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Biological Control 45 (2008) 254–271

www.elsevier.com/locate/ybcon

Maximizing ecosystem services from conservation biological

control: The role of habitat management
Anna K. Fiedler a,*, Doug A. Landis a, Steve D. Wratten b
a
Department of Entomology, 204 Center for Integrated Plant Systems, Michigan State University, East Lansing, MI 48824-1311, USA
b
National Centre for Advanced Bio-Protection Technologies, P.O. Box 84, Lincoln University, Lincoln 7647, New Zealand

Received 21 August 2007; accepted 20 December 2007

Available online 11 January 2008

Abstract

The intentional provision of flowering plants and plant communities in managed landscapes to enhance natural enemies is termed
habitat management and is a relatively new but growing aspect of conservation biological control. The focus of most habitat manage-
ment research has been on understanding the role of these plant-provided resources on natural enemy biology, ecology, and their ability
to enhance suppression of pest populations. Far less attention has been paid to additional ecosystem services that habitat management
practices could provide in managed landscapes. We first evaluate whether habitat management is well positioned to advance in these
areas. Our analysis of past habitat management studies indicates that four plant species have been tested in the majority of field eval-
uations, while plants native to the test area and perennial plants are particularly underrepresented. We suggest that synergies among
biodiversity conservation, ecological restoration, human cultural values, tourism, biological control and other ecosystem services have
largely been overlooked in past habitat management research and we illustrate how these potential ecosystem services could be evaluated
and enhanced. We then review two case studies in which broader ecosystem services were explicitly addressed in plant selection criteria.
One case study demonstrates that native plants useful in restoration of rare ecosystems can increase natural enemy abundance as much as
widely recommended non-natives. The second addresses additional ecosystem services provided by habitat management in New Zealand
vineyards. We conclude that addressing ‘stacked’ ecosystem services with multiple ecosystem service goals can decrease agriculture’s
dependence on ‘substitution’ methods such as the current reliance on oil-based agro-chemical inputs.
Ó 2007 Elsevier Inc. All rights reserved.

Keywords: Native plants; Ecological restoration; Biodiversity conservation; Biological control; Ecosystem services

1. Introduction duction of harvested products, provision of clean air and

Modern agricultural landscapes have been shaped by
production systems aimed at maximizing yield and profit-
ability. While these landscapes generally fulfill this goal
admirably, there are increasing calls for agriculture to
broaden the range of ecosystem services it provides to soci-
ety (Robertson and Swinton, 2005; Swinton et al., 2006).
Ecosystem (or nature’s) services are defined as all of the
‘‘conditions and processes” by which ecosystems ‘‘sustain
and fulfill human life” (Daily, 1997). Examples of these ser-
vices from both managed and natural systems include pro-
*
Corresponding author. Fax: +1 517 432 5282.
E-mail address: fiedlera@msu.edu (A.K. Fiedler).
water, regulation of climate, maintenance of biodiversity,
biological control of pests, diseases and weeds, and cultural
or aesthetic values (Costanza et al., 1997). As part of a con-
servation biological control approach, habitat management
seeks to maximize one specific ecosystem service, i.e., pest
regulation, by enhancing natural enemy impact through
manipulating plant-based resources in the landscape (Bugg
and Pickett, 1998). Typically, this is accomplished by
selecting plants that provide a limiting resource such as
pollen, nectar, alternative hosts, or shelter and establishing
these plants or plant communities within the managed sys-
tem (Landis et al., 2000). In contrast with other types of
pest management, habitat management appears to be
uniquely positioned to provide directly or to synthesize

