produce glycans with bioactivities
mimicking those of HMOs. Currently, much simpler structures, including inulin, fructo-oligosaccharides, and galactooligosaccharides are commercially available and have been
tested in clinical trials. These simple structures are either extracted from plants or obtained by -galactosidase-catalysed
conversion of lactose. These glycans stimulate the growth of
intestinal bacteria, but they do not selectively stimulate the
growth of commensal bacteria to the exclusion of undesired
bacteria (Ninonuevo and Bode, 2008). These oligosaccharides
are nonselective because their simple structures mean that only
a limited number of bacterial glycosidases are required for
their degradation. Solid-phase oligosaccharide synthesis is
useful to synthesize small amounts of simple oligosaccharides
for use as standards in analyses (Tolborg et al., 2002), but
production of large quantities needed for human trials is
currently economically prohibitive.
Commercial-scale sources of complex oligosaccharides that
more closely mimic the structures and functions of HMOs are
needed for clinical trials to determine their bioactivities, efcacy, and tolerability in humans. As structures of oligosaccharides from a variety of potential sources are identied
and quantitated, new sources and methods for their recovery
will emerge.
451
452
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Whey
Pasteurization
5
1
Centrifugation
Lipids
Skim whey
Ultrafiltration
(10 KDa)
Fractionation
Glycolipids
6
Whey
proteins
Fractionation
Glycoproteins
Whey premeate
Lactose hydrolysis
3
7
4
Nanofiltration
(5001000 Da)
Retentate
Purification
Oligosaccharides
Peptides
Figure 2 Processing the workow for whey bioactive component extraction. (1) After pasteurization, residual lipids are separated from whey by
centrifugation in a cream separator. (2) Once the lipids are removed, skim whey is further subdivided by a 10 kDa membrane to capture whey
proteins. (3) After the proteins are removed, lactose is hydrolyzed into glucose and galactose to prevent capture of lactose in the nanoltration
membrane. (4) Nanoltration of the lactose-hydrolyzed whey permeate yields a solution with oligosaccharides, peptides, and some mineral salts in
the retentate while glucose, galactose, and most mineral salts pass through the membrane into the permeate. This clean permeate solution can be
used as fermentation and growth media. Lipids can potentially be further fractionated from cream to obtain a selective enrichment in glycolipids.
(5) Solvent extraction can be used to fractionate acidic glycolipids from neutral lipids. Further purication of glycolipids can be achieved with
reverse-phase chromatography. Reverse-phase chromatography can also be employed at large-scale to remove other components from the
glycolipids and generate enough puried glycolipids for in vitro studies. Whey proteins are not all glycosylated so additional steps of fractionation
are necessary if increased purity is desired. (6) Proteins can be precipitated by adding ethanol; ion exchange chromatography, and lectin-afnity
chromatography can be used to recover glycosylated proteins. (7) Oligosaccharides in the nanoltration retentate are further puried from
monovalent salts and monosaccharides resulting from lactose hydrolysis by applying continuous or batch dialtration.
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
453
454
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
455
456
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
these peptides are glycosylated. Bovine lactoferrin hydrolysates produced by pepsin digestion were shown to protect
against foodborne pathogens, such as Salmonella, E. coli, L.
monocytogenes, and St. aureus, in an in vitro assay (Murdock
and Matthews, 2002). Both human and bovine lactoferricin
have been shown to have activity against the human papillomavirus, a known risk factor for cervical cancer (Mistry
et al., 2007). These peptides may affect the gut, intestinal
epithelium, and the immune system, but the required in vivo
studies have not yet been carried out.
Effective separation from bovine milk processing streams of
the aforementioned biomolecules, combined with evidence
of their health benets, is leading to new classes of bioactive
food ingredients. Current research suggests that concentrating
certain bioactives from whey permeate can be a cost-effective
process for the valorization of whey permeate into high
quality, protable novel dairy ingredients. Given the massive
quantities of bovine dairy streams available for capture
worldwide, large-scale production is possible with current
technologies. Although bioactives in whey are less abundant
than in breast milk, existing manufacturing capabilities based
on membrane ltration and chromatography will make it
possible to isolate these components in enough quantities to
carry on the needed studies for clinical validation. These lines
of research set the stage to enhance and improve existing
prebiotics by translating the evolutionarily linked benecial
association between human milk and their associated benecial bidobacteria.
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Acknowledgments
The authors would like to acknowledge Letcia Aquino and
Vitor DeMelo Silva for editorial assistance. The authors gratefully acknowledge support from the Bill and Melinda Gates
Foundation, the National Institutes of Health (awards
R01HD061923 & R01AT007079), and the UC Davis Peter J.
Shields Endowed Chair in Dairy Food Science.
References
Abdallah Ismail, N., Ragab, S.H., Abd ElBaky, A., et al., 2011. Frequency of
Firmicutes and Bacteroidetes in gut microbiota in obese and normal
weight Egyptian children and adults. Archives of Medical Science 7,
501507.
Abt, M., Artis, D., 2009. The intestinal microbiota in health and disease: The
inuence of microbial products on immune cell homeostasis. Current Opinion in
Gastroenterology 25, 496502.
Aebi, M., Bernasconi, R., Clerc, S., Molinari, M., 2010. N-glycan structures:
Recognition and processing in the ER. Trends in Biochemical Sciences 35,
7482.
Agyei, D., Danquah, M.K., 2011. Industrial-scale manufacturing of pharmaceuticalgrade bioactive peptides. Biotechnology Advances 29, 272277.
Albenberg, L.G., Lewis, J.D., Wu, G.D., 2012. Food and the gut microbiota in
inammatory bowel diseases: A critical connection. Current Opinion in
Gastroenterology 28, 314320.
Aldredge, D.L., Geronimo, M.R., Hua, S., et al., 2013. Annotation and structural
elucidation of bovine milk oligosaccharides and determination of novel
fucosylated structures. Glycobiology 23, 664676.
Andersson, B., Porras, O., Hanson, L.., Lagergrd, T., Svanborg-Edn, C., 1986.
Inhibition of attachment of Streptococcus pneumoniae and Haemophilus
inuenzae by human milk and receptor oligosaccharides. Journal of Infectious
Diseases 153, 232237.
Aniansson, G., Andersson, B., Lindstedt, R., Svanborg, C., 1990. Anti-adhesive
activity of human casein against Streptococcus pneumoniae and Haemophilus
inuenzae. Microbial Pathogenesis 8, 315323.
Armougom, F., Henry, M., Vialettes, B., Raccah, D., Raoult, D., 2009. Monitoring
bacterial community of human gut microbiota reveals an increase in
Lactobacillus in obese patients and methanogens in anorexic patients. PLoS One
4, e7125.
457
458
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Culligan, E.P., Hill, C., Sleator, R.D., 2009. Probiotics and gastrointestinal disease:
Successes, problems and future prospects. Gut Pathogens 1, 19.
Dallas, D.C., Guerrero, A., Khaldi, N., et al., 2013a. Extensive in vivo human milk
peptidomics reveals specic proteolysis yielding protective antimicrobial peptides.
Journal of Proteome Research 12, 22952304.
Dallas, D.C., Underwood, M.A., Zivkovic, A.M., German, J.B., 2012. Digestion of
protein in premature and terms infant. Journal of Nutritional Disorders & Therapy
2, 112120.
Dallas, D.C., Weinborn, V., de Moura Bell, J.M.L., et al., 2013b. Comprehensive
peptidomic and glycomic evaluation reveals sweet whey permeate from colostrum
is a source of milk protein-derived peptides and oligosaccharides. Food Research
International special issue FoodOmics 2013.
De Moura, J., Campbell, K., Almeida, N.M., de Glatz, C.E., Johnson, L.A., 2011a.
Protein extraction and membrane recovery in enzyme-assisted aqueous extraction
processing of soybeans. Journal of the American Oil Chemists' Society 88,
877889.
De Moura, J., Campbell, K., Almeida, N.M., de Glatz, C.E., Johnson, L.A., 2011b.
Protein recovery in aqueous extraction processing of soybeans using isoelectric
precipitation and nanoltration. Journal of the American Oil Chemists' Society
88, 14471454.
De Moura, J., Maurer, D., Jung, S., Johnson, L.A., 2011c. Pilot-plant proof-ofconcept for integrated, countercurrent, two-stage, enzyme-assisted aqueous
extraction of soybeans. Journal of the American Oil Chemists' Society 88,
16491658.
Dennis, E.A., Brown, H.A., Deems, R.A., et al., 2005. The LIPID MAPS approach to
lipidomics. In: Feng, L., Prestwich, G. (Eds.), Functional Lipidomics. London:
CRC Press/Taylor & Francis Group, pp. 115.
Di Stefano, V., Avellone, G., Bongiorno, D., et al., 2012. Applications of HPLCMS
for food analysis. Journal of Chromatography A 1259, 7485.
Donovan, S.M., Wang, M., Li, M., et al., 2012. Host-microbe interactions in the
neonatal intestine: Role of human milk oligosaccharides. Advance Nutrients 3,
450S455S.
Eiwegger, T., Stahl, B., Schmitt, J., et al., 2004. Human milk-derived
oligosaccharides and plant-derived oligosaccharides stimulate cytokine production
of cord blood T-cells in vitro. Pediatric Research 56, 536540.
Elwell, M.W., Barbano, D.M., 2006. Use of microltration to improve uid milk
quality. Journal of Dairy Science 89 (Suppl.), E20E30.
Fahy, E., Sud, M., Cotter, D., Subramaniam, S., 2007. LIPID MAPS online tools for
lipid research. Nucleic Acids Research 35, W606W612.
Fantini, J., Maresca, M., Hammache, D., Yahi, N., Delzay, O., 2000.
Glycosphingolipid (GSL) microdomains as attachment platforms for host
pathogens and their toxins on intestinal epithelial cells: Activation of signal
transduction pathways and perturbations of intestinal absorption and secretion.
Glycoconjugate Journal 17, 173179.
Farnaud, S., Evans, R.W., 2003. Lactoferrin A multifunctional protein with
antimicrobial properties. Molecular Immunology 40, 395405.
Finke, B., Stahl, B., Pfenninger, A., et al., 1999. Analysis of high-molecular-weight
oligosaccharides from human milk by liquid chromatography and MALDI-MS.
Analytical Chemistry 71, 37553762.
Fukuda, S., Toh, H., Hase, K., et al., 2011. Bidobacteria can protect from
enteropathogenic infection through production of acetate. Nature 469, 543547.
German, J.B., Dillard, C.J., Ward, R.E., 2002. Bioactive components in milk. Current
Opinion in Clinical Nutrition & Metabolic Care 5, 653658.
Gopal, P.K., Gill, H.S., 2000. Oligosaccharides and glycoconjugates in bovine milk
and colostrum. British Journal of Nutrition 84 (Suppl. 1), S69S74.
Goulas, A.K., Grandison, A.S., Rastall, R.A., 2003. Fractionation of oligosaccharides
by nanoltration. Journal of the Science of Food and Agriculture 83, 675680.
Goulas, A.K., Kapasakalidis, P.G., Sinclair, H.R., Rastall, R.A., Grandison, A.S.,
2002. Purication of oligosaccharides by nanoltration. Journal of Membrane
Science 209, 321335.
Gry, J., Black, L., Eriksen, F.D., et al., 2007. EuroFIR-BASIS A combined
composition and biological activity database for bioactive compounds in plantbased foods. Trends in Food Science & Technology 18, 434444.
Hakkarainen, J., Toivanen, M., Leinonen, A., et al., 2005. Human and bovine milk
oligosaccharides inhibit Neisseria meningitidis pili attachment in vitro. Journal of
Nutrition 135, 24452448.
Hansen, R., Dickson, A.J., Goodacre, R., Stephens, G.M., Sellick, C.A., 2010. Rapid
characterization of N-linked glycans from secreted and gel-puried monoclonal
antibodies using MALDI-ToF mass spectrometry. Biotechnology and
Bioengineering 107, 902908.
Harvey, D.J., 2006. Analysis of carbohydrates and glycoconjugates by matrixassisted laser desorption/ionization mass spectrometry: An update covering the
period 19992000. Mass Spectrometry Reviews 25, 595662.
He, H., Conrad, C.A., Nilsson, C.L., et al., 2007. Method for lipidomic analysis: p53
Expression modulation of sulfatide, ganglioside, and phospholipid composition of
U87 MG glioblastoma cells. Analytical Chemistry 79, 84238430.
Hernndez-Ledesma, B., del Mar Contreras, M., Recio, I., 2011. Antihypertensive
peptides: Production, bioavailability and incorporation into foods. Advances in
Colloid and Interface Science 165, 2335.
Holden, J.M., Bhagwat, S.A., Haytowitz, D.B., et al., 2005. Development of a database
of critically evaluated avonoids data: Application of USDA's data quality
evaluation system. Journal of Food Composition and Analysis 18, 829844.
Hong, P., Ninonuevo, M.R., Lee, B., Lebrilla, C., Bode, L., 2009. Human milk
oligosaccharides reduce HIV-1-gp120 binding to dendritic cell-specic ICAM3grabbing non-integrin (DC-SIGN). British Journal of Nutrition 101, 482486.
Hornef, M.W., Wick, M.J., Rhen, M., Normark, S., 2002. Bacterial strategies for
overcoming host innate and adaptive immune responses. Nature Immunology 3,
10331040.
Hua, S., Jeong, H.N., Dimapasoc, L.M., et al., 2013. Isomer-specic LC/MS and
LC/MS/MS proling of the mouse serum N-glycome revealing a number of
novel sialylated N-glycans. Analytical Chemistry 85, 46364643.
Hua, S., Nwosu, C.C., Strum, J.S., et al., 2012. Site-specic protein glycosylation
analysis with glycan isomer differentiation. Analytical and Bioanalytical Chemistry
403, 12911302.
Idota, T., Kawakami, H., 1995. Inhibitory effects of milk gangliosides on the
adhesion of Escherichia coli to human intestinal carcinoma cells. Bioscience,
Biotechnology, and Biochemistry 59, 6972.
Jenkins, D.J.A., Kendall, C.W.C., Vuksan, V., 1999. Inulin, oligofructose and
intestinal function. Journal of Nutrition 129, 1431.
John, R.P., 2009. Biotechnological potentials of cassava bagasse. In: nee Nigam, P.
S., Pandey, A. (Eds.), Biotechnology for Agro-Industrial Residues Utilisation. The
Netherlands: Springer, pp. 225237.
Jrgensen, A.L.W., Juul-Madsen, H.R., Stagsted, J., 2010. Colostrum and bioactive,
colostral peptides differentially modulate the innate immune response of intestinal
epithelial cells. Journal of Peptide Science 16, 2130.
Jumpertz, R., Le, D.S., Turnbaugh, P.J., et al., 2011. Energy-balance studies reveal
associations between gut microbes, caloric load, and nutrient absorption in
humans. American Journal of Clinical Nutrition 94, 5865.
Jung, S., de Moura, J., Campbell, K., Johnson, L., 2012. Enzyme-assisted aqueous
extraction of oilseeds. In: Lebovka, N. (Ed.), Enhancing Extraction Processes in
the Food Industry. Boca Raton, FL: CRC Press, pp. 457518.
Kalliomki, M., Collado, M.C., Salminen, S., Isolauri, E., 2008. Early differences in
fecal microbiota composition in children may predict overweight. American
Journal of Clinical Nutrition 87, 534538.
Kalliomaki, M., Isolauri, E., 2003. Role of intestinal ora in the development of
allergy. Current Opinion in Allergy & Clinical Immunology 3, 1520.
Kalliomki, M., Kirjavainen, P., Eerola, E., et al., 2001. Distinct patterns of neonatal
gut microora in infants in whom atopy was and was not developing. Journal of
Allergy and Clinical Immunology 107, 129134.
Kampa, M., Loukas, S., Hatzoglou, A., et al., 1996. Identication of a novel opioid
peptide (Tyr-Val-Pro-Phe-Pro) derived from human alpha S1 casein (alpha S1casomorphin, and alpha S1-casomorphin amide). Biochemical Journal 319,
903908.
King, Jr, J.C., Cummings, G.E., Guo, N., et al., 2007. A double-blind, placebocontrolled, pilot study of bovine lactoferrin supplementation in bottle-fed infants.
Journal of Pediatric Gastroenterology and Nutrition 44, 245251.
Kinsella, J.E., 1979. Functional properties of soy proteins. Journal of the American
Oil Chemists' Society 56, 242258.
Kletter, D., Singh, S., Bern, M., Haab, B.B., 2013. Global comparisons of lectin
glycan interactions using a database of analyzed glycan array data. Molecular &
Cellular Proteomics 12, 10261035.
Korhonen, H., Pihlanto, A., 2003. Food-derived bioactive peptides Opportunities
for designing future foods. Current Pharmaceutical Design 9, 12971308.
Korhonen, H., Pihlanto, A., 2006. Bioactive peptides: Production and functionality.
International Dairy Journal 16, 945960.
Korhonen, H., Pihlanto-Leppla, A., Rantamki, P., Tupasela, T., 1998. Impact of
processing on bioactive proteins and peptides. Trends in Food Science &
Technology 9, 307319.
Kronewitter, S.R., An, H.J., de Leoz, M.L., et al., 2009. The development of
retrosynthetic glycan libraries to prole and classify the human serum N-linked
glycome. Proteomics 9, 29862994.
Kunz, C., Rudloff, S., Baier, W., Klein, N., Strobel, S., 2000. Oligosaccharides in
human milk: Structural, functional, and metabolic aspects. Annual Review of
Nutrition 20, 699722.
Law, B.A., Reiter, B., 1977. The isolation and bacteriostatic properties of lactoferrin
from bovine milk whey. Journal of Dairy Research 44, 595599.
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Lawrence, R.M., Pane, C.A., 2007. Human breast milk: Current concepts of
immunology and infectious diseases. Current Problems in Pediatric and
Adolescent Health Care 37, 736.
Ledeen, R.W., Yu, R.K., 1982. Gangliosides: Structure, isolation, and analysis.
Methods in Enzymology 83, 139191.
Lee, H., An, H.J., Lerno, L.A., German, J.B., Lebrilla, C.B., 2011. Rapid proling of
bovine and human milk gangliosides by matrix-assisted laser desorption/
ionization fourier transform ion cyclotron resonance mass spectrometry.
International Journal of Mass Spectrometry 305, 138150.
Lee, H., German, J.B., Kjelden, R., Lebrilla, C.B., Barile, D., 2013. Quantitative
analysis of gangliosides in bovine milk and colostrum-based dairy products by
ultra-high performance liquid chromatography-tandem mass spectrometry.
Journal of Agricultural and Food Chemistry 61, 96899696.
Lee, H., Lerno, L.A., Choe, Y., et al., 2012. Multiple precursor ion scanning of
gangliosides and sulfatides with a reversed-phase microuidic chip and quadrupole
time-of-ight mass spectrometry. Analytical Chemistry 84, 59055912.
Legrand, D., Elass, E., Carpentier, M., Mazurier, J., 2005. Lactoferrin: A modulator
of immune and inammatory responses. Cellular and Molecular Life Sciences
62, 25492559.
Leoz, M.L.A.D., Wu, S., Strum, J.S., et al., 2013. A quantitative and comprehensive
method to analyze human milk oligosaccharide structures in the urine and feces
of infants. Analytical and Bioanalytical Chemistry 405, 40894105.
Liepke, C., Adermann, K., Raida, M., et al., 2002. Human milk provides peptides
highly stimulating the growth of bidobacteria. European Journal of Biochemistry
269, 712718.
Liepke, C., Zucht, H.-D., Forssmann, W.-G., Stndker, L., 2001. Purication of novel
peptide antibiotics from human milk. Journal of Chromatography B: Biomedical
Sciences and Applications 752, 369377.
Liu, B., Yu, Z., Chen, C., Kling, D.E., Newburg, D.S., 2012. Human milk mucin 1
and mucin 4 inhibit Salmonella enterica serovar typhimurium invasion of human
intestinal epithelial cells in vitro. Journal of Nutrition 142, 15041509.
LoCascio, R.G., Desai, P., Sela, D.A., Weimer, B., Mills, D.A., 2010. Broad
conservation of milk utilization genes in Bidobacterium longum subsp. infantis
as revealed by comparative genomic hybridization. Applied and Environmental
Microbiology 76, 73737381.
Lonnerdal, B., Iyer, S., 1995. Lactoferrin: Molecular structure and biological function.
Annual Review of Nutrition 15, 93110.
Manning, T.S., Gibson, G.R., 2004. Prebiotics. Best Practice & Research Clinical
Gastroenterology 18, 287298.
Marcelo, P.A., Rizvi, S.S.H., 2008. Physicochemical properties of liquid virgin whey
protein isolate. International Dairy Journal 18, 236246.
Marcobal, A., Barboza, M., Froehlich, J.W., et al., 2010. Consumption of human
milk oligosaccharides by gut-related microbes. Journal of Agricultural and Food
Chemistry 58, 53345340.
Marcobal, A., Barboza, M., Sonnenburg, E.D., et al., 2011. Bacteroides in the infant
gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host &
Microbe 10, 507514.
Marth, J.D., Grewal, P.K., 2008. Mammalian glycosylation in immunity. Nature
Reviews Immunology 8, 874887.
Martinez-Ferez, A., Rudloff, S., Guadix, A., et al., 2006. Goats milk as a natural
source of lactose-derived oligosaccharides: Isolation by membrane technology.
International Dairy Journal 16, 173181.
Martino, D.J., Currie, H., Taylor, A., Conway, P., Prescott, S.L., 2008. Relationship
between early intestinal colonization, mucosal immunoglobulin A production and
systemic immune development. Clinical & Experimental Allergy 38, 6978.
Marwaha, S.S., Kennedy, J.F., 1988. Whey Pollution problem and potential
utilization. International Journal of Food Science & Technology 23, 323336.
Maubois, J.-L., 2011. Liquid milk products: Membrane-processed liquid milk. In:
John, W.F. (Ed.), Encyclopedia of Dairy Sciences, second ed. San Diego:
Academic Press, pp. 307309.
Merrill, A.H., Sullards, M.C., Allegood, J.C., Kelly, S., Wang, E., 2005.
Sphingolipidomics: High-throughput, structure-specic, and quantitative analysis
of sphingolipids by liquid chromatography tandem mass spectrometry. Methods
36, 207224.
Migliore-Samour, D., Floc'h, F., Jolls, P., 1989. Biologically active casein peptides
implicated in immunomodulation. Journal of Dairy Research 56, 357362.
Miklavcic, J.J., Schnabl, K.L., Mazurak, V.C., Thomson, A.B., Clandinin, M.T., 2012.
Dietary ganglioside reduces proinammatory signaling in the intestine. Journal of
Nutrition and Metabolism 2012, 18.
Minkiewicz, P., Slangen, C.J., Lagerwerf, F.M., et al., 1996. Reversed-phase highperformance liquid chromatographic separation of bovine -casein macropeptide
and characterization of isolated fractions. Journal of Chromatography A 743,
123135.
459
Mistry, N., Drobni, P., Naslund, J., et al., 2007. The anti-papillomavirus activity of
human and bovine lactoferricin. Antiviral Research 75, 258265.
Mller, A., Unwin, I.D., Becker, W., Ireland, J., 2007. EuroFIR's food databank
systems for nutrients and bioactives. Trends in Food Science & Technology 18,
428433.
Morr, C.V., Ha, E.Y.W., 1993. Whey protein concentrates and isolates: Processing
and functional properties. Critical Reviews in Food Science and Nutrition 33,
431476.
Morrow, A.L., Ruiz-Palacios, G.M., Altaye, M., et al., 2004. Human milk
oligosaccharides are associated with protection against diarrhea in breast-fed
infants. Journal of Pediatrics 145, 297303.
Morrow, A.L., Ruiz-Palacios, G.M., Jiang, X., Newburg, D.S., 2005. Human-milk
glycans that inhibit pathogen binding protect breast-feeding infants against
infectious diarrhea. Journal of Nutrition 135, 13041307.
Murdock, C.a., Matthews, K.r., 2002. Antibacterial activity of pepsin-digested
lactoferrin on foodborne pathogens in buffered broth systems and ultra-high
temperature milk with EDTA. Journal of Applied Microbiology 93, 850856.
Newburg, D.S., 2001. Bioactive components of human milk: Evolution, protection
and efciency. In: Newburg, D.S. (Ed.), Bioactive Components of Human Milk.
New York, NJ: Springer, pp. 310.
Newburg, D.S., 2005. Innate immunity and human milk. Journal of Nutrition 135,
13081312.
Newburg, D.S., 2009. Neonatal protection by an innate immune system of human
milk consisting of oligosaccharides and glycans. Journal of Animal Science 87,
2634.
Newburg, D.S., Chaturvedi, P., 1992. Neutral glycolipids of human and bovine milk.
Lipids 27, 923927.
Newburg, D.S., Ruiz-Palacios, G.M., Altaye, M., et al., 2004. Human milk alphal,2linked fucosylated oligosaccharides decrease risk of diarrhea due to stable toxin
of E. coli in breastfed infants. Advances in Experimental Medicine and Biology
554, 457461.
Newburg, D.S., Ruiz-Palacios, G.M., Morrow, A.L., 2005. Human milk glycans
protect infants against enteric pathogens. Annual Review of Nutrition 25, 3758.
Nionuevo, M., An, H., Yin, H., et al., 2005. Nanoliquid chromatography-mass
spectrometry of oligosaccharides employing graphitized carbon chromatography
on microchip with a high-accuracy mass analyzer. Electrophoresis 26,
36413649.
Ninonuevo, M.R., Bode, L., 2008. Infant formula oligosaccharides opening the gates
(for speculation): Commentary on the article by Barrat et al. on page 34.
Pediatric Research 64, 810.
Nionuevo, M.R., Lebrilla, C.B., 2009. Mass spectrometric methods for analysis of
oligosaccharides in human milk. Nutrition Reviews 67, S216S226.
Ninonuevo, M.R., Park, Y., Yin, H., et al., 2006. A strategy for annotating the human
milk glycome. Journal of Agricultural and Food Chemistry 54, 74717480.
Nionuevo, M.R., Perkins, P.D., Francis, J., et al., 2007. Daily variations in
oligosaccharides of human milk determined by microuidic chips and mass
spectrometry. Journal of Agricultural and Food Chemistry 56, 618626.
Nwosu, C.C., Aldredge, D.L., Lee, H., et al., 2012. Comparison of the human and
bovine milk N-glycome via high-performance microuidic chip liquid
chromatography and tandem mass spectrometry. Journal of Proteome Research
11, 29122924.
Nwosu, C.C., Seipert, R.R., Strum, J.S., et al., 2011. Simultaneous and extensive
site-specic N- and O-glycosylation analysis in protein mixtures. Journal of
Proteome Research 10, 26122624.
Obermeier, S., Rudloff, S., Pohlentz, G., Lentze, M.J., Kunz, C., 1999. Secretion of
13C-labelled oligosaccharides into human milk and infant's urine after an oral
13C-galactose load. Isotopes in Environmental and Health Studies 35, 119125.
Ochoa, T.J., Chea-Woo, E., Campos, M., et al., 2008. Impact of lactoferrin
supplementation on growth and prevalence of Giardia colonization in children.
Clinical Infectious Disease 46, 18811883.
Ohtsubo, K., Marth, J.D., 2006. Glycosylation in cellular mechanisms of health and
disease. Cell 126, 855867.
Orsi, N., 2004. The antimicrobial activity of lactoferrin: Current status and
perspectives. Biometals 17, 189196.
Otnaess, A.B., Laegreid, A., Ertresvag, K., 1983. Inhibition of enterotoxin from
Escherichia coli and Vibrio cholerae by gangliosides from human milk. Infection
and Immunity 40, 563569.
Pabst, H.F., Spady, D.W., Pilarski, L.M., et al., 1997. Differential modulation of the
immune response by breast- or formula-feeding of infants. Acta Paediatrica 86,
12911297.
Packer, N.H., Lawson, M.A., Jardine, D.R., Redmond, J.W., 1998. A general
approach to desalting oligosaccharides released from glycoproteins.
Glycoconjugate Journal 15, 737747.
460
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Park, E.J., Suh, M., Thomson, B., et al., 2007. Dietary ganglioside inhibits acute
inammatory signals in intestinal mucosa and blood induced by systemic
inammation of Escherichia coli lipopolysaccharide. Shock 28, 112117.
Pfenninger, A., Karas, M., Finke, B., Stahl, B., 2002. Structural analysis of
underivatized neutral human milk oligosaccharides in the negative ion mode by
nano-electrospray MS(n) (part 1: methodology). Journal of the American Society
for Mass Spectrometry 13, 13311340.
Picariello, G., Ferranti, P., Mamone, G., Roepstorff, P., Addeo, F., 2008.
Identication of N-linked glycoproteins in human milk by hydrophilic interaction
liquid chromatography and mass spectrometry. Proteomics 8, 38333847.
Pouliot, Y., 2008. Membrane processes in dairy technology From a simple idea
to worldwide panacea. International Dairy Journal 18, 735740.
Proctor, L.M., 2011. The human microbiome project in 2011 and beyond. Cell Host
& Microbe 10, 287291.
Qin, J., Li, R., Raes, J., et al., 2010. A human gut microbial gene catalogue
established by metagenomic sequencing. Nature 464, 5965.
Ramchandran, L., Vasiljevic, T., 2013. Whey processing. In: Tamime, A.Y. (Ed.),
Membrane Processing. Oxford, UK: Blackwell Publishing Ltd., pp. 193207.
Rastall, R.A., Maitin, V., 2002. Prebiotics and synbiotics: Towards the next
generation. Current Opinion in Biotechnology 13, 490496.
Reddy, B.S., Rivenson, A., 1993. Inhibitory effect of Bidobacterium longum on
colon, mammary, and liver carcinogenesis induced by 2-amino-3-methylimidazo
[4, 5-f] quinoline, a food mutagen. Cancer Research 53, 39143918.
Reinhardt, C., Reigstad, C., Backhed, F., 2009. Intestinal microbiota during infancy
and its implications for obesity. Journal of Pediatric Gastroenterology 48,
249256.
Rendi, D., Wilson, I.B.H., Lubec, G., et al., 2007. Adaptation of the in-gel release
method to N-glycome analysis of low-milligram amounts of material.
Electrophoresis 28, 44844492.
Rosenberg, M., 1995. Current and future applications for membrane processes in the
dairy industry. Trends in Food Science & Technology 6, 1219.
Rothwell, J.A., Urpi-Sarda, M., Boto-Ordonez, M., et al., 2012. Phenol-Explorer 2.0:
A major update of the Phenol-Explorer database integrating data on polyphenol
metabolism and pharmacokinetics in humans and experimental animals. Database
(Oxford). doi: 10.1093/database/bas031.
Rowland, I.R., Rumney, C.J., Coutts, J.T., Lievense, L.C., 1998. Effect of
Bidobacterium longum and inulin on gut bacterial metabolism and carcinogeninduced aberrant crypt foci in rats. Carcinogenesis 19, 281285.
Rudloff, S., Pohlentz, G., Diekmann, L., Egge, H., Kunz, C., 1996. Urinary excretion
of lactose and oligosaccharides in preterm infants fed human milk or infant
formula. Acta Paediatrica 85, 598603.
Rueda, R., 2007. The role of dietary gangliosides on immunity and the prevention of
infection. British Journal of Nutrition 98 (Suppl. 1), S68S73.
Rueda, R., Sabatel, J.L., Maldonado, J., Molina-Font, J.A., Gil, A., 1998. Addition of
gangliosides to an adapted milk formula modies levels of fecal Escherichia coli
in preterm newborn infants. Journal of Pediatrics 133, 9094.
Saito, T., Yamaji, A., Itoh, T., 1991. A new isolation method of caseinoglycopeptide
from sweet cheese whey. Journal of Dairy Science 74, 28312837.
Sakata, S., Tonooka, T., Ishizeki, S., et al., 2005. Culture-independent analysis of
fecal microbiota in infants, with special reference to Bidobacterium species.
FEMS Microbiology Letters 243, 417423.
Sanchez, L., Calvo, M., Brock, J.H., 1992. Biological role of lactoferrin. Archives of
Disease in Childhood 67, 657661.
Sanders, M.E., 2000. Considerations for use of probiotic bacteria to modulate
human health. Journal of Nutrition 130, 384S390S.
Sarney, D.B., Hale, C., Frankel, G., Vulfson, E.N., 2000. A novel approach to the
recovery of biologically active oligosaccharides from milk using a combination of
enzymatic treatment and nanoltration. Biotechnology and Bioengineering 69,
461467.
Schanbacher, F.L., Talhouk, R.S., Murray, F.A., 1997. Biology and origin of bioactive
peptides in milk. Livestock Production Science 50, 105123.
Schingoethe, D.J., 1976. Whey utilization in animal feeding: A summary and
evaluation. Journal of Dairy Science 59, 556570.
Scoma, A., Pintucci, C., Bertin, L., Carlozzi, P., Fava, F., 2012. Increasing the large
scale feasibility of a solid phase extraction procedure for the recovery of natural
antioxidants from olive mill wastewaters. Chemical Engineering Journal
198199, 103109.
Scott, S.N., Krishnapillai, A., 2012. Isolation and Purication of Components of
Whey. US Patent Application Publication, 17 May 2012, US 2012/0121788 A1.
Seganti, L., Biase, A.M.D., Marchetti, M., et al., 2004. Antiviral activity of lactoferrin
towards naked viruses. Biometals 17, 295299.
Seifert, S., Watzl, B., 2007. Inulin and oligofructose: Review of experimental data on
immune modulation. Journal of Nutrition 137, 2563S2567S.
Sela, D.A., Garrido, D., Lerno, L., et al., 2012. Bidobacterium longum subsp.
infantis ATCC 15697 -fucosidases are active on fucosylated human milk
oligosaccharides. Applied and Environmental Microbiology 78, 795803.
Sela, D.A., Li, Y., Lerno, L., et al., 2011. An infant-associated bacterial commensal
utilizes breast milk sialyloligosaccharides. Journal of Biological Chemistry 286,
1190911918.
Sela, D.A., Mills, D.A., 2010. Nursing our microbiota: Molecular linkages
between bidobacteria and milk oligosaccharides. Trends in Microbiology 18,
298307.
Senkovich, O., Cook, W.J., Mirza, S., et al., 2007. Structure of a complex of
human lactoferrin N-lobe with pneumococcal surface protein a provides
insight into microbial defense mechanism. Journal of Molecular Biology 370,
701713.
Sepp, E., Julge, K., Vasar, M., et al., 1997. Intestinal microora of Estonian and
Swedish infants. Acta Paediatrica 86, 956961.
Serban, D.E., 2011. The gut microbiota in the metagenomics era: Sometimes a
friend, sometimes a foe. Roumanian archives of Microbiology and Immunology
70, 134140.
Shabana, I.I., ALgammal, A.M., Suzuki, H., 2013. Molecular typing of the
enteroaggregative E. coli heat-stable enterotoxin 1 gene (EAST1) in E. coli strains
isolated from human and calves with diarrhea. Global Animal Science Journal 1
(1), 11281138.
Shental-Bechor, D., Levy, Y., 2009. Folding of glycoproteins: Toward understanding
the biophysics of the glycosylation code. Current Opinion in Structural Biology
19, 524533.
Simon, P.M., Goode, P.L., Mobasseri, A., Zopf, D., 1997. Inhibition of Helicobacter
pylori binding to gastrointestinal epithelial cells by sialic acid-containing
oligosaccharides. Infection and immunity 65, 750757.
Simons, K., van Meer, G., 1988. Lipid sorting in epithelial cells. Biochemistry 27,
61976202.
Singh, J., Rivenson, A., Tomita, M., et al., 1997. Bidobacterium longum, a lactic
acid-producing intestinal bacterium inhibits colon cancer and modulates the
intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18, 833841.
Smithers, G.W., 2008. Whey and whey proteins From gutter-to-gold.
International Dairy Journal 18, 695704.
Sorensen, L.K., 2006. A liquid chromatography/tandem mass spectrometric approach
for the determination of gangliosides GD3 and GM3 in bovine milk and infant
formulae. Rapid Communications in Mass Spectrometry 20, 36253633.
Stins, M., Prasadarao, N., Ibric, L., Kim, K., 1994. Binding characteristics of S
mbriated Escherichia coli to isolated brain microvascular endothelial cells.
American Journal of Pathology 145, 12281236.
Strmqvist, M., Falk, P., Hansson, S.B.L., et al., 1995. Human milk k-casein and
inhibition of Helicobacter pylori adhesion to human gastric mucosa. Journal of
Pediatric Gastroenterology and Nutrition 21, 288296.
Strum, J.S., Kim, J., Wu, S., et al., 2012. Identication and accurate quantitation of
biological oligosaccharide mixtures. Analytical Chemistry 84, 77937801.
Sudo, N., Sawarnura, S., Tanaka, K., et al., 1997. The requirement of intestinal
bacterial ora for the development of an IgE production system fully susceptible
to oral tolerance induction. Journal of Immunology 159, 17391745.
Sullivan, S., Schanler, R.J., Kim, J.H., et al., 2010. An exclusively human milk-based
diet is associated with a lower rate of necrotizing enterocolitis than a diet of
human milk and bovine milk-based products. Journal of Pediatrics 156, 562567.
Sundekilde, U.K., Barile, D., Meyrand, M., et al., 2012. Natural variability in bovine
milk oligosaccharides from Danish Jersey and Holstein-Friesian breeds. Journal
of Agricultural and Food Chemistry 60, 61886196.
Svennerholm, L., Fredman, P., 1980. A procedure for the quantitative isolation of
brain gangliosides. Biochimica et Biophysica Acta (BBA) Lipids and Lipid
Metabolism 617, 97109.
Tao, N., DePeters, E.J., Freeman, S., et al., 2008. Bovine milk glycome. Journal of
Dairy Science 91, 37683778.
Tao, N., DePeters, E.J., German, J.B., Grimm, R., Lebrilla, C.B., 2009. Variations in
bovine milk oligosaccharides during early and middle lactation stages analyzed
by high-performance liquid chromatography-chip/mass spectrometry. Journal of
Dairy Science 92, 29913001.
Tao, N., Ochonicky, K.L., German, J.B., Donovan, S.M., Lebrilla, C.B., 2010.
Structural determination and daily variations of porcine milk oligosaccharides.
Journal of Agricultural and Food Chemistry 58, 46534659.
Tao, N., Wu, S., Kim, J., et al., 2011. Evolutionary glycomics: Characterization of
milk oligosaccharides in primates. Journal of Proteome Research 10, 15481557.
Thibault, H., Aubert-Jacquin, C., Goulet, O., 2004. Effects of long-term consumption
of a fermented infant formula (with Bidobacterium breve c50 and Streptococcus
thermophilus 065) on acute diarrhea in healthy infants. Journal of Pediatric
Gastroenterology and Nutrition 39, 147152.
Determining Functional Properties and Sources of Recently Identied Bioactive Food Components
Tolborg, J.F., Petersen, L., Jensen, K.J., et al., 2002. Solid-phase oligosaccharide
and glycopeptide synthesis using glycosynthases. Journal of Organic Chemistry
67, 41434149.
Turnbaugh, P.J., Hamady, M., Yatsunenko, T., et al., 2009. A core gut microbiome
in obese and lean twins. Nature 457, 480484.
Urashima, T., Tauk, E., 2010. Oligosaccharides in milk: Their benets and future
utilization. Media Peternakan 33 (3), 189197.
U.S. Export 5 Year Trend, 2013. United States Dairy Export Council Global Dairy
Market Outlook 17 (7), 17.
Valenti, P., Antonini, G., 2005. Lactoferrin: An important host defence against
microbial and viral attack. Cellular and Molecular Life Sciences 62, 25762587.
Vazquez, E., Gil, A., Rueda, R., 2001. Dietary gangliosides positively modulate the
percentages of Th1 and Th2 lymphocyte subsets in small intestine of mice at
weaning. Biofactors 15, 19.
Walzem, R.L., Dillard, C.J., German, J.B., 2002. Whey components: Millennia of
evolution create functionalities for mammalian nutrition: What we know and what
we may be overlooking. Critical Reviews in Food Science and Nutrition 42,
353375.
Ward, P.P., Uribe-Luna, S., Conneely, O.M., 2002. Lactoferrin and host defense.
Biochemistry and Cell Biology 80, 95102.
Ward, R.E., Ninonuevo, M., Mills, D.A., Lebrilla, C.B., German, J.B., 2006. In vitro
fermentation of breast milk oligosaccharides by Bidobacterium infantis and
Lactobacillus gasseri. Applied and Environmental Microbiology 72, 44974499.
Ward, R.E., Watzke, H.J., Jimenez-Flores, R., German, J.B., 2004. Bioguided
processing A paradigm change in food production. Food Technology 58,
4448.
Wickramasinghe, S., Hua, S., Rincon, G., et al., 2011. Transcriptome proling of
bovine milk oligosaccharide metabolism genes using RNA-sequencing. PLoS
One 6, e18895.
Wijngaard, H., Hossain, M.B., Rai, D.K., Brunton, N., 2012. Techniques to extract
bioactive compounds from food by-products of plant origin. Food Research
International 46, 505513.
Wu, S., Grimm, R., German, J.B., Lebrilla, C.B., 2010a. Annotation and structural
analysis of sialylated human milk oligosaccharides. Journal of Proteome
Research 10, 856868.
Wu, S., Salcedo, J., Tang, N., et al., 2012. Employment of tandem mass
spectrometry for the accurate and specic identication of oligosaccharide
structures. Analytical Chemistry 84, 74567462.
461
Wu, S., Tao, N., German, J.B., Grimm, R., Lebrilla, C.B., 2010b. Development of an
annotated library of neutral human milk oligosaccharides. Journal of Proteome
Research 9, 41384151.
Yamakawa, T., Nagai, Y., 1978. Glycolipids at cell-surface and their biological
functions. Trends in Biochemical Science 3, 128131.
Yatsunenko, T., Rey, F.E., Manary, M.J., et al., 2012. Human gut microbiome viewed
across age and geography. Nature 486, 222227.
Yekta, M.A., Verdonck, F., Van Den Broeck, W., et al., 2010. Lactoferrin inhibits E.
coli O157: H7 growth and attachment to intestinal epithelial cells. Veterinarni
Medicina 55, 359368.
Zhang, J., Ren, Y., Huang, B., et al., 2012. Determination of disialoganglioside GD3
and monosialoganglioside GM3 in infant formulas and whey protein concentrates
by ultra-performance liquid chromatography/electrospray ionization tandem mass
spectrometry. Journal of Separation Science 35, 937946.
Zivkovic, A.M., German, J.B., Lebrilla, C.B., Mills, D.A., 2011. Human milk
glycobiome and its impact on the infant gastrointestinal microbiota. Proceedings
of the National Academy of Sciences 108, 46534658.
Zydney, A.L., 1998. Protein separations using membrane ltration: New opportunities
for whey fractionation. International Dairy Journal 8, 243250.
Relevant Websites
http://www.fao.org/
Food and Agriculture Organization of the United Nations.
http://www.glycoforum.gr.jp/
Glycoforum.
http://masspec.scripps.edu/
Scripps Center for Metabolomics and Mass Spectrometry.
http://foodbioactives.ucdavis.edu/
UC Davis, Department of Food Science and Technology.
http://foodscience.ucdavis.edu/processing-facilities/milk-processing-laboratory
UC Davis, Food Science and Technology.
Domestication of Animals
TR Famula, University of California, Davis, CA
r 2014 Elsevier Inc. All rights reserved.
462
doi:10.1016/B978-0-444-52512-3.00230-8
Domestication of Animals
more than 5000 years BP, and rice cultivation in the Far East
some 7000 years BP (Bar-Yosef, 2012; Harris, 2012).