1049-9644/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.biocontrol.2007.12.009
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271
the provision of many additional ecosystem services that
society values. These include aesthetics, conservation of
biodiversity, wastewater treatment, and weed suppression
while enhancing invertebrate biological control. The latter
can be achieved through the provision of shelter, nectar,
alternative prey/hosts and/or pollen for natural enemies,
which can be easily deployed by individual growers.
Past research on habitat management for biological con-
trol has primarily focused on maximizing the pest reduc-
tion service it can provide. This emphasis is clearly
evident in the selection criteria used to choose plants for
habitat management research. These include: attractiveness
to natural enemies (Bugg et al., 1989; Maingay et al., 1991;
Patt et al., 1997), prolific production of pollen and/or nec-
tar (Zhao et al., 1992), accessibility of floral resources (Bag-
gen et al., 1999; Wäckers et al., 1996), flowering phenology
(Freeman-Long et al., 1998; Rebek et al., 2005; Stephens
et al., 1998; Winkler, 2005), availability of seed (Hickman
and Wratten, 1996), use of plants already present in, or
adapted to, agricultural areas (Altieri and Whitcomb,
1979; Foster and Ruesink, 1984; Idris and Grafius, 1995;
Nentwig, 1998; Nentwig et al., 1998; Nicholls et al.,
2000), previous success (Ambrosino et al., 2006; Frank
and Shrewsbury, 2004; Lavandero et al., 2005; Stephens
et al., 1998), and selectivity in favor of the natural enemy
rather than its own (fourth trophic level) natural enemies,
or the pest itself (Araj et al., 2006). However, for habitat-
management approaches to enhance other ecosystem ser-
vices, researchers need to consider additional criteria in
selecting plants for their studies as well as new partnerships
in both the research and implementation phases of their
work.
The goal of this paper is to document the ecosystem ser-
vices beyond pest suppression that might be enhanced via
habitat management, and to illustrate potential advantages
of research aimed at achieving multiple goals. We begin by
examining past field studies of habitat management and
asking whether the discipline is currently well positioned
to synergize broader ecosystem services. We then review
the range of additional ecosystem services that could
accrue from habitat management practices but have not
been well studied, specifically, biodiversity conservation,
ecological restoration, and human cultural values. Finally,
we examine case studies where the provision of ecosystem
services is explicitly woven into the research agenda and
how this can lead to increased multi-functionality of habi-
tat management practices.
2. Plant selection for multifunction habitat management
2.1. How diverse is the toolbox?
Achieving multiple ecosystem services from habitat
management is an attractive goal and plants that provide
resources for natural enemies may well provide such addi-
tional benefits. We therefore begin by examining past field
studies of habitat management to assess if the plants tested
255
to date already provide a broad cross-section of plant
diversity from which to harvest such ecosystem services.
We anticipate that surveying a large number of plant spe-
cies would provide the best chance for observing unique
benefits, and candidate plants should represent a broad
range of functional groups including trees, shrubs, vines,
grasses, legumes, and forbs. Additionally, it may be impor-
tant to screen species with differing life histories ranging
from annual to long-lived perennials. While both native
and exotic species should be represented, plants native to
the region of study may best enhance biodiversity and
related ecosystem services. Finally, the cultural services
that such plants could provide should also be considered.
To assess the number and diversity of plants that have
been studied for habitat management, we examined field
studies published in peer-reviewed literature in which
plants were purposefully established to provide nectar
and pollen to natural enemies. To identify such studies,
we performed a search on ISI Web of Science in the
‘‘Title/keywords/abstract” frame using the following
search terms: flower* and conservation biological control,
flower* and natural enemy, and habitat management and
conservation biological control (actual search terms in ital-
ics). We also considered any references cited within papers
found in these searches and selected only studies reporting
original data and excluded strictly laboratory or observa-
tional studies.
We found 34 studies that met our criteria dating from
1989 (Table 1). While several studies performed prior to
1989 documented natural enemies visiting flowering crops
or weeds already present in or near an agricultural area
(Altieri and Whitcomb, 1979; Bugg et al., 1987; Leius,
1967), none involved the purposeful establishment of
plants to enhance natural enemy effectiveness. The number
of published studies per year ranged from 0–9 and has
increased since 1989, indicating a growing interest in habi-
tat management (Fig. 1, Gurr et al., 2004). Of the studies
identified, 19/34 (0.56) examined only plants that were
not native to the area of study, while 14/34 (0.41) examined
both native and exotic plants, and 1/34 (0.03) only native
plants. Similarly, annual and perennial plants have not
been considered equally in habitat management: 14/34
(0.41) of studies considered only annual plants, 17/34
(0.5) included both annual and perennial plants and only
3/34 (0.09) considered perennial plants alone. In total, only
165 species of plants appear to have been field tested for
their utility in habitat management (Table 2). Even this
modest number is heavily influenced by just six studies that
each considered more than 20 plant species (Braman et al.,
2002; Chaney, 1998; Denys and Tscharntke, 2002; Fiedler
and Landis, 2007a; Freeman-Long et al., 1998; Rogers
and Potter, 2004). Species tested to date represent 35 plant
families but only 4 families have had more than 10 species
tested (Apiaceae, Asteraceae, Fabaceae, Lamiaceae). In
addition, species tested consist almost entirely of forbs,
with only 8 tree, 8 shrub, and 2 vine species, respectively
(Table 2).
 256
Table 1
Flowering forbs, shrubs, and trees species considered in habitat management field studies and the reason outlined for their selection