Realizing this represents a considerable swath of time, it is
nevertheless interesting to address the comparative simultaneity of agricultural development across the ancient world.
Why did agriculture begin at this time? Did the idea travel?
Did people in one area suggest this process to their neighbors
and bring domestication with them? Or did indigenous
people arrive at this invention on their own? Anthropologists
now seem to prefer the last alternative (Bellwood and Oxenham, 2008; Cauvin and Watkins, 1994) that as the climate
change of the ending Pleistocene era advanced, the rapidly
changing biology surrounding human communities almost
pointed to humans exploiting this bounty. Still, the transition
from nomadism and the hunter/gatherer to sedentism and
farming was hardly revolutionary (Lewin, 1988). The process
was slow, with ts and starts, failures and limited success
along the way. Nevertheless, eventually a transition was
made, a transition from which turning back to the past life of
hunting and gathering was not possible. Moreover, once that
line had been irrevocably crossed, the long process of identifying, subduing, taming, and eventually domesticating animals began.
The list of domesticated animals is remarkably short. Although the list of candidates would appear impossibly long,
the table of species that made the transition from wild to
human dominated is limited. Among the large herbivorous
mammals one would list sheep, goats, cattle, horses, pigs,
camels, llamas, donkeys, water buffalo, and yaks. Other large
herbivores that are considered domesticated are mithans, bali
cattle, and reindeer. Among the birds that have been domesticated, the authors list chickens, ducks, geese, and turkeys.
A handful of other animals that are considered domesticated
would be dogs and cats, rabbits, mice and rats, and other
rodents useful in laboratory work, and a small assortment of
aquatic species useful as a food resource like trout, salmon,
and catsh. In constructing this list, it is worth considering the
earlier denition, along with an assessment of genetic change.
In the end, domestication is about human needs and human
goals. That is why, ultimately, the line between tame/captive
and domesticated, though gray and blurry in some places, rests
on the notion of breed. Domesticated animals are constructed around the notion of breed, a population of animals
with distinguishable, heritable characteristics.
Why then, is this list so short? Why are so few species called
into service by human societies? This topic has been addressed
by many authors (Budiansky, 1999; Diamond, 1997) and
many competing ideas have been put forward as potential
explanations (Anderson, 1998; Darwin, 1900; Sauer, 1969;
Trut et al., 2009). Nevertheless, a consensus is building around
the exploitation of neoteny as the fuel that drives the domestication process (Trut et al., 2009). Neoteny is the expression of juvenile traits in adults of any species, essentially
the juvenilization of the individual. In the context of animal
domestication, the critical component of the process would be
the exploitation of variation, especially genetic variation, in
neotenic traits (e.g., food begging, reduced fear in confronting
foreign species) expressed in older, more adult, individuals. To
be able to approach, tame, and control undomesticated animals, these neotenic characteristics of behavior and anatomy
463
would be part of any humans unconscious selection decisions. A series of now classic experiments in the fox demonstrated that selection for juvenile behavior traits produced
correlated changes in the physiology and morphology of these
now domesticated foxes (Trut et al., 2009). Among the changes
observed include oppy ears, curly tails, large eyes, shortened
forehead, and a shortened muzzle. This exploitation of
the variation in neoteny is now considered to play a similar
role in the domestication of the dog (Wayne, 2001) and by
extension to the other major species of domesticated animals,
including livestock (Clutton-Brock, 1999; Driscoll et al., 2009;
Price, 1999).
So to answer, why these animals; apparently these are
species that satisfy two essential requirements. They are species
that offer some special benet for human survival, and second,
they possess the biological (including genetic) variation in
neoteny permitting them to be manipulated and eventually
domesticated by our human ancestors. It is thus a two-way
street, we have the desire/need and the animal gives rise to the
capacity to meet this need.
It is indeed an interesting marriage, one with a unique
evolutionary history; a history with three dominant articles.
The rst article, the longest, is one spanning hundreds of
thousands of years under the forces of natural selection
imposed by evolution. This is an article where animals and
humans led distinct lives, intersecting across the environments
they both inhabited and the potential to relate as predator and
prey. The second article, no more than several thousand years,
spans the transition from wild to domesticated. This article is
where the marriage began, and in which it has spent the
most time. We are presently in the nal, third article spanning
little more than a handful of decades. However, it is in this
article where we witness the intensive breeding and management practices inherent in modern animal agriculture. It
has been in this most recent article that humans have exerted
their most powerful pressure and in many ways tying our
destiny to theirs. It is now examined what special characteristics are required to make it to this select group of species that
has moved from the wild to a state of ownership by a human
partner.
464
Domestication of Animals
Flexible Diet
The key component of this distinctive principle is competition
with humans for food resources. Though there are exceptions
(and dogs and cats are perhaps the most obvious), most domesticated animals do not compete directly with human
beings for their nutritive needs. Indeed, one of the benecial
attributes of cattle, sheep, and goats is that as ruminants they
complement human diets rather than compete (Pond et al.,
2005). It is not known whether at the time of domestication,
or today, these livestock species are notable for their consumption of byproduct feeds. In the well-established agricultural systems of the developing agriculturalists of the Tigris
Euphrates river basin (Peters et al., 2005), sheep and goats
provided a much valued complement to the dry-land grain
farming of this society. Put simply: humans ate the seeds, the
animals ate the stalks, providing meat, milk, ber, and manure
in the process (Harris, 2012). Together, a viable and sustainable food production system was implemented, and indeed
lasts to this day.
Dogs and cats are, of course, an exception, both animals
being carnivores and thus more directly competing with their
human owners for food resources. Of course, in the case of
cats, it is their diet of vermin that makes them so valuable to
human agricultural societies (Driscoll et al., 2007). Protection
of seed stores from the infestation of mice and rats makes the
cat a valuable, if in theory competitive, companion. Dogs
on the contrary provide no such simple niche explanation.
Instead this closest of humananimal bonds needs more to
explain it than simple dietary complementarity.
Contrasting the doghuman relationship with newly domesticated aquatic species like trout, catsh, and salmon are
precisely the challenge this topic addresses (Wurts, 2000). The
long-term sustainability of salmon culture, a top of the food
chain aquatic predator, surely calls into question the wisdom
of domestication. Regardless of the species-specic comments,
it is clear that as a general principle, the diet of the potential
domesticate is clearly among the rst questions a would-be
domesticator must address.
Growth/Developmental Rate
In todays agricultural economy, a market hog is expected to
reach 100 kg of live body weight by 20 weeks of age. A market
broiler can make it to 5 lbs by 7 weeks after hatching (Field
and Taylor, 2012). Of course, the rst domesticated ancestors
of these animals did not grow at such accelerated rates.
Nevertheless, domesticating elephants, or redwoods, is not a
strategy for sustainable success in a society living in 12-month
Human-Directed Breeding
This topic, the human control of breeding decisions of animals
raised in human communities, hardly needs emphasis in the
discussion for this concept is rmly embedded in the earlier
denition of domestication. However, human control over
breeding must be paramount in the domestication process.
Without the control of which animals are entitled to become
parents of the next generation, what is indeed the point of
domestication? As one might expect, most species do not
willingly forswear this control. The few species that have been
domesticated seem to have several common attributes to their
reproductive strategies, strategies that are now considered.
The rst is promiscuous mating. This refers to the lack of an
elaborate (or in some cases even a rudimentary) mating ritual.
A more pedestrian means of describing this concept is to say
that the animal must breed in captivity. And that is true
enough. However, the point to emphasize is one more broadly
based. It does a human society no good if animals will breed
in captivity but not the precise male and female combinations
we desire. That is why the term of promiscuous mating is
much preferred, a mating strategy in which females will accept
any male that the breeders determine is suitable to meet their
objectives. Ultimately, if one is to realize the full potential of
animal domestication, human mastery of breeding is essential.
This control is among the chief impediments one confronts in
taking the rst steps to shift a species from its wild state to one
of domestication (Zohary et al., 1998).
It may be interesting to speculate overcoming this challenge with the modern tools available for reproductive
manipulation. That is, with a more thorough understanding of
the physiology of reproduction in a species of interest, it might
be feasible to control reproduction in the laboratory, not in
the eld, pen, or cage. Such options were not available to our
ancestors. However, the future of animal domestication may
nd that the tools of biotechnology can open doors that are
closed today. Regardless, the challenge still remains of identifying who gets to be a parent and who does not. That fundamental decision is the key to domestication; our principal
power and our principal challenge.
Suitable Disposition
First, do no harm. If taken for granted, the conceit that domestication of wild animals was considered by our ancestors
to enhance their survival in a harsh world, then domesticating
Domestication of Animals
465
paradigm. Cattle, sheep, goats, and horses are all familiar living in large, often gregarious, social structures, where dominance and submission play important roles in the social fabric
of the group and individual. However as in any other of
the conditions of domestication described in this list, such a
requirement can be violated. One need only think of the
domesticated cat. These animals are often found as solitary
predators, yet have become one of the more ubiquitous of
domesticated animals. Thus, the list is more an outline of the
general principles than a rigid inventory of hard and fast
requirements. However a stable social structure, where individuals know their place and behave accordingly, is a useful
tool for humans to have seized on. By manipulating these
animals to see us as part of their social environment increases
the probability that these animals can be transitioned from
wild independent creatures to animals willing to tolerate our
control of their food, territory, and breeding.
Domestication is about control; and this crude outline of
the principles common to domesticated species (i.e., breeding
in captivity, exibility of diet, avoidance of panic, and a uid
yet stable social structure) provides the grease on the gears of
this domestication machine. Though not exhaustive, and certainly not part of a necessary and sufcient test of domestication, these concepts help understand and evaluate what our
ancestors had to contend with and the thoughts and plans that
must have danced in their heads.
Tendency to Panic
Perhaps not as obvious a characteristic as an aggressive disposition, animals suitable as domesticates must certainly have
a demeanor free of panic. Animals prone to ee, and ee
quickly, from approaching threats are a safety hazard to
themselves and their handlers. Imagine a Grants gazelle, an
ungulate capable of fast acceleration to speeds in excess of
45 mph, forced into an enclosure (Heglund and Taylor, 1988).
Sheep and goats deal with threats in a far different manner
than these speed-oriented mammals, and their suitability for
domestication is evident. This speed, coupled with the associated temperament of nervousness, of the hyperawareness of
threats makes such animals unlikely candidates for domestication. Not that attempts have not been made. Rather, one can
see and explain the seeds for the universal failure of these
attempts.
Social Structure
It is evident in our language; the plural for sheep and cattle
are the same as the singular. These successful examples of
domestication demonstrate that animals that live in large
groups, with a prevailing social structure, have an increased
likelihood of being shaped by humans from wild to domesticated animals (Price, 1984, 1999). How conspecics
interact with one another, especially in systems of a dominance/submissive hierarchy can play an important role in the
success of domestication. That is because humans can insert
themselves in the social hierarchy, a mechanism to force the
transition from wild to domesticate.
Like so many other conditions, this requirement of
domestication is not apparent in all species that have been
successfully domesticated. However it is the dominant
466
Domestication of Animals
Domestication of Animals
467
468
Domestication of Animals
Modications of appearance
Absent bones and other physical evidence can span centuries,
but are limited in comparisons of appearances between wild
and domesticated animals by those occasional cases where the
wild ancestor survives. That is, one can see the dramatic
changes in coat color and hair quality between dogs and gray
wolves. One can directly observe the changes through this
direct comparison. Indeed, in the circumstance of comparing
dogs and wolves some of the changes have been so great that it
is challenging to see the remnants of a wolf in many of the
breeds of dog today (Larson et al., 2012). However, the study is
no longer limited by direct visual comparison for some of
these softer traits. As seen, through the sequencing of ancient
DNA, the wild horse coat colors were quite different from the
patterns and colors seen today. Animals with little chance of
survival in the past can now be protected and encouraged to
reproduce.
One can also note the reduction in size (or presence) of
horns. In the wild, horns can play a valuable role in defending
oneself from predators or in securing food, territory, or mates
from conspecics. As domesticates, horns are a threat to their
human handlers and to other animals in the ock or herd. This
is another simple example of how domestication modies the
external appearance and functionality of the animals in our
care (Zeder, 2012).
One might think of this as the price an animal pays for
submitting to the domestication process in the rst place.
Traditional views of domestication made the process seem
to be one of human instigation and human domination.
Domestication of Animals
However the process is now thought to be more of a two-way
street; where humans hope to take advantage of this captive
resource and the animals submit to the capture, nding this a
path to increased access to resources (food, water, and territory) and eventual survival (Budiansky, 1999). Perhaps this
exploitation, and selection, for an animals willingness to live
within the connes set by humans is the greatest impact we
have had on their morphology, behavior, and appearance
(Udell et al., 2010). In our mutual goal, to enhance both our
survival strategies, we have shaped each other into a species
that was not there at the outset. Neither of us has left the
process, which continues still, as we began.
Impacts on People
In the end, the whole purpose of this article is to describe the
impact of the process of domestication on our view of animals, one another, and how this process has inuenced our
past as it guides our future. The domestication of plants and
animals coincided with and facilitated our transition from
small bands of hunters and gatherers into the complex technological society we have become today. As a result, trying to
assess the impact of animal domestication on humans is as
simple as saying: everything. Although such brevity is hardly
informative, it surely contains a kernel of truth. All that we are,
and all that we are to become, can be traced to the capture,
taming, and eventual subjugation of our fellow animal species.
Nevertheless, one can, and should, take some time and space
to illustrate this sweeping conclusion with a few examples.
No example may be more powerful in demonstrating the
impact of animal domestication on people than the origin
469
470
Domestication of Animals
Domestication of Animals
471
span since the domestication of cattle is relatively short (between 7000 and 8000 years), there has been a demonstrable
change in our genome, as evidenced by the recent work on
lactase persistence in human populations associated with
adult milk consumption (Tishkoff et al., 2006).
Like all mammals, human infants use milk as their sole
source of nutrients, gradually taking on solid food until weaning. During infancy, with rare exception, lactose, a disaccharide
of glucose and galactose, is broken into its two simple sugars by
the enzyme lactase-phlorizin hydrolase (LPH) in the small intestine (Swallow, 2003). The capacity to activate LPH and digest
lactose typically declines after weaning. However, some individuals maintain this capacity into adulthood, a trait called
lactase persistence. Lactase persistence is a dominant Mendelian trait. The fascinating element of this trait, however, is the
changing frequency of this dominant allele from one human
population to the next. That is, nonpastoralist populations in
Asia and Africa have a very low frequency of this allele; approximately 1% in China and between 5% and 20% in West
Africa (Durham, 1992; Swallow, 2003). However in populations that rely on milk as a food source into adulthood,
populations with the practice of keeping cows, the allele for
lactase persistence jumps to more than 90% in places like
Denmark and Sweden (Durham, 1992; Swallow, 2003). Other
populations and ethnic groups in Africa, with a culture of cattle
and milk consumption into adulthood also carry the persistence
allele in high frequency (Tishkoff et al., 2006). What we see
demonstrated here is the presence of a very strong selective
sweep, one that has dramatically altered human evolution in a
relatively short span of time. Domestication of animals has not
just changed how we live and how we eat, it has fundamentally
altered our very biology.
Conclusion
For most of our time as a species, whenever that may have
begun, human beings lived in ways little different from our
animal relatives and neighbors. However eventually we began
to live in groups and social settings where we began to feel
different, feeling distinct, and separate from the other animals.
Eventually that feeling would change, and as human social
groups evolved we began to question our relationship to, and
with, the animals around us. That feeling of distinction nally
brought us to the task of changing some of these animals to t
our needs and expectations; to move them from wild animals
to our now close domestic partners. What the future will
hold for our mutual relationship can only be guessed. What
remains certain is the importance this process has played in
our lives and culture.
472
Domestication of Animals
References
Anderson, K., 1998. Animal domestication in geographic perspective. Society and
Animals 6, 119135.
Armelagos, G.J., Brown, P.J., Turner, B., 2005. Evolutionary, historical and political
economic perspectives on health and disease. Social Science & Medicine 61,
755765.
Bar-Oz, G., Zeder, M., Hole, F., 2011. Role of mass-kill hunting strategies in the
extirpation of Persian gazelle (Gazella subgutturosa) in the northern Levant.
Proceedings of the National Academy of Sciences 108, 73457350.
Bar-Yosef, O., 2012. From foraging to farming in Western and Eastern Asia. In:
Gepts, P., Famula, T.R., Bettinger, R.L., et al. (Eds.), Biodiversity in Agriculture:
Domestication, Evolution and Sustainability. Cambridge: Cambridge University
Press.
Bellwood, P., Oxenham, M., 2008. The expansions of farming societies and the role
of the Neolithic demographic transition. In: Bocquet-Appel, J.P., Bar-Yosef, O.
(Eds.), The Neolithic Demographic Transition and its Consequences. New York:
Springer Verlag.
Bradley, D.G., 2006. Documenting domestication: Reading animal genetic texts. In:
Zeder, M.A., Bradley, D.G., Emshwiller, E., Smith, B.D. (Eds.), Documenting
Domestication: New Genetic and Archaeological Paradigms. Berkeley, CA:
University of California Press.
Budiansky, S., 1999. The Covenant of the Wild: Why Animals Chose Domestication:
With a New Preface. Yale University Press.
Bulliet, R.W., 2005. Hunters, Herders, and Hamburgers: The Past and Future of
HumanAnimal Relationships. New York, NY: Columbia University Press.
Catlin, G., 1973. Letters and Notes on the Manners, Customs, and Conditions of the
North American Indians: Written During Eight Years' Travel (18321839)
Amongst the Wildest Tribes of Indians in North America. New York: Dover
Publications.
Cauvin, J., Watkins, T., 1994. The Birth of the Gods and the Origins of Agriculture.
Cambridge University Press.
Childe, V.G., 1942. What Happened in History. New York: Penguin Books.
Clutton-Brock, J., 1995. Origins of the dog: Domestication and early history. In:
Serpell, J. (Ed.), The Domestic Dog: Its Evolution, Behaviour and Interactions
with People. Cambridge: Cambridge University Press.
Clutton-Brock, J., 1999. A Natural History of Domesticated Mammals. Cambridge
University Press.
Darwin, C., 1900. The Variation of Animals and Plants Under Domestication. New
York, NY: D. Appleton and Company.
Diamond, J., 1987. The worst mistake in the history of the human race. Discover 8,
6466.
Diamond, J.M., 1997. Guns, Germs, and Steel: The Fates of Human Societies. New
York: W.W. Norton & Co.
Dobney, K., Larson, G., 2006. Genetics and animal domestication: New windows on
an elusive process. Journal of Zoology 269, 261271.
Driscoll, C.A., Macdonald, D.W., O'brien, S.J., 2009. From wild animals to domestic
pets: An evolutionary view of domestication. Proceedings of the National
Academy of Sciences 106, 99719978.
Driscoll, C.A., Menotti-Raymond, M., Roca, A.L., et al., 2007. The Near Eastern
origin of cat domestication. Science 317, 519523.
Dudd, S.N., Evershed, R.P., 1998. Direct demonstration of milk as an element of
archaeological economies. Science 282, 14781481.
Durham, W.H., 1992. Coevolution: Genes, Culture, and Human Diversity. Stanford,
CA: Stanford University Press.
Emshwiller, E., 2006. Genetic data and plant domestication. In: Zeder, M.A., Bradley,
D.G., Emshwiller, E., Smith, B.D. (Eds.), Documenting Domestication: New
Genetic and Archaeological Paradigms. Berkeley, CA: University of California
Press.
Ewers, J.C., 1955. The Horse in Blackfoot Indian Culture: With Comparative Material
from Other Western Tribes. Washington, DC: Smithsonian Institution.
Fernandez, H., Taberlet, P., Mashkour, M., Vigne, J.D., Luikart, G., 2005. Assessing
the origin and diffusion of domestic goats using ancient DNA. In: Vigne, J.D.,
Peters, J., Helner, D. (Eds.), The First Steps of Animal Domestication: New
Archaeozoological Approaches. Oxford: Oxbow Press.
Field, T.G., Taylor, R.E., 2012. Scientic Farm Animal Production: An Introduction to
Animal Science. Upper Saddle River, NJ: Prentice-Hall International, Inc.
Goodman, A.H., Martin, D.L., Aremlagos, G.J., Clark, G., 1984. Indications of stress
from bone and teeth. In: Cohen, M.N., Armelagos, G.J. (Eds.), Paleopathology at
the Origins of Agriculture. New York: Academic Press, Inc.
Gtherstrm, A., Anderung, C., Hellborg, L., et al., 2005. Cattle domestication in the
Near East was followed by hybridization with aurochs bulls in Europe.
Proceedings of the Royal Society B: Biological Sciences 272, 23452351.
Domestication of Animals
Rathbun, T.A., 1984. Skeletal pathology from the Paleolithic through the Metal Ages
in Iran and Iraq. In: Cohen, M.N., Armelagos, G.J. (Eds.), Paleopathology at the
Origins of Agriculture. New York: Academic Press, Inc.
Saa Segui, M., Helmer, D., Peters, J., Von Den Driesch, A., 1999. Early animal
husbandry in the Northern Levant. Palorient 25, 2748.
Sauer, C., 1969. Seeds, Spades, Hearth and Herds (Second edition of Agricultural
Origins and Dispersals). Cambridge, MA: MIT Press.
Swallow, D.M., 2003. Genetics of lactase persistence and lactose intolerance. Annual
Review of Genetics 37, 197219.
Tishkoff, S.A., Reed, F.A., Ranciaro, A., et al., 2006. Convergent adaptation
of human lactase persistence in Africa and Europe. Nature Genetics 39,
3140.
Troy, C.S., Machugh, D.E., Bailey, J.F., et al., 2001. Genetic evidence for NearEastern origins of European cattle. Nature 410, 10881091.
Trut, L., Oskina, I., Kharlamova, A., 2009. Animal evolution during domestication:
The domesticated fox as a model. BioEssays 31, 349360.
Udell, M.a.R., Dorey, N.R., Wynne, C.D.L., 2010. What did domestication do to
dogs? A new account of dogs' sensitivity to human actions. Biological Reviews
85, 327345.
Vigne, J.D., 2008. Zooarchaeological aspects of the Neolithic diet transition in the
Near East and Europe, and their putative relationships with the Neolithic
demographic transition. In: Bocquet-Appel, J.P., Bar-Yosef, O. (Eds.), The
Neolithic Demographic Transition and its Consequences. New York: Springer
Verlag.
Vigne, J.D., Peters, J., Helmer, D., 2005. The First Steps of Animal Domestication.
Oxford: Oxbow Books.
Vila, C., Leonard, J.A., Gtherstrm, A., et al., 2001. Widespread origins of
domestic horse lineages. Science 291, 474477.
Wayne, R.K., 2001. Consequences of domestication: Morphological diversity of the
dog. In: Ruvinsky, A., Sampson, J. (Eds.), The Genetics of the Dog, rst ed.
Wallingford, UK: CAB International.
473
Weisdorf, J.L., 2005. From foraging to farming: Explaining the Neolithic revolution.
Journal of Economic Surveys 19, 561586.
Wheeler, J.C., Chikhi, L., Bruford, M.W., 2006. Genetic analysis of the origins of
domestic South American camelids. In: Zeder, M.A., Bradley, D.G., Emshwiller,
E., Smith, B.D. (Eds.), Documenting Domestication: New Genetic and
Archaeological Paradigms. Berkeley, CA: University of California Press.
Wurts, W.A., 2000. Sustainable aquaculture in the twenty-rst century. Reviews in
Fisheries Science 8, 141150.
Zeder, M.A., 2012. Pathways to animal domestication. In: Gepts, P., Famula, T.R.,
Bettinger, R.L. et al. (Eds.), Biodiversity in Agriculture: Domestication, Evolution
and Sustainability. Cambridge: Cambridge University Press.
Zeder, M.A., 2006a. Archaeological approaches to documenting animal
domestication. In: Zeder, M.A., Bradley, D.G., Emshwiller, E., Smith, B.D. (Eds.),
Documenting Domestication: New Genetic and Archaeological Paradigms.
Berkeley, CA: University of California Press.
Zeder, M.A., 2006b. Central questions in the domestication of plants and animals.
Evolutionary Anthropology: Issues, News, and Reviews 15, 105117.
Zeder, M.A., 2006c. A critical examination of markers of initial domestication in
goats (Capra hircus). In: Zeder, M.A., Bradley, D.G., Emshwiller, E., Smith, B.D.
(Eds.), Documenting Domestication: New Genetic and Archaeological Paradigms.
Berkeley, CA: University of California Press.
Zeder, M.A., Bradley, D.B., Emshwiller, E., Smith, B.D., 2006a. Documenting
domestication: Bringing together plants, animals, archaeology, and genetics. In:
Zeder, M.A., Bradley, D.G., Emshwiller, E., Smith, B.D. (Eds.), Documenting
Domestication: New Genetic and Archaeological Paradigms. Berkeley, CA:
University of California Press.
Zeder, M.A., Emshwiller, E., Smith, B.D., Bradley, D.G., 2006b. Documenting
domestication: The intersection of genetics and archaeology. Trends in Genetics
22, 139155.
Zohary, D., Tchernov, E., Horwitz, L., 1998. The role of unconscious selection in the
domestication of sheep and goats. Journal of Zoology 245, 129135.
Domestication of Plants
P Gepts, University of California, Davis, CA, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Archaeobotany The identication and analysis of
botanical remains found in archeological investigations. The
remains can be subdivided into macroremains (identiable
to the naked eye) and microremains (require the use of a
microscope). Among macroremains are seeds and pods.
Microremains include pollen grains and subcellular
structures like starch grains and phytoliths (silica deposit
inside plant cells). The shape of microremains can be
diagnostic of the identity of the plant material. The
conservation of archaeobotanical remains can be favored by
certain environmental conditions (like dryness or excess
water).
Centers of agricultural origins Agriculture started in
multiple locations in the world some 10 000 years ago.
These locations (where crop domestications took place) are
distributed in some 10 areas generally between 301 northern
latitude and southern latitude. They tend to occur in areas
with higher levels of biodiversity.
Domestication Evolutionary process driven by natural
and human (whether conscious or unconscious) selection
applied to wild plants or animals and leading to adaptation
to cultivation and consumption or utilization.
Domestication can be complete, whereby organisms
become entirely dependent on humans for their continued
existence or can be partial or incipient, whereby they still
reproduce independently of human intervention.
Domestication syndrome A set of morphological,
biochemical, and physiological traits that distinguishes
domesticated plants or animals from their wild progenitor.
These traits depend on the life history (annual vs. perennial)
and reproductive system (outcrossing, selng, and
vegetative reproduction). Traits affected include dispersal of
Introduction
The evolutionary lineage leading to the modern human species
(Homo sapiens) has been marked by several key inventions,
such as the development of increasingly sophisticated tools
(Stout, 2011), the mastery of re (Alperson-Al and GorenInbar, 2010; Berna et al., 2012; Twomey, 2013), the acquisition of writing (Houston, 2004), and the current digital
revolution. Among these inventions is agriculture or the
transition from hunting-gathering (HG) to the cultivation of
crops and tending of animals. This transition initiated a
change that cannot be overestimated in all aspects of life on
the earth, including the biological and physical environment
and, obviously, also the way of life of humans. It is, therefore,
not surprising that this transition has been called the Neolithic
Revolution.
The signs of the changes brought about by the momentous
introduction of agriculture are numerous. For example, many
474
famous natural landscapes on the earth are actually agricultural landscapes: the rice terraces of Yunnan in China, the
rolling, cypress-studded lands of Tuscany in Italy, and the bigsky, luminous plains of the Palouse in Northwest United
States. Thirty-eight percent of total land area is now devoted to
agriculture, making it currently the single most important land
use. For example, forests (most of which are subjected to some
type of anthropic exploitation) only account for 30% of the
land area (FAO, Land use database).
Among the changes that were more or less concurrent with
the origination of agriculture were sedentism (as opposed to
nomadism) and the appearance of villages and ultimately
cities, the introduction of ceramics, the transformation of
more egalitarian societies into more hierarchical ones, a
stronger division of labor by the addition of nonfood production related occupations, and, later on, the introduction of
writing. The actual sequence and order of these technologies is
still being disputed and may diverge in different regions where
doi:10.1016/B978-0-444-52512-3.00231-X
Domestication of Plants
475
476
Domestication of Plants
Domestication of Plants
Central Asia
Eastern North
America
Sunflower
Tobacco
Sassafras
Strawberry
Pecan
Sumpweed
Mesoamerica (including
Central America)
Common bean
Lima bean
Maize
Pepper (capsicum)
Upland cotton
Avocado
Tomato
Papaya
Vanilla
Agave
Sweet potato
Squash
Amaranth
Andean South
America
Common bean
Lima bean
Pima cotton
Potato
Oca
Arracacha
Pepper (Capsicum)
Maca
Strawberry
Squash
Quinoa
Amaranth
Apple
Pomegranate
Horseradish
Walnut
Southwest Asia or
Fertile Crescent
China
Wheats
Barley
Pea
Lentil
Chickpea
Onion
Date palm
Grape
Millets (foxtail)
Rice (japonica)
Tea
Peach
Lichee
Mulberry
Soybean
Citrus
South Asia
Africa
Lowland South
America
Cassava
Peanut
Peach palm
Pepper
Pineapple
Cacao
Aai
Brazil nut
Cashew
Guaran
477
Sorghum
Pearl millet
Cowpea
Bambara groundnut
Oil palm
Enset
Rice (African)
Okra
Coffee
Watermelon
Hyacinth bean
Shea
Teff
Mung bean
Mango
Rice (indica)
Giant taro
Ginger
Jute
Eggplant
Southeast Asia,
Sunda, and Sahul
Banana
Sugarcane
Durian
Coconut
Sago palm
Clove
Breadfruit
478
Domestication of Plants
then assess to what extent they have played a role in the origins of agriculture and crop domestication. Such an analysis
reveals that several crops originated in two biomes, the
Mediterranean and tropical savanna biomes. Among crops
domesticated in the Mediterranean biome are those from the
Fertile Crescent, such as wheat, barley, lentil, chickpea, and
pea. Crops domesticated in the savanna biome (and adjacent
dry tropical forest) include crops such as maize, common
bean, rice, cassava, and peanut. These two biomes share the
characteristic of a long dry season, whether during the summer
for the former or the winter for the latter (monsoon-type of
climate). The dry season may have been an impetus toward
cultivation because of the increased need to develop a store of
food, irrespective of whether they are grain or roots.
Domestications are not exclusive to the Mediterranean or
tropical dry savanna and forest biomes. Other environments
have contributed crops as well, such as highland environments
(e.g., coffee in the Ethiopian plateau; several root crops, including potato in the Andes Mountains). Coastal areas have
contributed coconut, beets and more recently sugarbeets, and
cotton. Temperate forest may have contributed fruits and nuts,
such as apples, pear, cherry, and walnut. Tropical rain forests
were most likely the home of sugarcane, banana and plantain,
mango, and cacao.
Centers of domestication tend to occur in areas of higher
biodiversity or biodiversity hotspots (Gepts, 2008). Thus, actual or prospective farmers have been opportunistic in recognizing potential crop plants by domesticating them from local
biodiversity, wherever they were located. In this regard, it is
perhaps not surprising that certain species or groups of related
species have been domesticated multiple times. For example,
there are ve domesticated Phaseolus bean species, two of
which common bean and lima bean (Phaseolus lunatus)
have been domesticated twice, in Mesoamerica and in the
Andes (Gepts, 1998; Serrano-Serrano et al., 2012; AnduezaNoh et al., 2013). Three other domesticated Phaseolus species
runner bean (Phaseolus coccineus), year bean (Phaseolus dumosus), and tepary bean (Phaseolus acutifolius) were domesticated in ecologically different environment (Freytag and
Debouck, 2002), reecting a possible choice on the part of
farmers to select different domesticates rather than adapt a
single domesticate to a broad range of environments. Other
examples are Capsicum species (ve species domesticated in
different areas of Mexico, Central America, and South America;
Pickersgill, 2007), cotton (four species domesticated, two in
the Old World and two in the New World; Wendel et al.,
2009), and wheat (three species domesticated in and around
the Fertile Crescent; Willcox, 2013).
Domestication of Plants
479
480
Domestication of Plants
Domestication of Plants
481
regions as previously identied QTLs for the sunower domestication syndrome. The timing of selection could be presumably narrowed down to the initial domestication process
per se or the subsequent improvement stage by distinguishing
within the domesticated group between the so-called primitive
(or landrace) varieties and varieties improved by selective
breeding. Hufford et al. (2012) conducted a genome-wide
resequencing in wild, landrace, and improved maize entries.
Among their ndings were the existence of stronger selection
during the actual domestication phase than in the subsequent
improvement phase. An additional observation is the existence
of potential introgression from a wild relative (Z. mays var.
mexicana), which is not the progenitor of maize but contributed nevertheless alleles that are potentially instrumental in
adaptation to higher altitudes (van Heerwaarden et al., 2011).
Furthermore, several regions were identied that showed evidence of selective sweeps, representing some 12% of the
maize gene set. Some of these genes map near QTLs that had
been identied previously. As a note of caution, the separation
between domestication and improvement genes may not always be clear-cut, and in some cases, such as color or shape,
variants may involve arbitrary decisions as to the timing of the
appearance of these variants. In addition, some domestication
genes (identied as such by their absence in the wild progenitor gene pool) are not distributed across the entire domestication gene pool but characterize only a subset of the
gene pool, suggesting that there is no clear dichotomy between
these two classes of genes.
Concurrent with these studies, many genes controlling important domestication traits, whether they are considered domestication or improvement traits, have been isolated using
map-based cloning of QTLs or a candidate gene approach,
based on sequence information of genes controlling similar
phenotypes in other species (Paterson et al., 1995; Lenser and
Theyen, 2013). Doebley et al. (2006), Gross and Olsen (2010),
and Olsen and Wendel (2013) presented recent overviews
of genes that have been isolated. The majority of these genes
are transcriptional regulators, such as the tb1 gene in maize
(conditioning the single-stem, nonbranched plant type of
domesticated maize; Wang et al., 1999); however, a signicant
proportion codes for structural genes like enzymes, such as the
waxy locus (not only in rice but also in broomcorn millet and
maize) and the BADH2 gene (for rice fragrance). The types
of mutations involved are diverse and include nucleotide substitutions (leading to premature stop codons or amino acid
substitutions), insertions or deletions (indels), transposon insertions, or cis-regulatory changes (the latter outside the gene,
such as is the case for the tb1 locus controlled by an enhancerlike transposon insertion some 65 kbp upstream of the gene).
In most cases, a single causative mutation can be identied. An
exception to this pattern is the PvTFL1y gene, which is responsible for the determinate growth pattern in common bean, in
which a retrotransposon insertion, synonymous substitutions,
nonsynonymous substitutions, indels, a putative intron-splicing
failure, and a deletion of the entire locus, all lead to loss of
function, consistent with the recessive nature of the determinate
phenotype (Repinski et al., 2012; Kwak et al., 2012). This observation suggests that the determinate trait has been selected
multiple times, underscoring the importance of earliness and
compact growth habit in crop cultivation.
482
Domestication of Plants
Domestication of Plants
References
Abbo, S., Rachamim, E., Zehavi, Y., et al., 2011. Experimental growing of wild pea
in Israel and its bearing on Near Eastern plant domestication. Annals of Botany
107, 13991404.
Abbo, S., Zezak, I., Zehavi, Y., et al., 2013. Six seasons of wild pea harvest in
Israel: Bearing on Near Eastern plant domestication. Journal of Archeological
Science 40, 20952100.
Allaby, R.G., Fuller, D.Q., Brown, T.A., 2008. The genetic expectations of a
protracted model for the origins of domesticated crops. Proceedings of the
National Academy of Sciences 105, 1398213986.
Allison, P.A., Bottjer, D.J., 2011. Taphonomy: Process and Bias through Time,
second ed. Dordrecht: Springer.
Alperson-Al, N., Goren-Inbar, N., 2010. The Acheulian Site of Gesher Benot
Yaaqov Volume II: Ancient Flames and Controlled Use of Fire. Berlin: Springer.
dAlpoim Guedes, J., 2011. Millets, rice, social complexity, and the spread of
agriculture to the Chengdu Plain and Southwest China. Rice 4, 104113.
Alvarez, N., Garine, E., Khasah, C., et al., 2005. Farmers practices, metapopulation
dynamics, and conservation of agricultural biodiversity on-farm: A case study of
sorghum among the Duupa in sub-sahelian Cameroon. Biological Conservation
121, 533543.
Andrade-Snchez, P., Gore, M.A., Heun, J.T., et al., 2013. Development and
evaluation of a eld-based high-throughput phenotyping platform. Functional
Plant Biology 41, 6879.
Andueza-Noh, R.H., Serrano-Serrano, M.L., Chacn Snchez, M.I., et al., 2013.
Multiple domestications of the Mesoamerican gene pool of lima bean (Phaseolus
483
lunatus L.): Evidence from chloroplast DNA sequences. Genetic Resources and
Crop Evolution 60, 10691086.
Asfaw, A., Almekinders, C.J.M., Blair, M.W., Struik, P.C., 2012. Participatory
approach in common bean (Phaseolus vulgaris L.) breeding for drought tolerance
for southern Ethiopia. Plant Breeding 131, 125134.
Balter, M., 2010. The tangled roots of agriculture. Science 327, 404406.
Ban, N., Coomes, O.T., 2004. Home gardens in Amazonian Peru: Diversity and
exchange of planting material. Geographical Review 94, 348367.
Barnaud, A., Joly, H.I., McKey, D., et al., 2008. Management of sorghum (Sorghum
bicolor) genetic resources among Duupa farmers (northern Cameroon). Cahiers
Agricultures 17, 178182.
Bar-Yosef, O., 2011. Climatic uctuations and early farming in West and East Asia.
Current Anthropology 52, S175S193.
Battilana, J., Lorenzi, S., Moreira, F., et al., 2013. Linkage mapping and molecular
diversity at the ower sex locus in wild and cultivated grapevine reveal a
prominent SSR haplotype in hermaphrodite plants. Molecular Biotechnology 54,
10311037.
Benz, B., 2001. Archeological evidence of teosinte domestication from Guil Naquitz.
Proceedings of the National Academy of Sciences 98, 21042106.
Berna, F., Goldberg, P., Horwitz, L.K., et al., 2012. Microstratigraphic evidence of
in situ re in the Acheulean strata of Wonderwerk Cave, Northern Cape province,
South Africa. Proceedings of the National Academy of Sciences 109,
E1215E1220.
Bettinger, R.L., Barton, L., Morgan, C., 2010. The origins of food production in
north China: A different kind of agricultural revolution. Evolutionary Anthropology
19, 921.
Bitocchi, E., Bellucci, E., Giardini, A., et al., 2013. Molecular analysis of the parallel
domestication of the common bean (Phaseolus vulgaris) in Mesoamerica and the
Andes. New Phytologist 197, 300313.
Bradbury, E.J., Duputi, A., Deltre, M., et al., 2013. Geographic differences in
patterns of genetic differentiation among bitter and sweet manioc (Manihot
esculenta subsp. esculenta; Euphorbiaceae). American Journal of Botany 100,
857866.
Brown, C.H., 2006. Prehistoric chronology of the common bean in the New World:
The linguistic evidence. American Anthropologist 108, 507516.
Brown, C.H., Clement, C.R., Epps, P., Luedeling, E., Wichmann, S., 2013a. The
paleobiolinguistics of domesticated chili pepper (Capsicum spp.). Ethnobiology
Letters 4, 111.
Brown, C.H., Clement, C.R., Epps, P., Luedeling, E., Wichmann, S., 2013b. The
paleobiolinguistics of domesticated manioc (Manihot esculenta). Ethnobiology
Letters 4, 6170.
Buchmann, C., 2009. Cuban home gardens and their role in social ecological
resilience. Human Ecology 37, 705721.
Burke, J.M., Burger, J.C., Chapman, M.A., 2007. Crop evolution: From genetics to
genomics. Current Opinion in Genetics & Development 17, 525532.
Caicedo, A.L., Williamson, S.H., Hernandez, R.D., et al., 2007. Genome-wide patterns
of nucleotide polymorphism in domesticated rice. PLOS Genetics 3, e163.
de Candolle, A., 1882. Lorigine des plantes cultives. New York, NY: Appleton.
English translation: The origin of cultivated plants.
Ceccarelli, S., Grando, S., Singh, M., et al., 2003. A methodological study on
participatory barley breeding II. Response to selection. Euphytica 133,
185200.
Ceccarelli, S., Grando, S., Tutwiler, R., et al., 2000. A methodological study on
participatory barley breeding I. Selection phase. Euphytica 111, 91104.
Chapman, M.A., Pashley, C.H., Wenzler, J., et al., 2008. A genomic scan for
selection reveals candidates for genes involved in the evolution of cultivated
sunower (Helianthus annuus). Plant Cell 20, 29312945.
Clement, C., De Cristo-Arajo, M., Coppens DEeckenbrugge, G., Alves Pereira, A.,
Picano-Rodrigues, D., 2010. Origin and domestication of native Amazonian
crops. Diversity 2, 72106.
Clough, Y., Barkmann, J., Juhrbandt, J., et al., 2011. Combining high biodiversity
with high yields in tropical agroforests. Proceedings of the National Academy of
Sciences 108, 83118316.
Cohen, D.J., 2011. The beginnings of agriculture in China: A multiregional view.
Current Anthropology 52, S273S293.
Colledge, S., Conolly, J., 2010. Reassessing the evidence for the cultivation of wild
crops during the Younger Dryas at Tell Abu Hureyra, Syria. Environmental
Archeology 15, 124138.
Cornille, A., Gladieux, P., Giraud, T., 2013. Crop-to-wild gene ow and spatial
genetic structure in the closest wild relatives of the cultivated apple. Evolutionary
Applications 6, 737748.
Couturon, E., Mariac, C., Bezanon, G., Lauga, J., Renno, J.F., 2003. Impact of
natural and human selection on the frequency of the F1 hybrid between
484
Domestication of Plants
cultivated and wild pearl millet (Pennisetum glaucum (L.) R. Br.). Euphytica 133,
329337.
Dai, F., Nevo, E., Wu, D.Z., et al., 2012. Tibet is one of the centers of domestication
of cultivated barley. Proceedings of the National Academy of Sciences 109,
1696916973.
Dempewolf, H., Rieseberg, L., Cronk, Q., 2008. Crop domestication in the
Compositae: A family-wide trait assessment. Genetic Resources and Crop
Evolution 55, 11411157.
Diamond, J., 1997. Guns, Germs, and Steel. New York, NY: Norton.
Doebley, J., 1992. Molecular systematics and crop evolution. In: Soltis, P.S., Soltis,
D.E., Doyle, J.J. (Eds.), Molecular Systematics of Plants. New York, NY:
Chapman Hall, pp. 202222.
Doebley, J.F., Gaut, B.S., Smith, B.D., 2006. The molecular genetics of crop
domestication. Cell 127, 13091321.
Durand, E., Tenaillon, M., Ridel, C., et al., 2010. Standing variation and new
mutations both contribute to a fast response to selection for owering time in
maize inbreds. BMC Evolutionary Biology 10, 2.
Elias, M., McKey, D., Panaud, O., Anstett, M.C., Robert, T., 2001. Traditional
management of cassava morphological and genetic diversity by the Makushi
Amerindians (Guyana, South America): Perspectives for on-farm conservation of
crop genetic resources. Euphytica 120, 143157.
Eyre-Walker, A., Gaut, R., Hilton, H., Feldman, D., Gaut, B., 1998. Investigation of
the bottleneck leading to the domestication of maize. Proceedings of the National
Academy of Sciences 95, 44414446.