A.K. Fiedler et al. / Biological Control 45 (2008) 254–271

Ref. Study Origin Growth habit Species considered Study Reason Other considerations
type
Introduced Native Annual Perenniala Phacelia Buckwheat Alyssum Coriander
1 Bugg and Wilson 1 — — 1 E O —
(1989)
2 Maingay et al. (1991) 8 4 2 10 + S O Agronomic, natural enemy
benefit
3 Lövei et al. (1992) 1 — 1 — + E Li Agronomic
4 Zhao et al. (1992) — 1 — 1 E O Natural enemy benefit
5 Lövei et al. (1993) 9 — 9 — + + + S S Agronomic
6 White et al. (1995) 1 — 1 — + E L Agronomic
7 Hickman and 1 — 1 — + E L Agronomic
Wratten (1996)
8 Patt et al. (1997) 2 — 2 — + E O Agronomic, natural enemy
benefit
9 Baggen and Gurr 2 — 2 — + S, E S Selective food plant
(1998)
10 Chaney (1998) 12 10 21 1 S, E S Annual/perennial based on
system
11 Freeman-Long et al. 8 15 10 13 + + + E B Annual, perennial, natural
(1998)b enemy benefit
12 Stephens et al. (1998) 1 — 1 — + E L Presumed natural enemy
benefit
13 Colley and Luna 10 1 7 4 + + + + S L, O, S Agronomic
(2000)
14 Nicholls et al. (2000) 1 1 2 + E C Presumed natural enemy
benefit
15 Berndt et al. (2002) 1 — 1 — + E L Agronomic
16 Braman et al. (2002)b 7 15 9 10 (4)g E M Mix, ornamental, structural
complexity
17 Denys and 3 19 8 14 + + + E Mj Research design/biodiversity
Tscharntke (2002)
18 English-Loeb et al. 2 — 1 1 + E Agronomic
(2003)
19 Fitzgerald and 4 10 8 6 + + S, E S —
Solomon (2004)
20 Frank and 1 1 1 1 + E L Ornamental
Shrewsbury (2004)
21 Rogers and Potter 18 10 5 22 (1)h S O Ornamental, natural enemy
(2004)c benefit
22 Shrewsbury et al. 2 — 1 1 + E O Ornamental
(2004)c
23 Ellis et al. (2005) 3 1 1 3 E O Ornamental, agronomic,
natural enemy benefit
24 Lavandero et al. 1 — 1 — + E L Selective food plant
(2005)
25 Lee and Heimpel 1 — 1 — + E L Natural enemy benefit, selective
(2005) food plant
26 Rebek et al. (2005, 2 2 — 4 E L, O Natural enemy benefit
2006)d
27 Ambrosino et al. 3 1 4 — + + + + S L —
(2006)
28 Begum et al. (2006) 5 — 4 1 + + + E C Selective food plant

A.K. Fiedler et al. / Biological Control 45 (2008) 254–271

29 Berndt et al. (2006) 1 — 1 — + E L Agronomic
30 Fiedler and Landis 5 43 5 43 S S, L Biodiversity, agronomic
(2007a,b)d
31 Forehand et al. 15 — 7 8 + + E M —
(2006)e
32 Irvin et al. (2006) 3 — 2 1 + + + E, S L Perennial, agronomic
33 Pontin et al. (2006) 7 — 6 1 + + + + S M, L Single plant vs. mixtures
34 Winkler et al. (2006)f 1 — 1 — + E L Selective food plant