Freeman, G.F., 1912. Southwestern Beans and Teparies. Tucson, AZ: University of
Arizona Agricultural Experiment Station. pp. 573619. Bulletin 68.
Freytag, G.F., Debouck, D.G., 2002. Taxonomy, Distribution, and Ecology of the
Genus Phaseolus (Leguminosae Papilionoideae) in North America, Mexico and
Central America. Forth Worth, TX: Botanical Research Institute of Texas.
Fu, W., Akey, J.M., 2013. Selection and adaptation in the human genome. Annual
Review of Genomics and Human Genetics 14, 467489.
Fuller, D.Q., 2007. Contrasting patterns in crop domestication and domestication
rates: Recent archaeobotanical insights from the Old World. Annals of Botany
100, 903924.
Fuller, D.Q., Allaby, R., 2009. Seed dispersal and crop domestication: Shattering,
germination and seasonality in evolution under cultivation. In: stergaard, L.
(Ed.), Annual Plant Reviews Volume 38: Fruit Development and Seed Dispersal.
Oxford: Wiley-Blackwell, pp. 238295.
Fuller, D.Q., Asouti, E., Purugganan, M.D., 2012. Cultivation as slow evolutionary
entanglement: Comparative data on rate and sequence of domestication.
Vegetation History and Archaeobotany 21, 131145.
Fuller, D.Q., Qin, L., Zheng, Y.F., et al., 2009. The domestication process and
domestication rate in rice: Spikelet bases from the Lower Yangtze. Science 323,
16071610.
Fuller, D.Q., Willcox, G., Allaby, R.G., 2012. Early agricultural pathways: Moving
outside the core area hypothesis in Southwest Asia. Journal of Experimental
Botany 63, 617633.
Furbank, R.T., Tester, M., 2011. Phenomics Technologies to relieve the
phenotyping bottleneck. Trends in Plant Science 16, 635644.
Gepts, P., 1993. The use of molecular and biochemical markers in crop evolution
studies. Evolutionary Biology 27, 5194.
Gepts, P., 1998. Origin and evolution of common bean: Past events and recent
trends. HortScience 33, 11241130.
Gepts, P., 2004. Domestication as a long-term selection experiment. Plant Breeding
Reviews 24 (Part 2), 144.
Gepts, P., 2006. Plant genetic resources conservation and utilization: The
accomplishments and future of a societal insurance policy. Crop Science 46,
22782292.
Gepts, P., 2008. Tropical environments, biodiversity, and the origin of crops. In:
Moore, P., Ming, R. (Eds.), Genomics of Tropical Crop Plants. Berlin: Springer,
pp. 120.
Gross, B.L., Olsen, K.M., 2010. Genetic perspectives on crop domestication. Trends
in Plant Science 15, 529537.
Guo, J., Wang, Y., Song, C., et al., 2010. A single origin and moderate bottleneck
during domestication of soybean (Glycine max): Implications from microsatellites
and nucleotide sequences. Annals of Botany 106, 505514.
Hammer, K., 1984. Das Domestikationssyndrom. Kulturpanze 32, 1134.
Hancock, J.F., 2004. Plant Evolution and the Origin of Crop Species, second ed.
Wallingford, Oxon: CAB International.
Harlan, J., 1967. A wild wheat harvest. Archeology 20, 197201.
Harlan, J.R., 1992. Crops and Man. Madison, WI: American Society of Agronomy.
Harlan, J.R., de Wet, J.M.J., 1971. Towards a rational classication of cultivated
plants. Taxon 20, 509517.
Harlan, J., de Wet, J., Price, G., 1973. Comparative evolution of cereals. Evolution
27, 311325.
Harper, J.L., Lovell, P.H., Moore, K.G., 1970. The shapes and sizes of seeds.
Annual Review of Ecology and Systematics 1, 327356.
Hedrick, U., 1931. The Vegetables of New York. I: Legumes, Cucurbits, Corn,
Alliums, Asparagus. Part ii. Beans. Albany, NY: J.B. Lyon.
van Heerwaarden, J., Doebley, J., Briggs, W.H., et al. 2011. Genetic signals of
origin, spread, and introgression in a large sample of maize landraces. In:
Proceedings of the National Academy of Sciences.
Hillman, G.C., Davies, M.S., 1990. Domestication rates in wild-type wheats and
barley under primitive cultivation. Biological Journal Linnean Society 39,
3978.
Houston, S.D., 2004. The First Writing: Script Invention as History and Process.
Cambridge: Cambridge University Press.
Hufford, M.B., Lubinsky, P., Pyhjrvi, T., et al., 2013. The genomic signature of
crop-wild introgression in maize. PLOS Genetics 9, e1003477.
Hufford, M.B., Xu, X., van Heerwaarden, J., et al., 2012. Comparative population
genomics of maize domestication and improvement. Nature Genetics 44, 808.
U118.
Hyten, D.L., Choi, I.-Y., Song, Q., et al., 2007. Highly variable patterns of linkage
disequilibrium in multiple soybean populations. Genetics 175, 19371944.
Jaenicke-Desprs, V., Buckler, E.S., Smith, B.D., et al., 2003. Early allelic selection
in maize as revealed by ancient DNA. Science 302, 12061208.
Johannsen, W., 1909. Elementen der Exakten Erblichkeitslehre. Jena: Fisher.
Kaplan, L., Lynch, T., 1999. Phaseolus (Fabaceae) in archeology: AMS radiocarbon
dates and their signicance for pre-Columbian agriculture. Economic Botany 53,
261272.
Kiers, E.T., Leakey, R.R.B., Izac, A.-M., et al., 2008. Agriculture at a crossroads.
Science 320, 320321.
Kolkman, J.M., Berry, S.T., Leon, A.J., et al., 2007. Single nucleotide
polymorphisms and linkage disequilibrium in sunower. Genetics 177,
457468.
Kuzmin, Y.V., Jull, A.J.T., Burr, G.S., 2011. Major patterns in the Neolithic
chronology of East Asia: Issues of the origin of pottery, agriculture, and
civilization. Radiocarbon 51, 891903.
Kwak, M., Gepts, P., 2009. Structure of genetic diversity in the two major gene
pools of common bean (Phaseolus vulgaris L., Fabaceae). Theoretical and
Applied Genetics 118, 979992.
Kwak, M., Kami, J.A., Gepts, P., 2009. The putative Mesoamerican domestication
center of Phaseolus vulgaris is located in the Lerma-Santiago basin of Mexico.
Crop Science 49, 554563.
Kwak, M., Toro, O., Debouck, D., Gepts, P., 2012. Multiple origins of the
determinate growth habit in domesticated common bean (Phaseolus vulgaris L.).
Annals of Botany 110, 15731580.
Ladizinsky, G., 1985. Founder effect in crop-plant evolution. Economic Botany 39,
191198.
Ladizinsky, G., 1998. Plant Evolution under Domestication. Dordrecht: Kluwer.
Lakis, G., Ousmane, A.M., Sanoussi, D., et al., 2011. Evolutionary dynamics of cycle
length in pearl millet: The role of farmers practices and gene ow. Genetica 139,
13671380.
Lam, H.-M., Xu, X., Liu, X., et al., 2010. Resequencing of 31 wild and cultivated
soybean genomes identies patterns of genetic diversity and selection. Nature
Genetics 42, 10531059.
Leakey, R.R.B., 1998. Agroforestry in the humid lowlands of West Africa: Some
reections on future directions for research. Agroforestry Systems 40,
253262.
Leakey, R.R.B., 2012. Participatory domestication of indigenous fruit and nut trees:
New crops for sustainable agriculture in developing countries. In: Gepts, P.,
Famula, T.R., Bettinger, R., et al. (Eds.), Biodiversity in Agriculture:
Domestication, Evolution, and Sustainability. Cambridge: Cambridge University
Press, pp. 479501.
Leakey, R.R.B., Asaah, E.K., 2013. Underutilised species as the backbone of
multifunctional agriculture The next wave of crop domestication. Acta
Horticulturae 979, 293310.
Lenser, T., Theyen, G., 2013. Molecular mechanisms involved in convergent crop
domestication. Trends in Plant Science 18, 704714.
Livi-Bacci, M., 2012. A Concise History of World Population. Oxford: Wiley.
Loaiza-Figueroa, F., Ritland, K., Cancino, J.A.L., Tanskley, S.D., 1989. Patterns of
genetic variation of the genus Capsicum (Solanaceae) in Mexico. Plant
Systematics and Evolution 165, 159188.
Maisels, C., 1993. The Emergence of Civilization: From Hunting and Gathering
To Agriculture, Cities, and the State in the Near East. New York, NY:
Routledge.
Domestication of Plants
von Martens, G., 1860. Die Gartenbohnen: Ihre Verbreitung, Cultur und Bentzung.
Stuttgart: Verlag von Ebner & Seubert. Available at: https://play.google.com/store/
books/detailsid=VyhAAAAAcAAJ (accessed 01.10.13).
Matsuoka, Y., Vigouroux, Y., Goodman, M.M., et al., 2002. A single domestication
for maize shown by multilocus microsatellite genotyping. Proceedings of the
National Academy of Sciences 99, 60806084.
McCouch, S., Baute, G.J., Bradeen, J., et al., 2013. Agriculture: Feeding the future.
Nature 499, 2324.
McKey, D., Elias, M., Pujol, B., Duputi, A., 2010. The evolutionary ecology of
clonally propagated domesticated plants. New Phytologist 186, 318332.
McKey, D.B., Elias, M., Pujol, B., Duputi, A., 2012. Ecological approaches to crop
domestication. In: Gepts, P., Famula, T.R., Bettinger, R., Brush, S.B., Damania,
A.B., McGuire, P.E., Qualset, C.O. (Eds.), Biodiversity in Agriculture:
Domestication, Evolution, and Sustainability. Cambridge: Cambridge University
Press, pp. 377406.
Meyer, R.S., DuVal, A.E., Jensen, H.R., 2012. Patterns and processes in crop
domestication: An historical review and quantitative analysis of 203 global food
crops. New Phytologist 196, 2948.
Miller, A.J., Gross, B.L., 2011. From forest to eld: Perennial fruit crop
domestication. American Journal of Botany 98, 13891414.
Mochida, K., Shinozaki, K., 2011. Advances in omics and bioinformatics tools for
systems analyses of plant functions. Plant and Cell Physiology 52, 20172038.
Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B., Worm, B., 2011. How many
species are there on earth and in the ocean? PLOS Biology 9, e1001127.
Morrell, P.L., Clegg, M.T., 2007. Genetic evidence for a second domestication of
barley (Hordeum vulgare) east of the Fertile Crescent. Proceedings of the
National Academy of Sciences 104, 32893294.
Motto, M., Soressi, G.P., Salamini, F., 1978. Seed size inheritance in a cross
between wild and cultivated common beans (Phaseolus vulgaris L.). Genetica 49,
3136.
Myles, S., Boyko, A.R., Owens, C.L., et al., 2011. Genetic structure and
domestication history of the grape. Proceedings of the National Academy of
Sciences 108, 35303535.
Olsen, K.M., Caicedo, A.L., Polato, N., et al., 2006. Selection under domestication:
Evidence for a sweep in the rice Waxy genomic region. Genetics 173,
975983.
Olsen, K.M., Wendel, J.F., 2013. A bountiful harvest: Genomic insights into crop
domestication phenotypes. Annual Review of Plant Biology 64, 4770.
Papa, R., Acosta, J., Delgado-Salinas, A., Gepts, P., 2005. A genome-wide analysis
of differentiation between wild and domesticated Phaseolus vulgaris from
Mesoamerica. Theoretical and Applied Genetics 111, 11471158.
Papa, R., Bellucci, E., Rossi, M., et al., 2007. Tagging the signatures of
domestication in common bean (Phaseolus vulgaris) by means of pooled DNA
samples. Annals of Botany 100, 10391051.
Papa, R., Gepts, P., 2003. Asymmetry of gene ow and differential geographical
structure of molecular diversity in wild and domesticated common bean
(Phaseolus vulgaris L.) from Mesoamerica. Theoretical and Applied Genetics 106,
239250.
Paterson, A.H., Lin, Y.R., Li, Z.K., Schertz, K.F., 1995. Convergent domestication of
cereal crops by independent mutations at corresponding genetic loci. Science
269, 17141718.
Payr de la Cruz, E., Gepts, P., Colunga GarciaMarn, P., Zizumbo Villareal, D.,
2005. Spatial distribution of genetic diversity in wild populations of Phaseolus
vulgaris L. from Guanajuato and Michoacn, Mxico. Genetic Resources and
Crop Evolution 52, 589599.
Perfecto, I., Vandermeer, J., 2010. The agroecological matrix as alternative to the
land-sparing/agriculture intensication model. Proceedings of the National
Academy of Sciences 107, 57865791.
Peter, B.M., Huerta-Sanchez, E., Nielsen, R., 2012. Distinguishing between selective
sweeps from standing variation and from a de novo mutation. PLOS Genetics 8,
e1003011.
Pickersgill, B., 2007. Domestication of plants in the Americas: Insights from
Mendelian and molecular genetics. Annals of Botany 100, 925940.
Pinhasi, R., Fort, J., Ammerman, A.J., 2005. Tracing the origin and spread of
agriculture in Europe. PLOS Biology 3, e410.
Piperno, D., Pearsall, D., 1998. The Origin of Agriculture in the Neotropics. San
Diego: Academic Press.
Piperno, D.R., 2011. The origins of plant cultivation and domestication in the New
World Tropics: Patterns, process, and new developments. Current Anthropology
52, S453S470.
Piperno, D.R., Dillehay, T.D., 2008. Starch grains on human teeth reveal early broad
crop diet in northern Peru. Proceedings of the National Academy of Sciences
105, 1962219627.
485
Piperno, D.R., Ranere, A.J., Holst, I., Iriarte, J., Dickau, R., 2009. Starch grain and
phytolith evidence for early ninth millennium B.P. maize from the Central Balsas
River Valley, Mexico. Proceedings of the National Academy of Sciences 106,
50195024.
Price, T.D., Bar-Yosef, O., 2010. Traces of inequality at the origins of agriculture in
the Ancient Near East. In: Price, T.D., Feinman, G.M. (Eds.), Pathways to Power.
New York, NY: Springer, pp. 147168.
Price, T.D., Bar-Yosef, O., 2011. The origins of agriculture: New data, new ideas: An
introduction to supplement 4. Current Anthropology 52, S163S174.
Pujol, B., David, P., McKey, D., 2005. Microevolution in agricultural environments:
How a traditional Amerindian farming practice favours heterozygosity in cassava
(Manihot esculenta Crantz, Euphorbiaceae). Ecology Letters 8, 138147.
Ramsay, L., Comadran, J., Druka, A., et al., 2011. INTERMEDIUM-C, a modier of
lateral spikelet fertility in barley, is an ortholog of the maize domestication gene
TEOSINTE BRANCHED 1. Nature Genetics 43, 169172.
Repinski, S.L., Kwak, M., Gepts, P., 2012. The common bean growth habit gene
PvTFL1y is a functional homolog of Arabidopsis TFL1. Theoretical and Applied
Genetics 124, 15391547.
Richerson, P., Boyd, R., Bettinger, R., 2001. Was agriculture impossible during the
Pleistocene but mandatory during the Holocene? American Antiquity 66,
387411.
Riehl, S., Zeidi, M., Conard, N.J., 2013. Emergence of agriculture in the foothills of
the Zagros Mountains of Iran. Science 341, 6567.
Rossi, M., Bitocchi, E., Bellucci, E., et al., 2009. Linkage disequilibrium and
population structure in wild and domesticated populations of Phaseolus vulgaris
L. Evolutionary Applications 2, 504522.
Ross-Ibarra, J., Morrell, P.L., Gaut, B.S., 2007. Plant domestication, a unique
opportunity to identify the genetic basis of adaptation. Proceedings of the
National Academy of Sciences 104, 86418648.
Roullier, C., Benoit, L., McKey, D.B., Lebot, V., 2013. Historical collections reveal
patterns of diffusion of sweet potato in Oceania obscured by modern plant
movements and recombination. Proceedings of the National Academy of Sciences
110, 22052210.
Sage, R.F., 1995. Was low atmospheric CO2 during the Pleistocene a limiting factor
for the origin of agriculture? Global Change Biology 1, 93106.
Sadou, A.A., Mariac, C., Luong, V., et al., 2009. Association studies identify natural
variation at PHYC linked to owering time and morphological variation in pearl
millet. Genetics 182, 899910.
Serrano-Serrano, M.L., Andueza-Noh, R.H., Martnez-Castillo, J., Debouck, D.G.,
Chacn, S.M.I., 2012. Evolution and domestication of lima bean in Mexico:
Evidence from ribosomal DNA. Crop Science 52, 16981712.
Smartt, J., 1990. Grain Legumes: Evolution and Genetic Resources. Cambridge:
Cambridge University Press.
Smith, B.D., 1989. Origins of agriculture in eastern North America. Science 246,
15661571.
Smith, B.D., 1997. The initial domestication of Cucurbita pepo in the Americas
10 000 years ago. Science 276, 932934.
Smith, M., Castillo, F., Gmez, F., 2001. Participatory plant breeding with maize in
Mexico and Honduras. Euphytica 122, 551563.
Soleri, D., Cleveland, D., Smith, S.E., et al., 2002. Understanding farmers knowledge
as the basis for collaboration with plant breeders: Methodological development and
examples from ongoing research in Mexico, Syria, Cuba and Nepal. In: Soleri, D.,
Cleveland, D. (Eds.), Farmers, Scientists and Plant Breeding: Integrating Knowledge
and Practice. Wallingford, Oxon: CABI, pp. 1960.
Stout, D., 2011. Stone toolmaking and the evolution of human culture and cognition.
Philosophical Transactions of the Royal Society B: Biological Sciences 366,
10501059.
Studer, A., Zhao, Q., Ross-Ibarra, J., Doebley, J., 2011. Identication of a functional
transposon insertion in the maize domestication gene tb1. Nature Genetics 43,
11601163.
Tanno, K.-i., Willcox, G., 2006. How fast was wild wheat domesticated? Science
311, 1886.
Thornton, P.K., Jones, P.G., Alagarswamy, G., Andresen, J., 2009. Spatial variation
of crop yield response to climate change in East Africa. Global Environmental
Change 19, 5465.
Tracy, W.W., 1907. American Varieties of Garden Beans. Washington, DC: US
Department of Agriculture.
Twomey, T., 2013. The cognitive implications of controlled re use by early
humans. Cambridge Archeological Journal 23, 113128.
Tzarfati, R., Saranga, Y., Barak, V., et al., 2013. Threshing efciency as an incentive
for rapid domestication of emmer wheat. Annals of Botany 112, 829837.
Vanderborght, T., 1979. Le dosage de lacide cyanhydrique chez Phaseolus lunatus
L. Annales de Gembloux 85, 2941.
486
Domestication of Plants
Vigouroux, Y., Mariac, C., De Mita, S., et al., 2011. Selection for earlier owering
crop associated with climatic variations in the Sahel. PLOS ONE 6.
Wang, C., Chen, J., Zhi, H., et al., 2010. Population genetics of foxtail millet and its
wild ancestor. BMC Genetics 11, 90.
Wang, R.-L., Stec, A., Hey, J., Lukens, L., Doebley, J., 1999. The limits of selection
during maize domestication. Nature 398, 236239.
Wendel, J.F., Brubaker, C., Alvarez, I., Cronn, R., Stewart, J.M., 2009. Evolution and
natural history of the cotton genus. In: Paterson, A.H. (Ed.), Genetics and
Genomics of Cotton. New York, NY: Springer, pp. 322.
Willcox, G., 2013. The roots of cultivation in Southwestern Asia. Science 341,
3940.
Willcox, G., Fornite, S., Herveux, L., 2008. Early Holocene cultivation before
domestication in northern Syria. Vegetation History and Archaeobotany 17,
313325.
Worthington, M., Soleri, D., Aragn-Cuevas, F., Gepts, P., 2012. Genetic
composition and spatial distribution of farmer-managed bean plantings: An
example from a village in Oaxaca, Mexico. Crop Science 52, 17211735.
Wright, S.I., Bi, I.V., Schroeder, S.G., et al., 2005. The effects of articial selection
of the maize genome. Science 308, 13101314.
Zhu, Q.H., Zheng, X.M., Luo, J.C., Gaut, B.S., Ge, S., 2007. Multilocus
analysis of nucleotide variation of Oryza sativa and its wild relatives: Severe
bottleneck during domestication of rice. Molecular Biology and Evolution 24,
875888.
Zizumbo-Villareal, D., Colunga GarcaMarn, P., 2010. Origin of agriculture and plant
domestication in West Mesoamerica. Genetic Resources and Crop Evolution 57,
813825.
Zizumbo-Villarreal, D., Colunga-GarcaMarn, P., Payr de la Cruz, E., DelgadoValerio, P., Gepts, P., 2005. Population structure and evolutionary dynamics of
wildweedydomesticated complexes of common bean in a Mesoamerican
region. Crop Science 35, 10731083.
Zizumbo-Villarreal, D., Flores-Silva, A., Colunga-Garca Marn, P., 2012. The archaic
diet in Mesoamerica: Incentive for milpa development and species domestication.
Economic Botany 66, 328343.
Relevant Websites
http://faostat.fao.org/site/377/default.aspx#ancor
FAO, Land use database.
http://www.fao.org/publications/so/en/
FAO, The State of Food Insecurity.
http://esa.un.org/unpd/wpp/index.htm
United Nations, Department of Economic and Social Affairs.
http://www.census.gov/main/www/popclock.html
World Population Clock, US Census Bureau.
Glossary
Dust Fine particulate matter, usually with an aerodynamic
diameter of 10 m.
Emission factor Amount of particulate matter emitted per
unit of a specic activity.
doi:10.1016/B978-0-444-52512-3.00089-9
487
488
Environmental Regulations
Many nations around the world have adopted air-quality
standards to protect the health and welfare of its citizens
against the adverse effects of air pollution. The World Health
Organization, which has representation from 194 nations, has
adopted a constitution that set guidelines on air pollutants
including atmospheric dust. The guidelines established by the
Organization recommend the respective daily PM2.5 and
PM10 concentrations not exceed 25 and 50 g m3 and the
respective annual PM2.5 and PM10 concentrations not exceed
10 and 20 g m3 (World Health Organization, 2005).
There is no clear and unequivocal evidence that associates
adverse health effects of people to exposure to specic concentrations of particulate matter in the atmosphere. This lack of
evidence is, in part, due to the variability among people in their
response to exposure to particulate matter. As a result, nations
have adopted guidelines or air-quality standards on the basis of
availability of resources and risk assessment. Air-quality
standards adopted by individual nations may, therefore, be
more relaxed or more stringent than World Health Organization guidelines. The European Union, for example, has adopted a daily PM10 Air Quality Standard of 50 g m3 that
should not be exceeded more than 35 days per year (European
Commission, 2011). The European Union has not set a daily
air-quality standard for PM2.5, but has adopted an annual
PM2.5 and PM10 Air Quality Standard of, respectively, 25 and
40 g m3. Similarly, Australia and New Zealand have adopted
a daily PM10 Standard of 50 g m3, that is, respectively, not to
be exceeded more than 5 and 1 day per year. The United States
has adopted a daily PM2.5 Air Quality Standard of 35 g m3
that should not exceed the 98th percentile averaged over
3 years and a daily PM10 Air Quality Standard of 150 g m3
that should not be exceeded more than 1 day per year averaged
over 3 years. Although annual concentrations of PM10 are not
regulated, the United States has adopted an annual PM2.5 Air
Quality Standard of 15 g m3. Chile, Costa Rica, and Mexico
have adopted a daily PM10 Air Quality Standard similar to the
United States (not to exceed 150 g m3).
New air-quality standards for particulate matter were established by China in 2012. Before this time, no air quality
standard had been established for PM2.5. The new air-quality
standards, which are to be implemented by residential, industrial, and rural areas across China by 2016, include a respective daily PM2.5 and PM10 concentration not to exceed
75 and 150 g m3 and a respective annual PM2.5 and PM10
concentration not to exceed 35 and 70 g m3.
Many communities across the world fail or have failed to
comply with air-quality standards for particulate matter.
489
490
Agricultural Facilities
Agricultural facilities, or primarily those enclosures that conne livestock and store or process raw materials into feed,
ber, food, and fuel, can contribute to the dust load in the
atmosphere. These facilities generate dust from grinding,
shearing, and pulverizing raw products; dander, hair, or feather shedding from animals; or vegetative particles from crop
processing, storage, and transfer. Dust emitted from these facilities can be controlled through management practices that
involve ltration, design, and husbandry.
The primary risks associated with dust generated by agricultural facilities include explosions, respiratory impairment of
humans or animals, nuisance (including associated odors) to
neighbors, and reduced visibility (together with its associated
trafc hazards). Explosions require conned spaces, threshold
concentrations of entrained, ammable dusts, and an ignition
source. Therefore, explosions are of concern in grain elevators,
feed mills, and similar structures and facilities. Respiratory
impairment of livestock and poultry in conned facilities
may result in economically signicant reductions in productivity or increases in maintenance costs. Exposure to dust in
these facilities has more wide-ranging effects on humans, from
reduced occupational productivity to impaired health. Agricultural dust as a nuisance can cause interferences in the use or
enjoyment of property by neighbors whereas reduced visibilities caused by dust can be a safety hazard and detract from
the enjoyment of particularly scenic areas.
Our focus will be on livestock facilities and grain storage
and processing facilities that are major sources of agricultural
dust.
Livestock facilities
The worldwide production of animal protein and its coproducts involve a nearly innite spectrum of management systems. At one extreme, animals are free to roam across
expansive and largely nonconned areas. For example, cattle,
sheep, and goats may be free to move within a rangeland or
pasture, whereas swine and poultry may be free to roam an
entire building and adjacent outdoor areas unconstrained by
individual cages or pens. In these nonconned facilities, animal excreta may be reincorporated into the landscape by
natural processes or may be collected and stored for fuel or
fertilizer. Dust generated from these nonconned or open-lot
facilities may originate from both animal activity as well as
natural processes (erosion of the native landscape).
At the other extreme, animals live in conned or concentrated facilities. Animals in these facilities are stocked more
densely in space and, in the case of poultry or veal calves,
raised in cages or small hutches. Conned beef operations may
be either sheltered (under roof) or nonsheltered (open lot
without roof) feedyards. Feedyards may have paved or earthen
surfaces and be stocked at densities such that no vegetation
can be maintained on the surface. Dairy operations may use
open-lot facilities similar to beef feedyards, full connement
facilities like poultry buildings, or some intermediate form
such as a free-stall barn with both sheltered and nonsheltered
areas accessible to the herd. Swine are generally conned
within roofed facilities, with animals being segregated according to developmental stage. In conned facilities, animal
generate dust particles and entrain them in the air. This dust,
known as fugitive dust or dust emitted from a diffuse or
nonpoint source, consists primarily of dried manure particles
but will also include soil and waste feed particles, animal
dander, exhaust from light vehicles and heavy machinery, dust
from unpaved roads, and hair.
Fugitive dust emitted from a feedyard surface tends to be
dominated by relatively coarse particles. The median aerodynamic diameter of fugitive dust from feedyards is in the
range of 1525 m. Sweeten et al. (1988) reported that the
ratio of PM10 to total suspended particulate (TSP) in fugitive
feedyard dust, as measured by high volume samplers, is in the
range of 0.190.40. Less is known about the relative abundance of ne particles (PM2.5) in feedyard dust, but recent
measurements suggest that the PM2.5/TSP ratio is on the order
of 0.05. Rainfall events reduce coarse-particle emissions to a
greater extent than ne-particle emissions such that both the
PM10/TSP and PM2.5/TSP ratios increase temporarily following precipitation but return to original levels within days
thereafter.
Fugitive dust emissions from cattle feedyards are usually
expressed as emission uxes (mass per unit of pen area per
unit time) or emission factors (mass per animal unit per unit
time). These quantities are difcult to measure directly and are
usually estimated by measuring dust concentrations both upwind and downwind of the source area. The measured dust
concentrations are then input to a dispersion model to infer
the emission ux that would have been required to generate
the difference in measured concentrations. This indirect approach yields estimates of emission uxes and emission factors
that vary over an order of magnitude as shown in Table 1. The
high uncertainty in values in Table 1 may be expected given
the differences in climate, feedyard management practices,
feed composition, aerosol monitor performance, and dispersion-modeling algorithms across all studies.
Concentrations of fugitive dust in the air downwind of beef
feedyards vary diurnally and seasonally depending on emission ux, topography, atmospheric stability, particle-size distribution, and the distance downwind from the source.
Because these emissions occur at ground level, increasing atmospheric stability associated with nighttime, dense daytime
cloud cover, or atmospheric inversions tends to favor higher
ground-level concentrations. Even a short-term inversion may
Table 1
491
Published emission factors and/or uxes of fugitive particulate matter from open-lot beef cattle feedyards
Citation
Study location
California (USA)
Texas (USA)
California (USA)
Texas (USA)
Texas (USA)
Australia
Kansas (USA)
PM2.5
PM10
PM2.5
PM10
TSP
6
0.60.8
1.56
1.5
0.30.5
35
23
29
34
831
8
23
1325
1116
114
1115
33122
31
710
5198
4464
14
1.41.8
415
4
0.81.2
612
56
70
79
2075
19
46
3160
2730
280
2836
80300
76
1624
124240
108120
Emission uxes in this table are computed from the published emission factors on the basis of a nominal animal spacing of 14 m2 per head. PM2.5 and PM10 are assumed
to be 5% and 25% of TSP, respectively.
b
When primary data sources for these columns were provided on an animal unit basis, we have converted them to a per-head basis by assuming a nominal mean live weight
of 454 kg per head.
a
492
Day 1
Day 2
3:00
6:00
12
Day 3
Day 4
10
C/C24 ratio
0:00
21:00
18:00
15:00
12:00
9:00
0:00
493
12
Day 1
Day 2
10
C/C24 ratio
0:00
21:00
18:00
15:00
12:00
9:00
6:00
3:00
0:00
Table 2
Published or adopted emission factors and/or uxes of fugitive particulate matter from various dairy-housing systems
Citation
USDA (2000)
Goodrich et al. (2002, 2003)
NAEI (2010)
Countess Environmental (2006)c
Conguration/study location
Open-lot
Free-stall, Texas
Full connement, UK
Synthesis of data
PM2.5
PM10
TSP
PM2.5
PM10
TSP
0.2
0.10.4
0.02
0.1
1.1
0.61.9
0.1
0.8
4.3
2.27
0.4
1.7
0.8
0.41.4
0.1
0.3
4
27
0.4
3
16
827
1.6
6.5
Emission uxes in this table were computed from published emission factors on the basis of a nominal animal spacing of 37.2 m2 per head. PM2.5 and PM10 are assumed
to be 5% and 25% of TSP, respectively, except where noted.
b
When primary data sources for these columns were provided on an animal unit basis, we have converted to a per-head basis on the assumption of standard Holstein cows
having a nominal live weight of 636 kg per head.
c
PM2.5 and PM10 emission factors were determined on the basis of the California Air Resources Board guidance that assumes PM10 and PM2.5 are 48% and 5.3% of TSP,
respectively.
a
Most of the sheep and goats raised around the world are
pastured, with sheep preferring grasslands and goats being
raised in more woody or brushy rangelands. Animals raised for
milk may be conned near the milking parlor during the
winter months. Sheep and goats raised for meat or ber typically live on pasture or range, but meat animals may be nished on grain-based diets to achieve desirable meat qualities.
Nonvegetated sheep and goat feedlots are common in the
United States and Australia and have many similarities to
cattle feedyards and, to a lesser extent, open-lot dairies. As with
the beef and open-lot dairy operations, dust emissions and
downwind concentrations from sheep and goat feedlots are
driven by regional climate, short-term weather phenomena,
feeding and pen-surface management, and patterns of
animal activity. However, researchers have not examined
emission rates of fugitive dust from sheep and goat feedlots.
Fully conned (i.e., in buildings or under roof) sheep and
goat production does have a substantial presence in Europe,
and limited research there has provided some estimates of
494
other forages. Therefore, pork, poultry meat, and eggs are produced predominantly in a wide range of connement systems.
Swine and poultry facilities may be fully or quasi-conned,
roofed or open-lot, actively or passively ventilated, and on
earthen or paved surfaces. Quasi-conned facilities allow animals to move liberally around a relatively large and partialoutdoor environment, but are fed in specied locations.
Examples of quasi-conned facilities include free-range areas
for poultry and hoop barns for swine. By contrast, fully conned facilities are essentially designed to optimize the animals'
stocking density and to control their environment for economic
productivity. Although there is some trend toward quasi-conned facilities for the sake of animal-welfare considerations, the
majority of swine, poultry meat, and eggs is produced under
roof with controlled or semicontrolled indoor environments.
As a result, most of the dust emitted from swine or poultry
houses originates as an indoor air pollutant that poses health
and productivity risks to both the animals and the workers.
Where natural wind currents are insufcient to maintain
acceptable indoor air quality, forced ventilation, and attentive
dust-management practices in swine (Pedersen et al., 2000) and
poultry houses are essential. Among all of the world's major
livestock-production systems, swine and poultry houses have
been the most extensively studied with respect to dust concentrations, characteristics, and emissions.
Swine
China accounts for nearly one-half, whereas the European
Union accounts for 20% and the United States and Brazil
together account for 10% of the world's swine production
(USDA, 2012). Swine production generally involves the use of
conned facilities with houses having paved or earthen oors,
natural or articial lighting, and passive or forced ventilation.
Moreover, different growth stages of the animals may be raised
in different housing types to ensure that animals in the growth
stages most vulnerable to health impairment or productivity
loss (sows, baby pigs, and breeding boars) are subjected to the
least environmental stress. As a result, the sources, mechanisms, and characteristics of dust produced in swine houses
may be meaningfully stratied by animal growth stage. For
example, one recent study found that dust from a growingnishing house, in which slaughter pigs were fed on a concrete, partially slatted oor, was composed primarily of feed,
feces, and skin particles. In contrast, dust was largely composed of straw fragments when nishing houses used straw for
bedding material (Aarnink et al., 2004). Reecting the diversity
in swine-production systems, Haeussermann et al. (2008) developed a mathematical model to predict PM10 emissions
from swine facilities that accounted for variations in stocking
rate, animal liveweight, animal growth stage, and characteristics of the housing system.
The rate at which dust is emitted from swine houses is
governed by the indoor dust concentration and the ventilation
rate, both of which vary strongly with time. Estimating emissions from houses with forced-air ventilation systems involves
continuously measuring the ow rate of air through the exhaust fans and synchronized monitoring of indoor dust
concentrations at the fan intake (Hinz and Linke, 1998a).
Emissions from passively ventilated houses are more difcult
to measure and are characterized by greater uncertainty, as
Cotton gins
Cotton is a natural ber derived from the fruit, or boll, of the
woody plant. Cotton requires a long growing season with
abundant sunshine; thus, it is grown throughout the desert,
temperate, and tropical climates of the world. Most of the
cotton produced worldwide comes from Asia (i.e., China,
India, Pakistan), Brazil, Australia, Turkey, and the United
States. In the United States, major cotton-growing states include California, Georgia, Mississippi, and Texas. Together,
China and India are responsible for more than half of the
world's cotton production.
The mature cotton boll consists of three main parts, namely
the seed, lint, and burr. The seed is high in protein and oil and
is embedded within and attached to the lint; the lint consists
of bers used to manufacture fabrics. Modern cotton harvesting is highly automated and is accomplished with either a
cotton picker or cotton stripper. Cotton pickers are designed to
mimic the selective action of manual harvesting and may pass
through a eld more than once. Cotton strippers move more
quickly through the eld and strip nearly all of the bolls from
the plant leaving behind the main stalk and larger stems. The
raw products obtained from these two harvesters differ primarily in terms of the relative amounts of mature versus immature lint and the amount of nonlint material in the
harvested bulk.
Cotton ginning is essentially a two-stage mechanical process of removing gin trash (stems, burrs, soil, and other debris)
from cotton bolls and separating the cotton bers from the
seed. The modern cotton gin originated in the late eighteenth
century but has become a highly sophisticated, multistage,
high-throughput operation that yields compressed lint bales
weighing 200225 kg. Cotton gins now consist of many specialized, mechanical processes (Figure 6). The conveyors in a
cotton gin are pneumatic, using air ow at high speed to move
the materials from point to point. Along the way, debris, lint,
and seeds must be removed from the various air streams with
the conveying air ultimately exhausted to the outside.
Dust emissions from cotton gins originate from the exhaust
of conveying systems within the gin enclosure. The dust consists of soil particles, insect fragments, and fragments of lint,
leaves, stems, and other plant parts. Each of the specialized,
mechanical processes within a gin produces a characteristic
type of dust. Moreover, the manner in which the cotton is
harvest (i.e., picker vs. stripper) strongly inuences the load on
each stage of the ginning process. Stripper-harvested cotton
may generate 67 times as much trash during the ginning
process as picker-harvested cotton (USEPA, 1995).
As with most agricultural dusts, cotton gin dust is composed of both organic (plant-derived) and mineral (soil derived) particles. Most of the dust generated by cotton ginning,
therefore, is relatively coarse with aerodynamic diameters exceeding 10 mm. The ratio of PM10 to TSP varies slightly between processes, but is typically between 0.25 and 0.5. In
addition to the parent materials, dust associated with cottongin exhaust may also contain traces of chemical residues, including pesticides and harvest aids (defoliants).
As implied by Figure 6, estimates of the total dust emissions from cotton gins are assembled from individual process
emissions. As shown in Table 3, emissions are typically calculated from an emission factor for each process (mass of
495
496
Cotton
cleaning
system
Unloading
system
Emissions
(3-02-004-01)
Emissions
(3-02-004-20)
Stick
machine
Emissions
(3-02-004-21)
(3-02-004-22)
Overflow
system
Distributor
Emissions
(3-02-004-25)
- Optional process
- Trash
Extractor/
feeder
Lint cotton
system
Cotton
seed
storage
Gin stands
No. 1 lint
cleaner*
- Exhaust stream
- Product stream
- Low pressure side
components
Emissions
(3-02-004-07)
No. 2 lint
cleaner*
Mote fan
Mote
cleaner
Emissions
(3-02-004-35)
Mote trash
fan
Emissions
(3-02-004-36)
Baled motes
Battery
condenser and
baling system*
Emissions
(3-02-004-08)
Master
trash fan
Bale storage
Emissions
(3-02-004-03)
Solid waste
Cyclone
robber
system
Emissions
(3-02-004-30)
Figure 6 Schematic of a modern cotton gin showing the numerous discrete processes that generate dust emissions (USEPA, 1995). Numbers in
parentheses are Source Classication Codes used by the USEPA to categorize operations that emit particulate matter.
Table 3
497
Emission factors for modern cotton gins with high-efciency cyclone controls on the exhaust streams (USEPA, 1995)
Source
PM10/TSP ratio
Unloading fan
#1 Dryer/cleaner
#2 Dryer/cleaner
#3 Dryer/cleaner
Overow fan
0.132
0.164
0.109
0.043
0.032
0.055
0.005
0.042
0.015
0.012
0.41
0.03
0.39
0.35
0.37
Lint cleaners:
with high-efciency cyclones
with screen drums or cages
Cyclone robber
Mote fan
Mote trash fan
0.264
0.500
0.082
0.127
0.035
0.109
0.024
0.059
0.010
0.41
0.29
0.46
0.27
Battery condenser:
with high-efciency cyclones
with screen drums or cages
Master trash fan
Grand total
0.018
0.077
0.245
1.828
0.006
0.034
0.370
0.36
0.14
0.30
type of grain has its own intrinsic dustiness, which may vary
with moisture content, harvest method, or other management factors (USEPA, 2003). In principle, then, there could
be a unique emission factor for each permutation of grain
type, grain condition, harvest method, and elevator or mill
process.
Agricultural Lands
Agricultural lands, primarily in the arid and semiarid regions
of the world, contribute to the dust load in the atmosphere. The lack of precipitation in these regions impairs crop
production and generally results in dry and poorly structured
soils, both of which affect dust emissions from agricultural lands. Dust is emitted into the atmosphere from
agricultural lands as a result of natural events and farming
operations. Although natural events cannot be controlled
or regulated, management practices or farming operations
imposed on these lands can dramatically inuence dust
emissions.
Natural events
High winds, volcanic eruptions, and wildres are natural
events that can affect atmospheric PM10 concentrations. Highwind events are of particular relevance to agriculture. Dust
emitted into the atmosphere as a result of high winds eroding
agricultural lands (Figure 8) constitutes 10% of the atmospheric dust load worldwide (Tegen et al., 2004). Windblown
dust has contributed to exceedance of national PM10 airquality standards in China, Europe, and the United States (Liu
et al., 2011; Escudero et al., 2007; Sharratt and Lauer, 2006).
Long-range transport of PM10 from eroding agricultural land
has also contributed to exceedance of PM10 air-quality
standards. For example, transport from agricultural lands in
the Ukraine have resulted in exceedance of the European
Union air quality standard for PM10 (daily concentration not
to exceed 50 g m3) in Slovakia, the Czech Republic, Poland,
498
Truck/rail
receiving
Barge/ship
receiving
Conveyor
Conveyor
Optional
Boot
Intermediate
storage bin
(vent)
Tunnel belt
Leg
Receiving
leg
Annex storage
bin (vent)
Grain
dryer
Conveyor
Headhouse
Distributor
Grain
cleaner
Gallery
belt
Interstice
bin
Garner
scale
Tripper
Storage bin
(vent)
Conveyor
Truck/rail
shipping
Barge/ship
shipping
Figure 7 Schematic of emissions sources in a grain elevator (USEPA, 2003). VOC, volatile organic compound.
Table 4
Example emission factors for processes within grain elevators and feed mills in the United States (USEPA, 2003)
Process
Feed mill:
Grain receiving
Hammer mill with cyclone
Feed shipping
Grain elevator:
Grain cleaning with cyclone
Grain receiving, hopper truck
Grain handling
PM10/TSP ratio
8.5
33.5
1.65
1.25
0.15
0.4
0.24
37.5
17.5
12.5
9.5
3.9
3.15
0.25
0.22
0.25
Two studies have estimated PM10 emissions from agricultural lands during high winds. Saxton et al. (2000) estimated
PM10 vertical uxes as high as 300 000 g m2 s1 from agricultural elds during a design wind storm in some portions of
the Columbia Plateau. These estimates, based on an integrated
meteorological/chemical transport/PM10 emissions model,
were not conrmed in the eld. Xuan and Sokolik (2002) estimated an annual PM10 loss across gridded locations in
northern China using an empirical model which estimates
PM10 loss from surface characteristics and climate. Their analyses suggest that annual PM10 loss can approach 10 kg ha1 in
agricultural regions.
Geologic material is generally composed of coarser particle
matter and, thus, PM2.5 constitutes a small percentage of
PM10 emitted from agricultural lands. For example, PM2.5
comprised from 4% to 7% of PM10 that was observed
downwind of eroding agricultural lands in the Columbia
Plateau region of the Inland Pacic Northwest (Sharratt and
Lauer, 2006). Gillette and Walker (1977) measured the size
distribution of particulate matter 1.5 m above eroding agricultural soils in Texas and found that PM2.5 comprised from
approximately 1% to 4% of PM10.