The number of species of native and non-native origin and the number that are perennial and annual are based on the study location. The four most commonly considered species are listed individually,
marked with a ‘‘+” when considered in a study. Study type is characterized as: E: efficacy in natural enemy attraction or impact, or S: screening plants for future evaluation. The stated reason for plant
selection listed is: O: attractive based on observation, L: attractive based on literature, S: screening plants for attractiveness, M: mix of pre-selected plants, B: bloom period, C: cover crop. Additional
considerations for plant selection are listed.
a
Includes biennials and perennials.
b
Used two plant groupings to bloom during different time periods.
c
Cultivars counted as one species.
d
Both publications use the same study design.
e
Achillea spp. included in mix but unidentifiable beyond genus; not included in these counts.
f
Field mesocosm study.
g
Three plants not identified to species; origin unidentifiable, growth habit unidentifiable for two.
h
Species in parentheses grow as annual or perennial depending on growing conditions.
i
Conference proceedings, based on a 1993 publication.
j
Testing a variety of strip establishment methods.

257
258
8 in previous studies (literature), 7/34 (0.21) were based on
Number of studies published
6
4 (0.12) included a combination of these rationales for spe-
2 Finally, we examined other considerations that the
0
1988 1990 1992 1994 1996 1998 2000 2002 2004 2006
Year
Fig. 1. The number of habitat management field studies using plants to
provide nectar and pollen published per year, through October 2006.
The four most frequently studied plant species in habitat
management include Phacelia tanacetifolia Benth. (phac-
elia), Fagopyrum esculentum Moench (buckwheat), Lobu-
laria maritima (L.) Desv. (alyssum) and Coriandrum
sativum L. (coriander). One or more of these four plant spe-
cies was used in 27/34 (0.79) of the studies tabulated (Table
1). All four of these species are annual, although L. mariti-
ma grows as a perennial in temperate climates. It appears
that because these plants were effective in early habitat
management studies, they have become influential on other
research programs. Frequently, researchers note that they
included one or more of these plants in their studies
because they were effective in prior work. Additionally,
research groups have tended to repeatedly publish on spe-
cies they find of particular usefulness. The overall result is
that a relatively small suite of plants has come to dominate
the habitat management literature and they are frequently
used in areas outside of their native ranges. However, it is
true that when these four species have been compared in
laboratory bioassays, their enhancement of the fitness of
parasitoids does confirm their high ranking (Araj et al.,
2006; Berndt et al., 2006; Irvin et al., 2006; Lavandero
et al., 2005), although such laboratory comparisons rarely
include plants endemic to the country in which the experi-
ments are conducted.
Choice of plant species is also likely influenced by the
primary goal of the research. Efficacy studies often focus
on one or a few species already proven to be highly attrac-
tive to natural enemies while screening studies typically cast
a wider net. With this in mind we characterized the studies
in Table 1 into several broad types based on their primary
goal. Most, 23/34 (0.68) were conducted primarily to assess
efficacy, e.g., increased natural enemy abundance, parasit-
ism rates, or decreasing pest populations in the field. In
contrast, 7/34 (0.21) of the studies were primarily screening
efforts where efficacy was not addressed, and the remainder
of studies included both screening and efficacy compo-
nents, 4/34 (0.12). We identified several primary reasons
for plant selection (Table 1). In 12/34 (0.35) of the studies,
A.K. Fiedler et al. / Biological Control 45 (2008) 254–271
species were selected based primarily on their effectiveness
researcher observation of frequent natural enemy visita-
tion, 4/34 (0.12) were primarily performed to screen plants
for relative attractiveness, and 3/34 (0.09) to assess mix-
tures of previously recommended species. Another 4/34
cies selection; all included selection based on prior
literature.
researchers used in plant selection. The most common of
these were agronomic considerations such as use of plants
already in crop environments, ease of establishment, seed
availability, and value in agriculture as cover or alternative
crops. A large number of studies also stated that plant
selection was at least in part based on perceived benefits
of the plants to natural enemies, including prolonged flow-
ering period, accessibility of nectar, and using plants from
families known to be attractive to natural enemies (e.g.,
Asteraceae, Apiaceae). Another group of studies also
examined plant species’ ability to provide resources to nat-
ural enemies and not pests (selective food plants). Only two
studies explicitly considered biodiversity maintenance and
enhancement or conservation potential as a criterion for
plant selection.
Worldwide, flowering plant diversity is estimated to be
ca. 248,000 species (Judd, 2002); it is clear that only a tiny
fraction of the plants that might potentially be used in hab-
itat management have ever been tested. The pattern that
emerges in habitat management is that: (1) a small number
of annual plant species which have been proven effective
have been tested repeatedly, often in locations where they
are not native, (2) nearly half of the studies used plants
selected based on previous success, (3) the majority of stud-
ies have primarily sought to test efficacy, with only a small
proportion aimed at identifying new species for use in hab-
itat management, and (4) of all these studies, only two have
expressly sought to explore additional ecosystem benefits
beyond pest population reduction. These patterns suggest
that additional screening to identify species with potential
to provide multiple ecosystem services should be a high pri-
ority for habitat management researchers. Such future
studies should include plants from different growth habit
and life history groups.
3. Ecosystem services and habitat management
3.1. Types of ecosystem services
The concept of ecosystem services (Daily, 1997) has seen
rapid acceptance and is currently viewed as a major orga-
nizing principle in sustainability research and implementa-
tion (Reid et al., 2005). Taken as a whole, the earth’s
biodiversity is organized into various managed and unman-
aged ecosystems which provide many services to human-
kind (Table 3). These include basic supporting services
such as soil formation, photosynthesis and primary
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271 259