Best management practices to reduce dust emissions
from agricultural soils during high-wind events are similar
to those required to control wind erosion. These practices
include the use of wind barriers, ridge tillage, tillage operations that enhance surface roughness or cover with crop
499
Farming operations
Tillage, harvest, seeding, fertilizing, and spraying are routine
farming operations that generate dust. Dust generated by
agricultural operations is typically characterized by particles
with diameters larger than 2.5 m (Capareda et al., 2004)
and, therefore, does not solely contribute to exceedance of
the PM2.5 air-quality standard. Dust emitted into the atmosphere as a result of farming operations has contributed to
the exceedance of the PM10 air-quality standards in the
United States, most notably in California (Chow et al., 1992;
Dolislager and Motallebi, 1999). Dust generated by farming
operations is the second largest source, with road dust being
the largest source, in the San Joaquin Valley of California
(Cassel et al., 2003). Air stagnation in the Imperial Valley and
San Joaquin Valley during the autumn, winter, and spring
trap ne particles in the atmosphere that are emitted during
tillage or harvest operations (Chow and Watson, 2001).
In northern Europe, high atmospheric dust concentrations in
the spring have been linked to tillage activities (Goossens,
2004).
Tillage and harvest operations typically generate a higher
proportion of coarse particulate matter (particulates with a
diameter 2.510 m) as compared with PM2.5 (Matsumura
et al., 2003; Kasumba et al., 2011). Particulates emitted during
tillage or land preparation operations are affected by the
type of implement, speed of implement, surface characteristics
(e.g., roughness and residue cover), soil properties (e.g., type
and moisture), and atmospheric conditions. Particulates
emitted during harvest, however, tend to be unique to each
crop. Some crops require only one harvest operation (e.g.,
direct combine), whereas the harvest of other crops, such as
nut trees, require multiple operations. Each operation can
contribute to the particulate load in the atmosphere. Particulates can be emitted during the cutting, swathing, raking, or
combining operations of eld crops or the shaking, sweeping,
and pickup operations of tree crops. For example, the harvest
of almonds in California involves shaking the tree to allow the
Table 5
PM10 concentration, vertical ux and loss measured within eroding agricultural elds during a high-wind event. PM10 concentration
was measured at various heights above an eroding surface
Citation
Location
Height (m)
Gillette (1974)
Zobeck and VanPelt (2006)
Kjelgaard et al. (2004)
Sharratt et al. (2007)
Stetler and Saxton (1996)
Texas
Texas
Washington
Washington
Washington
2
3
5
1.5
2200
6500
8535
1255
10 000
0.48
258
255
260
212
15
80
12
60
9
40
6
20
3
500
0
0
12
18
24
Time (hour)
Figure 9 Five-minute averages of wind speed at 2 m (black line), Tapered Element Oscillating Microbalance PM10 concentration at 1 (blue line)
and 2 m (light blue line), and vertical PM10 ux (red line) above an eroding agricultural eld during a September 2009 high-wind event in eastern
Washington.
Biomass burning
Biomass burning is used throughout the world to control
diseases and pests in crops, remove crop residue that otherwise
interferes with harvest or seeding operations, and as a fuel
source. Biomass burning, however, can contribute to the dust
load in the atmosphere. For example, burning wheat and corn
residue is a major contributor to high PM2.5 concentrations in
Beijing, China (Li et al., 2007; Song et al., 2006), whereas
burning sugarcane is the main source of PM2.5 in some
Brazilian cities (Lara et al., 2005). Burning biomass generates a
higher proportion of PM2.5 as compared with coarser particulate matter. In fact, 93% and 98% of the PM10 liberated
from burning respectively wheat straw and corn stover is
PM2.5 (Li et al., 2007). In addition, biomass burning can release toxic compounds such as polycyclic aromatic hydrocarbons and phenols. PM2.5 and PM10 emission factors for
burning agricultural residues are provided in Table 7. The
range in emission factors for any crop is likely due to differences in atmospheric conditions (e.g., relative humidity),
conguration of residue, or moisture content of residue during
the burn.
A greater awareness of biomass burning being a source of
atmospheric PM2.5 has prompted government organizations
around the world to adopt policies that regulate burning of
crop residue. In Washington, for example, agricultural burning has been reduced by half over the past decade and is
currently allowed on certain days by those possessing a permit.
Violation of this law has resulted in nes that exceed
US$20 000. Other methods of handling crop residue are being
advocated rather than burning; these include removing residue
from the soil surface after harvest, incorporating residue into
the soil after harvest, or using no-till seeding technologies and
pesticides.
501
Table 6
PM2.5 and PM10 emission factors for tillage and harvest
operations of agricultural crops
Table 7
PM2.5 and PM10 emission factors applicable to burning
biomass of agricultural crops
Operation
Crop
PM2.5
PM10
g m2
Tillage
Chisel
Cultivate
Disk
Harrow
Land smoothing
Plow
Subsoil
Weeding
Harvest
Almond
Shake
0.03c
0.55d
0.010.13c
0.010.12d
Sweep
Pickup
Corn
Cotton
Oat
Potato
Rice
Sugar beet
Wheat
0.0002k
PM10
g kg1
a
0.01c
0.01c, 0.01
0.11d
PM2.5
0.13 , 0.25
0.19c
0.080.65d, 0.081.38e,
0.09f, 0.13a, 0.14c,
0.21b
0.08c
0.122.32e, 0.500.65b,
1.34d, 1.40a
0.121.05c
0.040.72d, 0.51f, 0.52a
0.09a
4.58g
0.015h, 0.042g, 0.05b,
1.65i
0.08b, 0.20h, 0.42g, 1.94i
0.19b, 1.07j, 1.22h, 3.23i,
4.12g
0.19a
0.04h, 0.05k, 0.11e, 0.38a
0.65a
0.19a
0.19a
0.19a
0.65a
Almond
Apple
Barley
Canola
Corn
Cotton
Kentucky bluegrass
Oat
Olive
Rice
Sugarcane
Walnut
Wheat
4.1a, 4.5b
4.0a
7.4a,b
8.5a
5.0c, 6.0b, 11.7d
6.2c, 8.5a
11.6c, 12.1e, 29.6f
10.9a
8.3a
2.4c, 3.2b, 13.0g
2.2i, 2.6j, 4.3c, 5.0a
4.7b
0.84.7e, 3.6k, 4.0c,
4.7g, 5.4a,b, 7.6d
4.3a, 4.8b
4.2a
7.7a,b
8.9a
6.2b, 10.7c
8.9a,
15.8c
11.4a
8.9a
3.3c, 3.5b, 3.7h
4.9c, 5.4a
5.0b
5.7a,b, 7.0c
See also: Air: Conned Animal Facilities and Air Quality Issues.
Beef Cattle. Dairy Animals. Land Use: Management for Biodiversity
and Conservation. Swine Diseases and Disorders. Tree Fruits and
Nuts
Future Perspectives
The pursuit of clean air will intensify as societies become
more urbanized and interest escalates in protecting public
health. Air-quality standards are being adopted and revised
by many nations around the world. For example, China will
fully implement new air-quality standards by 2016. In
addition, the USEPA is mandated to review and revise, if
appropriate, air-quality standards every 5 years. There is
expectation that stricter or tighter PM2.5 and PM10 airquality standards will be adopted as more evidence associates
adverse health effects with exposure to dust. Tighter or more
restrictive air-quality standards will necessitate that even
greater measures be taken or better practices be implemented
to control dust emissions. This will be a challenge for the
agricultural industry, particularly in regions where weather
affects emissions and prot margins are thin. Meeting this
References
Aarnink, A.J.A., Roest, H.I.J., Cambria-Lopez, M., et al., 2012. Emissions and
concentrations of dust and pathogens from goat houses. In: Proceedings of
the Ninth International Livestock Environment Symposium, Paper Number ILES
12-0968. St. Joseph, MI: American Society of Agricultural and Biological
Engineers.
Aarnink, A.J.A., Stockhofe-Zurwieden, N., Wagemans, M.J.M., 2004. Dust in different
housing systems for growing-nishing pigs. In: Engineering the Future,
Proceedings of the AgEng2004 Conference. Antwerpen, Belgium: Technologisch
Instituut.
Air Sciences Inc, 2003. Final Report: Cereal-grain residue open eld burning
emissions study. Project 152-02. Available at: http://www.ecy.wa.gov/programs/
air/pdfs/FinalWheat_081303.pdf (accessed 20.08.13).
Air Sciences Inc, 2004. Quantifying post-harvest emissions from bluegrass seed
production eld burning. Available at: http://www.ag.uidaho.edu/bluegrass/
FromJohn/Kentucky%20bluegrass/Emissions/BLUEGRASS%20FINAL%
20Emissions%20REPORT%204-5-04.pdf (accessed 20.08.13).
502
Air Sciences Inc, 2005. 2002 re emission inventory for the WRAP region
Phase II. Western Regional Air Partnership Project No. 178-6, Portland,
Oregon: Air Sciences, Inc.
Ashbaugh, L., Matsumura, R., Flocchini, R., 1997. Calculation of PM10 emission
rates using a simple box model and a vertical proling method. In: Emission
inventory: Planning for the future. Pittsburgh, Pennsylvania: Air and Waste
Management Association, pp. 282288.
Ashbaugh, L., Matsumura, R., James, T., Carvacho, O., Flocchini, R., 1996.
Modeling PM10 dust emissions from eld harvest operations. In: Proceedings of
the International Conference on Air Pollution from Agricultural Operations. Ames,
Iowa: Midwest Plan Service, pp. 155159.
de Azeredo Franca, D., Longo, K.M., Neto, T.G.S., et al., 2012. Pre-harvest
sugarcane burning: Determination of emission factors through laboratory
measurements. Atmosphere 3, 164180.
Birmili, W., Schepanski, K., Ansmann, A., et al., 2008. A case of extreme particlaute
matter concentrations over Central Europe caused by dust emitted over the
southern Ukraine. Atmospheric Chemistry and Physics 8, 9971016.
Bogman, P., Cornelis, W., Rolle, H., Gabriels, D., 2007. Prediction of TSP and
PM10 emissions from agricultural operations in Flanders, Belgium. In: DustConf
2007: How to improve air quality. Maastricht, The Netherlands: The Dutch
Ministry of Housing, Spatial Planning and the Environment.
Bonifacio, H.F., Maghirang, R.G., Auvermann, B.W., et al., 2012. Particulate
matter emission rates from beef cattle feedlots in Kansas reverse dispersion
modeling. Journal of the Air & Waste Management Association 62,
350361.
Busacca, A., Wagoner, L., Mehringer Jr., P., Bacon, M., 1998. Effect of human
activity on dustfall: A 1,300 year lake-core record of dust deposition on the
Columbia Plateau, Pacic Northwest, USA. In: Busacca, A.J. (Ed.), Dust
Aerosols, Loess Soils, and Global Change. Pullman, Washington, DC:
Washington State University College of Agriculture and Home Economics.
Miscellaneous Publication Number MISC0190.
California Air Resources Board, 2003. Emission inventory procedural manual Volume
III: Methods for assessing area source emissions. Sacramento, California:
California Air Resources Board.
Capareda, S.C., Wang, L., Parnell Jr., C.B., Shaw, B.W., 2004. Particle size
distribution of particulate matter emitted by agricultural operations: Impacts on
FRM PM10 and PM2.5 concentration measurements. In: Proceedings of the
2004 Beltwide Cotton Production Conferences. Cordova, Tennessee: National
Cotton Council.
Cassel, T., Trzepla-Nabaglo, K., Flocchini, R., 2003. PM10 emission factors for
harvest and tillage of row crops. In: 12th International Emissions Inventory
Conference: Emission Inventories Applying New Technologies. Washington,
DC: United States Environmental Protection Agency.
Chow, J.C., Watson, J.G., 2001. Zones of representation for PM10
measurements along the US/Mexico border. Science of the Total Environment
276, 4968.
Chow, J.C., Watson, J.G., Lowenthal, D.H., et al., 1992. PM10 source
apportionment in Californias San Joaquin Valley. Atmospheric Environment 26A,
33353354.
Countess Environmental. 2006. WRAP Fugitive Dust Handbook. Westlake Village,
California. Available at: http://www.wrapair.org/forums/dejf/fdh/ (accessed
20.08.13).
Dhammapala, R., Claiborn, C., Corkill, J., Gullett, B., 2006. Particulate emissions
from wheat and Kentucky bluegrass stubble burning in eastern Washington and
northern Idaho. Atmospheric Environment 40, 10071015.
Dolislager, I.J., Motallebi, N., 1999. Characterization of particulate matter in
California. Journal of the Air & Waste Management Association 49,
PM45PM56.
Escudero, M., Querol, X., Avila, A., Cuevas, E., 2007. Origin of the exceedances of
the European daily PM limit value in regional background areas of Spain.
Atmospheric Environment 41, 730744.
European Commission, 2011. Air quality standards. Available at: http://ec.europa.eu/
environment/air/quality/standards.htm (accessed 20.08.13).
Faulkner, W.B., Capareda, S.C., 2012. Effects of sweeping depth on particulate
matter emissions from almond harvest operations. Atmospheric Pollution
Research 3, 219225.
Fields, P.G., Wolf, M.E., Sadeghi, V., George, M., 2001. Estimating the impacts of
agricultural best management practices in the Maricopa County PM10 nonattainment area. International Emission Inventory Conference One Atmosphere,
One Inventory, Many Challenges. Washington, DC: United States Environmental
Protection Agency.
Flocchini, R., Cahill, T.A., Matsumura, R.T., Carvacho, O. Lu, Z., 1994. Study of
fugitive PM10 emissions from selected agricultural practices on selected
agricultural soils. San Joaquin Valley Unied Air Pollution Control District Grant
File #20960. Davis, California: University of California.
Flocchini, R.G., James, T.A., Ashbaugh, L.L., et al., 2001. Sources and sinks of
PM10 in the San Joaquin Valley. Davis, California: University of California
Interim report to the United States Department of Agriculture, Contract Nos. 9433825-0383 and 98-38825-6063.
Fryrear, D.W., 1986. A eld dust sampler. Journal of Soil and Water Conservation
41, 117120.
Gillette, D.A., 1974. Production of ne dust by wind erosion of soil: Effect of wind
and soil texture. Atmosphere-surface exchange of particulate and gaseous
pollutants: Proceedings of a symposium. Richland, Washington: Pacic
Northwest Laboratory.
Gillette, D.A., 1977. Fine particulate emissions due to wind erosion. Transactions of
the ASAE 20, 890897.
Gillette, D.A., Blifford Jr., I.H., Fenster, C.R., 1972. Measurements of aerosol size
distributions and vertical uxes of aerosols on land subject to wind erosion.
Journal of Applied Meteorology 11, 977986.
Gillette, D.A., Walker, T.R., 1977. Characteristics of airborne particles produced by
wind erosion of sandy soil, high plains of west Texas. Soil Science 123,
97110.
Gillis, J.P., 1985. Detection and Suppression of Fires in Bucket Elevators.
Washington, DC: National Grain and Feed Association.
Gomes, L., Rajot, J.L., Alfaro, S.C., Gaudichet, A., 2003. Validation of a dust
production model from measurements performed in semi-arid agricultural areas
of Spain and Niger. Catena 52, 257271.
Goodrich, L.B., Parnell Jr., C.B., Mukhtar, S., Lacey, R.E., Shaw, B.W., 2002.
Preliminary PM10 emission factor for free-stall dairies. In: Proceedings of the
American Society of Agricultural Engineers Annual International Meeting, Paper
Number 024214. St. Joseph, Michigan: American Society of Agricultural and
Biological Engineers. Available at: http://elibrary.asabe.org/techpapers.asp?
cond=cil2002 (accessed 20.08.13).
Goodrich, L.B., Parnell Jr., C.B., Mukhtar, S., et al., 2003. A science based
PM10 emission factor for free-stall dairies. In: Proceedings of the American
Society of Agricultural Engineers Annual International Meeting, Paper Number
034115. St. Joseph, MI: American Society of Agricultural and Biological
Engineers. Available at: http://elibrary.asabe.org/techpapers.asp?cond=cil2002
(accessed 20.08.13).
Goossens, D., 2004. Wind erosion and tillage as a dust production mechanism. In:
Goossens, D., Riksen, M. (Eds.), Wind Erosion and Dust Dynamics:
Observations, Simulations, Modeling. Wageningen, The Netherlands: ESW
Publications, pp. 713.
Goossens, D., Offer, Z., London, G., 2000. Wind tunnel and eld calibration of ve
aeolian sand traps. Geomorphology 35, 233252.
Goossens, D., Offer, Z.Y., 2000. Wind tunnel and eld calibration of six aeolian dust
samplers. Atmospheric Environment 34, 10431057.
Haeussermann, A., Costa, A., Aerts, J.M., et al., 2008. Development of a dynamic
model to predict PM10 emissions from swine houses. Journal of Environmental
Quality 37, 557564.
Hall, D.J., Upton, S.L., Marsland, G.W., 1994. Designs for a deposition gauge and a
ux gauge for monitoring ambient dust. Atmospheric Environment 28,
29632979.
Hays, M.D., Fine, P.M., Geron, C.D., Kleeman, M.J., Gullett, B.K., 2005. Open
burning of agricultural biomass: Physical and chemical properties of particlephase emissions. Atmospheric Environment 39, 67476764.
Hinz, I.T., Funk, R., 2007. Particle emissions of soils induced by agricultural eld
operations. In: DustConf2007: How to improve air quality. Maastricht, The
Netherlands: The Dutch Ministry of Housing, Spatial Planning and the
Environment.
Hinz, T., Linke, S., 1998a. A comprehensive experimental study of aerial pollutants
in and emissions from livestock buildings, part 1: Methods. Journal of
Agricultural Engineering Research 70, 111118.
Hinz, T., Linke, S., 1998b. A comprehensive experimental study of aerial pollutants
in and emissions from livestock buildings, part 2: Results. Journal of Agricultural
Engineering Research 70, 119129.
Holman, B.A., James, T.A., Ashbaugh, L.L., Flocchini, R.G., 2001. Lidar-assisted
measurement of PM10 emissions from agricultural tilling in Californias San
Joaquin Valley Part II: Emission factors. Atmospheric Environment 35,
32653277.
Hughs, S.E., Armijo, C.B., Whitelock, D.P., Buser, M.D., 2008. Particulate
emission prole of a cotton gin. Applied Engineering in Agriculture 24,
145151.
Husar, R.B., Tratt, D.M., Schichtel, B.A., et al., 2001. The Asian dust events of April
1998. Journal of Geophysical Research 106, 1831718330.
Janssen, W., Tetzlaff, G., 1991. Entwicklung und eichung einer registrierenden
suspensionsfalle. Zitschrift fur Kulturtechnic und Landensentwicklung 32,
167180.
Jenkins, B.M., Turn, S.Q., Williams, R.B., et al., 1996. Atmospheric pollutant
emission factors from open burning of agricultural and forest biomass by wind
tunnel simulations. Davis, California: University of California California Air
Resources Board Project No. A932-126.
Jones, C., 2011. Preventing grain dust explosions. Bulletin BAE-1737.
Stillwater, OK: Oklahoma Cooperative Extension Service. Available at: http://pods.
dasnr.okstate.edu/docushare/dsweb/Get/Document-2604/BAE-1737web.pdf
(accessed 20.08.13).
Kadam, K.L., Forrest, L.H., Jacobson, W.A., 2000. Rice straw as a lignocellulosic
resource: collection, processing, transportation, and environmental aspects.
Biomass and Bioenergy 18, 369389.
Kasumba, J., Holmen, B.A., Hiscox, A., Wang, J., Miller, D., 2011. Agricultural
PM10 emissions from cotton eld disking in Las Cruces, NM. Atmospheric
Environment 45, 16681674.
Kjelgaard, J., Sharratt, B., Sundram, I., et al., 2004. PM10 emission from
agricultural soils on the Columbia Plateau: Comparison of dynamic and timeintegrated eld-scale measurements and entrainment mechanisms. Agricultural
and Forest Meteorology 125, 259277.
Lange, J., Wanjura, J., Skloss, S., Parnell Jr., C.B., 2007. Emission factors for cattle
feedlots in Texas based on particle size using ISCST3 and AERMOD. In:
Proceedings of the American Society of Agricultural and Biological Engineers.
Paper Number 07-4106. St. Joseph, Michigan: American Society of Agricultural
and Biological Engineers.
Lara, L.L., Artaxo, P., Martinelli, L.A., et al., 2005. Properties of aerosols from
sugar-cane burning emissions in southeastern Brazil. Atmospheric Environment
39, 46274637.
Li, X., Wang, S., Duan, L., et al., 2007. Particulate and trace gas emissions from
open burning of wheat straw and corn stover in China. Environmental Science
and Technology 41, 60526058.
Liu, L., Shi, P., Hu, X., et al., 2011. Natural factors inuencing blown sand hazards
in Beijing. International Journal of Disaster Risk Science 2, 2331.
Matsumura, R.T., Ashbaugh, L., James, T., Carvacho, O., Flocchini, R., 2003. Size
distribution of PM10 soil dust emissions from harvesting crops. In: Rapport, D.
J., Lasley, W.L., Rolston, D.E., Nielsen, N.O., Qualset, C.O., Damania, A.B.
(Eds.), Managing for Healthy Ecosystems. Boca Raton, FL: CRC Press,
pp. 801806.
McCarty, J.L., 2011. Remote sensing-based estimates of annual and seasonal
emissions from crop residue burning in the contiguous United States. Journal of
the Air & Waste Management Association 61, 2234.
McGinn, S.M., Flesch, T.K., Chen, D., et al., 2010. Coarse particulate matter
emissions from cattle feedlots in Australia. Journal of Environmental Quality 39,
791798.
McGowan, H.A., Marx, S.K., Soderholm, J., Denholm, J., 2010. Evidence of solar
and tropical-ocean forcing of hydroclimate cycles in southeastern Australia for
the past 6500 years. Geophysical Research Letters 37, L10705.
Moulton, G.E., 1991. Journals of the Lewis & Clark Expedition. Lincoln, Nebraska:
University of Nebraska Press vol. 7, p. 178.
NAEI, 2010. United Kingdom National Atmospheric Emissions Inventory. Available
at: http://naei.defra.gov.uk/emissions/selection.php (accessed 20.08.13).