Table 2
Plant species evaluated in the field for use in habitat management through October 2006
Family Genus species Common name Growth habit References
Apiaceae Ammi majus L. Bishop’s flower Forb 10, 33
Ammi visnaga (L.) Lamarck Toothpick ammi Forb 1, 2, 16
Anethum graveolens L. Dill Forb 2, 8, 31, 33, 34
Angelica atropurpurea L. Angelica Forb 16, 34
Anthriscus cerefolium (L.) Hoffmann Chervil Forb 10, 31
Anthriscus sylvestris (L.) Hoffmann Cow parsley Forb 17, 19
Apium graveolens L. Celery Forb 11, 31
Carum carvi L. Caraway Forb 2, 31
Coriandrum sativum L. Coriander/cilantro Forb 2, 5, 8, 9, 10, 11, 13, 17, 19, 22,
27, 28, 31, 33, 34
Daucus carota L. Wild carrot/Queen Anne’s lace Forb 2, 17, 19, 21, 31
Foeniculum foeniculum (Pursh) Kuntze Blue giant hyssop Forb 31
Foeniculum vulgare Mill. Fennel Forb 2, 13, 21, 33
Heracleum sphondylium L. Eltrot Forb 17
Heracleum maximum Bartr. Cow parsnip Forb 34
Pastinaca sativa L. Wild parsnip Forb 17
Zizia aurea (L.) Koch Golden alexanders Forb 34
Apocynaceae Apocynum cannabinum L. Indian hemp Forb 34
Asclepiadaceae Asclepias fascicularis Dcne. Milkweed Forb 11
Asclepias incarnata L. Swamp milkweed Forb 34
Asclepias syriaca L. Common milkweed Forb 2
Asclepias tuberosa L. Butterfly weed Forb 2, 21, 34
Asteraceae Achillea millefolium L. Yarrow Forb 2, 10, 11, 13, 16, 17, 21
Achillea spp. Yarrow Forb 34
Anthemis arvensis L. Corn chamomile Forb 19
Aster laevis L. Smooth aster Forb 34
Aster novae angliae L. New England aster Forb 34
Aster novi-belgii L. New York aster Forb 23
Baccharis pilularis DC. Coyotebrush Shrub 11
Baccharis viminea DC. Mule fat Shrub 11
Cacalia atriplicifolia L. Pale Indian plantain Forb 34
Calendula officinalis L. Calendula Forb 5, 13, 17
Centaurea cyanus L. Garden cornflower Forb 16, 17, 19
Centaurea jacea L. Brownray knapweed Forb 17
Centaurea montana L. Mountain bluet Forb 21
Chrysanthemum maximum x superbumi Max chrysanthemum Forb 22
Chrysanthemum segetum (L.) Fourr. Corn marigold Forb 19
Cichorium intybus L. Chickory Forb 17
Coreopsis lanceolata L. Sand coreopsis Forb 16, 34
Coreopsis tinctoria Nutt. Golden tickseed Forb 16
Coreopsis verticillata L.b Coreopsis Forb 20, 26
Echinacea purpurea (L.) Moench Purple coneflower Forb 21
Eupatorium perfoliatum L. Boneset Forb 34
Gaillardia aristata Pursh Common gaillardia Forb 16
Gaillardia pulchella Foug. Firewheel Forb 16
Gazania rigens (L.) Gaertn. Treasure-flower Forb 23
Helianthus annum L. Sunflower Forb 5, 14
Helianthus strumosus L. Pale-leaved sunflower Forb 34
Helichrysum bracteatum (Vent.) Andr. Bracted strawflower Forb 16
Layia platyglossa (Fisch. & C.A. Mey.) Gray Tidy tips Forb 10, 11
Leucanthemum vulgare Lam. Oxeye daisy Forb 17, 19
Leucanthemum x superbum Shasta daisy Forb 23
Liatris aspera Michx. Rough blazing star Forb 34
Melampodium paludosum L. Medallion flower Forb 21
Ratibida columnifera (Nutt.) Woot. & Standl.a Prairie coneflower Forb 21
Ratibida pinnata (Vent.) Barnh. Yellow coneflower Forb 34
Rudbeckia hirta L.c Blackeyed Susan Forb 16, 21
Senecio obovatus Muhl. ex Willd. Round-leaved ragwort Forb 34
Silphium perfoliatum L. Cup plant Forb 34
Solidago sp. Goldenrod Forb 2
Solidago canadensis L.b Late goldenrod Forb 23, 26
(continued on next page)
260 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271