Papanastasiou, D.K., Fidaros, D., Bartzanas, T., Kittas, C., 2011. Monitoring
particulate matter levels and climate conditions in a Greek sheep and
goat livestock building. Environmental Monitoring and Assessment 183,
285296.
Parnell Jr., C.B., Shaw, B.W., Auvermann, B.W., 1999. Agricultural air quality ne
particle project Task 1: Livestock feedlot PM emission factors and
emissions inventory estimates. Austin, Texas: Texas Natural Resource
Conservation Commission.
Pedersen, S., Nonnenmann, M., Rautiainen, R., et al., 2000. Dust in pig buildings.
Journal of Agricultural Safety and Health 6, 261274.
Peters, J.A., Blackwood, T.R., 1977. Source assessment: Beef cattle feedlots. Report
EPA-600/2-77-107. Research Triangle Park, North Carolina: United States
Environmental Protection Agency.
Saxton, K., Chandler, D., Stetler, L., et al., 2000. Wind erosion and fugitive dust
uxes on agricultural lands in the Pacic Northwest. Transactions of the ASAE
43, 623630.
Schwartz, D.A., Thorne, P.S., Yagla, S.J., et al., 1995. The role of endotoxin in grain
dust-induced lung disease. American Journal of Respiratory and Critical Care
Medicine 152, 603608.
Seedorf, J., Hartung, J., Schroder, M., et al., 1998. Concentrations and
emissions of airborne endotoxins and microorganisms in livestock
503
504
Yokelson, R.J., Christian, T.J., Karl, T.G., Guenther, A., 2008. The tropical
forest and re emissions experiment: Laboratory re measurements
and synthesis of campaign data. Atmospheric Chemistry and Physics 8,
35093527.
Zobeck, T.M., Van Pelt, R.S., 2006. Wind-induced dust generation and transport
mechanisms on a bare agricultural eld. Journal of Hazardous Materials 132,
2638.
Relevant Websites
http://Pnw-winderosion.wsu.edu
Columbia Plateau Wind Erosion Air Quality Project.
http://school.dustwatch.edu.au/site.html
Ofce of Environment and Heritage and Grifth University.
http://www.dustwatch.edu.au/
Ofce of Environment and Heritage and Grifth University.
http://www.weru.ksu.edu/
USDA Agricultural Research Service Wind Erosion Research Unit.
http://www.wrapair.org/
Western Regional Air Partnership.
ENCYCLOPEDIA OF
AGRICULTURE AND
FOOD SYSTEMS
VOLUME 3
ENCYCLOPEDIA OF
AGRICULTURE AND
FOOD SYSTEMS
EDITOR-IN-CHIEF
Academic Press
Academic Press is an imprint of Elsevier
32 Jamestown Road, London NW1 7BY, UK
225 Wyman Street, Waltham, MA 02451, USA
525 B Street, Suite 1800, San Diego, CA 92101-4495, USA
Copyright r 2014 Elsevier Inc. unless otherwise stated. All rights reserved
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic,
mechanical, photocopying, recording or otherwise without the prior written permission of the publisher
Permissions may be sought directly from Elseviers Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865
843830; fax (+44) (0) 1865 853333; email: permissions@elsevier.com. Alternatively you can submit your request online by visiting the
Elsevier web site at http://elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material
Notice
No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability,
negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein,
Because of rapid advances in the medical sciences, in particular, independent verication of diagnoses and drug dosages should be made
British Library Cataloguing in Publication Data
A catalogue record for this book is available from the British Library
Library of Congress Cataloging-in-Publication Data
A catalog record for this book is available from the Library of Congress
ISBN (print): 978-0-444-52512-3
EDITORIAL BOARD
Editor-in-Chief
Neal K Van Alfen
University of California, Davis, CA, USA
Associate Editors
Brent Clothier
Plant & Food Research
Palmerston North
New Zealand
John P Nichols
Texas A& M University
College Station, TX
USA
Daryl Lund
University of Wisconsin
Madison, WI
USA
Harris A Lewin
University of California
Davis, CA
USA
Mary Delany
University of California
Davis, CA
USA
R James Cook
Washington State University
Pullman, WA
USA
Roger RB Leakey
James Cook University
Queensland
Australia
Jeremy J Burdon
Commonwealth Scientic and Industrial
Research Organisation
Black Mountain, Canberra
Australia
Ronald L Phillips
University of Minnesota
St Paul, MN
USA
CONTRIBUTORS TO VOLUME 3
JM Alston
University of California, Davis, CA, USA
W Edwards
Iowa State University, Ames, IA, USA
VO Alvarenga
University of Campinas, Campinas, Brazil
L Ericson
Ume University, Ume, Sweden
R Appels
Murdoch University, Perth, WA, Australia
DJ Field
The University of Sydney, Sydney, NSW, Australia
CW Bamforth
University of California, Davis, CA, USA
NR Fredrickson
University of Minnesota, St. Paul, MN, USA
JL Baumert
University of Nebraska, Lincoln, NE, USA
M Gonzalez
McCormick and Company, Inc., Baltimore, MD, USA
JM Beddow
University of Minnesota, InSTePP Center, Saint Paul,
MN, USA
L Grivetti
University of California, Davis, CA, USA
JA Birchler
University of Missouri, Columbia, MO, USA
D Blandford
Pennsylvania State University, University Park, PA,
USA
RM Boom
Wageningen University, WG Wageningen, The
Netherlands
MC Bourne
Cornell University, Geneva, NY, USA
JB Braden
University of Illinois, Urbana, IL, USA
L Buck
Cornell University, Ithaca, NY, USA
JJ Burdon
Commonwealth Scientic and Industrial Research
Organisation, Canberra, ACT, Australia
RV Carvalho
Federal University of Espirito Santo, Alegre, Brazil
SR Cattle
The University of Sydney, Sydney, NSW, Australia
D Diepeveen
Government of Western Australia, Perth, WA,
Australia, and Murdoch University, Perth, WA,
Australia
L Guarino
Global Crop Diversity Trust, Bonn, Germany
T Hager
Fayetteville, AR, USA
L Hassan
Universiti Putra Malaysia, Serdang Selangor, Malaysia
KA Havas
Veterinarians Without Borders United States, Davis,
CA, USA
HM Hngaro
Federal University of Viosa, Viosa, Brazil
TM Hurley
University of Minnesota, InSTePP Center, Saint Paul,
MN, USA
CA Hutt
RdR Solutions, Aubrey, TX, USA
H Jaeger
Technische Universitaet Berlin, Berlin, Germany
AEM Janssen
Wageningen University, WG Wageningen, The
Netherlands
BM Jenkins
University of California, Davis, CA, USA
YS Jeong
Jeonbuk National University, Jeonju, Republic of Korea
JB Dodgson
Michigan State University, East Lansing, MI, USA
B Jiang
Jiangnan University, Wuxi, Jiangsu, PR China
P Duffy
Auburn University, Auburn, AL, USA
D Knorr
Technische Universitaet Berlin, Berlin, Germany
vii
viii
Contributors to Volume 3
KP Koutsoumanis
Aristotle University of Thessaloniki, Thessaloniki,
Greece
DY Kwon
Korea Food Research Institute, Songnam, Republic of
Korea
G Kyureghian
Korea University, Seoul, Korea
B Lainoff
Global Crop Diversity Trust, Bonn, Germany
Y Li
Jiangnan University, Wuxi, Jiangsu, PR China
A Lianou
Agricultural University of Athens, Athens, Greece
C Lusty
Global Crop Diversity Trust, Bonn, Germany
N Meneses
Buehler AG, Corporate Technology, Uzwil, Switzerland
B van der Meulen
Wageningen University, Hollandseweg Wageningen,
The Netherlands
DH Putnam
University of California, Davis, CA, USA
G Rausser
University of California, Berkeley, CA, USA
K Reineke
Leibniz Institute for Agricultural Engineering (ATB),
Potsdam, Germany
GL Robertson
University of Queensland, Brisbane, Australia
AS SantAna
University of Campinas, Campinas, Brazil
SJ Scherr
EcoAgriculture Partners, Washington, DC, USA
O Schlueter
Leibniz Institute for Agricultural Engineering (ATB),
Potsdam, Germany
JS Shortle
Pennsylvania State University, University Park, PA,
USA
NBM Silva
Federal University of Espirito Santo, Alegre, Brazil
M Miao
Jiangnan University, Wuxi, Jiangsu, PR China
B Singh
The University of Sydney, Sydney, NSW, Australia
JC Milder
Rainforest Alliance, New York, NY, USA
JL Slavin
University of Minnesota, Saint Paul, MN, USA
S Mohanty
CGIAR, Philippines
JN Sofos
Colorado State University, Fort Collins, CO, USA
RO Morawicki
Fayetteville, AR, USA
SL Taylor
University of Nebraska, Lincoln, NE, USA
RM Nayga Jr.
University of Arkansas, Fayetteville, AR, USA
MR Thomsen
University of Arkansas, Fayetteville, AR, USA
E Nyakudya
Research Center for Industrial Development of Biofood
Materials, Jeonju, Republic of Korea
PH Thrall
Commonwealth Scientic and Industrial Research
Organisation, Canberra, ACT, Australia
SB Orloff
University of California Cooperative Extension, Yreka,
CA, USA
CP Timmer
Harvard University, Cambridge, MA, USA, and
Australian National University, Canberra, Australia
PG Pardey
University of Minnesota, InSTePP Center, Saint Paul,
MN, USA
J Toll
Global Crop Diversity Trust, Bonn, Germany
WEL Pea
Federal University of Viosa, Viosa, Brazil
RL Phillips
University of Minnesota, St. Paul, MN, USA
JH Trienekens
Wageningen University, Wageningen, The Netherlands
R Tsao
Guelph Food Research Centre, Guelph, Ontario,
Canada
Contributors to Volume 3
CN Verdouw
Wageningen University, Wageningen, The Netherlands
H Webster
Murdoch University, Perth, WA, Australia
L Willemen
Cornell University, Ithaca, NY, USA
CS Watts
Ross Road, Silver Spring, MD, USA
D Zilberman
University of California, Berkeley, CA, USA
ix
Cross-References
Index
Contributors
xi
SUBJECT CLASSIFICATION
Agriculture and People
Agribusiness Organization and Management
Agricultural Cooperatives
Agricultural Ethics and Social Justice
Agricultural Finance
Agricultural Labor: Demand for Labor
Agricultural Labor: Gender Issues
Agricultural Labor: Labor Market Operation
Agricultural Labor: Supply of Labor
Agricultural Law
Agricultural Policy: A Global View
Analyses of Total Phenolics, Total Flavonoids, and
Total Antioxidant Activities in Foods and Dietary
Supplements
Changing Structure and Organization of US
Agriculture
Climate Change, Society, and Agriculture: An
Economic and Policy Perspective
Computer Modeling: Policy Analysis and Simulation
Consumer-Oriented New Product Development
Crop Insurance
Determining Functional Properties and Sources of
Recently Identied Bioactive Food Components:
Oligosaccharides, Glycolipids, Glycoproteins, and
Peptides
Farm Management
Food Chain: Farm to Market
Food Labeling
Food Law
Food Marketing
Food Security, Market Processes, and the Role of
Government Policy
Food Security: Development Strategies
Food Security: Food Defense and Biosecurity
From Foraging to Agriculture
Global Food Supply Chains
Government Agricultural Policy, United States
Human Nutrition: Malnutrition and Diet
Industrialized Farming and Its Relationship to
Community Well-Being
Intellectual Property in Agriculture
International and Regional Institutions and
Instruments for Agricultural Policy, Research, and
Development
International Trade
Investments in and the Economic Returns to
Agricultural and Food R&D Worldwide
Markets and Prices
Mathematical Models to Elaborate Plans for Adaptation
of Rural Communities to Climate Change
xiii
xiv
Subject Classication
Agriculture Products
Advances in Pesticide Risk Reduction
Agricultural Mechanization
Agroforestry: Complex Multistrata Agriculture
Agroforestry: Fertilizer Trees
Agroforestry: Fodder Trees
Agroforestry: Participatory Domestication of Trees
Agroforestry: Practices and Systems
Asian Aquaculture
Beef Cattle
Climate Change: Animal Systems
Climate Change: Cropping System Changes and
Adaptations
Climate Change: Horticulture
Climate Change: New Breeding Pressures and Goals
Critical Tracking Events Approach to Food
Traceability
Dairy Animals
Edaphic Soil Science, Introduction to
Fermentation: Food Products
Fermented Beverages
Food Engineering
Food Microbiology
Food Packaging
Food Safety: Emerging Pathogens
Food Safety: Food Analysis Technologies/Techniques
Food Safety: Shelf Life Extension Technologies
Food Security: Postharvest Losses
Food Security: Yield Gap
Food Toxicology
Forage Crops
Global Agriculture: Industrial Feedstocks for Energy
and Materials
Green Revolution: Past, Present, and Future
Medicinal Crops
Organic Agricultural Production: Plants
Organic Livestock Production
Precision Agriculture: Irrigation
Animal Health
Animal Health: Ectoparasites
Animal Health: Foot-and-Mouth Disease
Animal Health: Global Antibiotic Issues
Animal Health: Mycotoxins
Animal Health: Tuberculosis
Animal Welfare: Stress, Global Issues, and
Perspectives
Biosecurity and Equine Infectious Diseases
Detection and Causes of Bovine Mastitis with
Emphasis on Staphylococcus aureus
Emerging Zoonoses in Domesticated Livestock of
Southeast Asia
Invasive Aquatic Animals
Marek's Disease and Differential Diagnosis with
Other Tumor Viral Diseases of Poultry
Poultry and Avian Diseases
Quarantine and Biosecurity
Swine Diseases and Disorders
Vaccines and Vaccination Practices: Key to
Sustainable Animal Production
Zoonotic Helminths of Livestock
Plant Health
Climate Change and Plant Disease
Emerging Plant Diseases
Integrated Pest Management in Tree Fruit Crops
Invasive Species: Plants
Mineral Nutrition and Suppression of Plant Disease
Pathogen-Tested Planting Material
Plant Abiotic Stress: Salt
Plant Abiotic Stress: Temperature Extremes
Plant Abiotic Stress: Water
Plant Biotic Stress: Weeds
Plant Disease and Resistance
Plant Health Management: Biological Control of
Insect Pests
Subject Classication
xv
Biotechnology: Pharming
Biotechnology: Plant Protection
Biotechnology: Regulatory Issues
Breeding: Animals
Breeding: Plants, Modern
Cloning Animals by Somatic Cell Nuclear
Transplantation
Cloning: Plants Micropropagation/Tissue Culture
Domestication of Animals
Domestication of Plants
Genebanks: Past, Present, and Optimistic Future
Genomics of Food Animals
Genomics: Plant Genetic Improvement
Heterosis in Plants
Plant Cloning: Macropropagation
Plant Virus Control by Post-Transcriptional Gene
Silencing
Regulatory Challenges to Commercializing the
Products of Ag Biotech
Stem Cells
Transgenic Methodologies Plants
PREFACE
Food is absolutely necessary for human existence, yet for most
in wealthy nations it is largely taken for granted because of its
abundance. Sufcient food is a concern, however, for about 1
billion of the earth's inhabitants today who often go to bed
hungry. Food security in a broad sense is becoming a worry of
the future for those who understand the limitations of our
earth's ecosystems. Malthusian prophecies have so far been
wrong, but there is growing concern that we are rapidly
reaching the point where feeding the world's growing and
richer population will be at the cost to our environment that is
unacceptable. In the next few decades we face the challenge of
growing more food, with less water, with less fertilizer on less
land because of the growth of urban areas on prime agriculture land. We also face the largely unknown consequences
that global warming will have on agricultural production.
During the last century agricultural scientists were able to bring
cutting-edge science into traditional agricultural practices and
increase food production sufciently to prevent global food
shortages. The hope that new scientic discoveries will provide
the means to keep ahead of world food demand is complicated by a growing public discomfort with biotechnology
being applied to food production.
The concept of services being provided by the ecosystems of
the earth is a fairly recent attempt to understand and place
value on functions of natural lands that have historically been
assumed to have few limits. In the past, if more food was
needed, new lands were converted from forests or steppe lands
into farm land and new water systems developed to provide
the water needed for agriculture. When human populations
were low our activities were largely buffered by the abundance
of forest and steppe, but too late, we are beginning to
understand that these provisioning services of our ecosystems
are being overused and are no longer buffered by the abundance of wild lands and waters. We are rapidly losing our
planet's biodiversity, irreplaceable ground water is being unsustainably consumed, and major river systems are being
overused and polluted. Our oceans, the last place on the planet that still support our hunter and gathering traditions may
not be able to sustain these activities into the future. And, food
production and processing activities contribute to the greenhouse gas emissions that are rapidly warming our planet.
Agriculture is the single greatest user of the earth's land and
water resources. In the concept of ecosystem services, provisioning or providing food for all organisms is one of the
services provided by ecosystems. Human population growth
has and will continue to overtax the ecosystems we inhabit.
The ultimate outcome of this major diversion of nature's resources into provisioning the human species is unknown, but
it is critically important for us to understand what we must do
to sustain our planet.
The breakthrough discovery about 10 000 years ago that
plants and animals could be bred to provide a more abundant
and secure food source was the foundation upon which
all other human activities were able to ourish. Activities other
than nding food now became possible and our diverse
The issue raised by Dr. Borlaug is probably the most important challenge we face. Human behavior and the food
choices of consumers will determine the outcome of the race
between food supply and population. Population control has
been advocated for decades, and in some cases has become
part of national policy, but the world's population continues
to grow. Science breakthroughs cannot solve our food security
and environmental quality challenges if consumers reject food
that is not traditionally produced. Likewise, if meat products
and other inefciently produced food continue to be in high
demand by consumers, there will be increased pressure on our
food production systems. As supplies become short, prices rise.
While this may be good for farmers, high food prices and food
shortages will probably undermine our efforts to preserve the
xvii
xviii
Preface
fortunate to be joined by a very distinguished group of colleagues who, I hope, are still friends. They spent much more
time and effort in bringing this project to completion than any
of us anticipated. I want to thank our authors who while
overly committed and overworked, fullled their commitments to contribute to this work. I have been impressed with
the quality of their contributions. The editorial staff of Elsevier
have had the professionalism and patience to work with scientists who do not work under the same time and budget
constraints that the staff work. I want to particularly thank
Kristi Gomez, Donna de Weerd-Wilson, and Simon Holt who,
each in succession, oversaw this effort, and I especially thank
the project managers, who worked directly with me, and the
associate editors, Kate Miklaszewka-Gorczyca, Will BowdenGreen, and Sam Mahfoudh.
Neal K Van Alfen
Professor, Department of Plant Pathology Dean Emeritus,
College of Agricultural and Environmental Sciences,
University of California Davis, CA, USA
CONTENTS TO VOLUME 3
Editorial Board
Contributors to Volume 3
Guide to using the Encyclopedia
v
vii
xi
Subject Classification
xiii
Preface
xvii
E
Ecoagriculture: Integrated Landscape Management for People, Food, and Nature
SJ Scherr, L Buck, L Willemen, and JC Milder
18
35
59
68
82
F
Farm Management
W Edwards and P Duffy
100
113
Fermented Beverages
CW Bamforth
124
137
Food Engineering
RM Boom and AEM Janssen
154
Food Labeling
CA Hutt and M Gonzalez
167
Food Law
B van der Meulen
186
Food Marketing
MR Thomsen, G Kyureghian, and RM Nayga Jr.
196
Food Microbiology
HM Hungaro, WEL Pena, NBM Silva, RV Carvalho, VO Alvarenga, and AS SantAna
213
xix
xx
Contents to Volume 3
Food Packaging
GL Robertson
232
250
273
289
304
311
324
338
352
Food Toxicology
SL Taylor and JL Baumert
366
Forage Crops
DH Putnam and SB Orloff
381
406
G
Genebanks: Past, Present, and Optimistic Future
C Lusty, L Guarino, J Toll, and B Lainoff
417
433
454
461
499
518
529
H
Heterosis in Plants
JA Birchler
539
544
E
Ecoagriculture: Integrated Landscape Management for People, Food,
and Nature
SJ Scherr, EcoAgriculture Partners, Washington, DC, USA
L Buck and L Willemen, Cornell University, Ithaca, NY, USA
JC Milder, Rainforest Alliance, New York, NY, USA
r 2014 Elsevier Inc. All rights reserved.
Glossary
Agricultural biodiversity (agrobiodiversity) The
variability among living organisms associated with the
cultivation of crops and rearing of animals, and the
ecological complexes of which those species are part. This
includes diversity within and between species, and of
ecosystems.
Agroecosystem An ecological and socioeconomic
system, comprising domesticated plants and animals
and the people who husband them, intended for the
purpose of producing food, ber, and other agricultural
products.
Biological diversity (biodiversity) The variability among
living organisms from all sources, including terrestrial,
marine, and other aquatic ecosystems and the ecological
complexes of which they are part; this includes
genetic diversity within species, between species, and of
ecosystems (Convention on Biological Diversity or CBD,
article 2).
Connectivity A measure of spatial continuity of a
vegetative corridor, biological network, or matrix.
Conservation agriculture An agriculture practice that aims
to achieve sustainable and protable agriculture through the
application of the three principles: (1) minimal mechanical
soil disturbance, (2) permanent soil cover, and (3) crop
rotation (based the Food and Agriculture Organization of
the United Nations publications).
Corridor A strip of a particular type of land that differs
from the adjacent land on both sides. Such corridors may
have important ecological functions including conduit,
barrier, habitat, and improve connectivity.
Ecoagriculture An approach to the managing landscapes
for the simultaneous and synergistic achievement of three
sets of outcomes: (1) maintaining, increasing, or improving
agricultural production; (2) conserving biodiversity and
ecosystem services; and (3) enhancing human livelihoods
and well-being. These elements are stitched together by
institutions that support multistakeholder collaboration to
achieve these outcomes.
doi:10.1016/B978-0-444-52512-3.00029-2