Table 2 (continued)
Family Genus species Common name Growth habit References
Solidago riddellii Frank ex Riddell Riddell’s goldenrod Forb 34
Solidago speciosa Nutt. Showy goldenrod Forb 34
Tagetes patula L. French marigold Forb 13
Tanacetum vulgare L. Common tansy Forb 17
Vernonia missurica Raf. Ironweed Forb 34
Zinnia elegans Jacquin Common zinnia Forb 21
Boraginaceae Borago officinalis L. Borage Forb 9, 17, 28
Echium lycopsis L. p.p. Borage Forb 5
Echium vulgare L. Common viper’s bugloss Forb 17
Brassicaceae Aurinia saxitalis (L.) Desv. Aurinia Forb 13
Brassica juncea (L.) Czern. Mustard Forb 13, 28
Iberis sp. Candytuft Forb 16
Lobularia maritima (L.) Desv. Alyssum Forb 10, 11, 13, 20, 27,
28, 31, 32, 33, 34
Nasturtium sp. Forb 16
Raphanus sativus L. Daikon/radish Forb 31
Sinapis alba L. White mustard Forb 17
Campanulaceae Campanula glomerata L. Bell flower Forb 19
Campanula persicifolia L. Peach-leaved bellflower Forb 21
Lobelia cardinalis L. Cardinal flower Forb 21
Lobelia siphilitica L. Great blue lobelia Forb 21, 34
Caprifoliaceae Sambucus mexicana K. Presl ex DC. Elderberry Shrub 11
Sambucus racemosa L. Red-berried elder Tree 34
Caryophyllaceae Agrostemma githago Common corncockle Forb 17, 19
Gypsophila sp. Gypsophila Forb 31
Silene alba (P. Mill.) Krause Bladder campion Forb 17
Chenopodiaceae Chenopodium quinoa Willd. Quinoa Forb 5
Euphorbiaceae Euphorbia epithymoides L. Flowering spurge Forb 26
Fabaceae Amorpha canescens Pursh Leadplant Shrub 34
Cassia fasciculata Michx. Partridge pea Tree 16
Desmodium canadense (L.) DC. Showy tick trefoil Forb 34
Lespedeza hirta (L.) Hornem. Hairy bush-clover Forb 34
Lotus corniculatus L. Bird’s foot trefoil Forb 19
Lupinus albus L. White lupine Forb 10
Medicago sativa L. Alfalfa Forb 31
Trifolium incarnatum L. Crimson clover Forb 11, 31
Trifolium repens L. Ladino, white clover Forb 11, 18, 26, 31
Trifolium subterrraneum L. Subclover Forb 11, 31
Vicia faba L. Faba bean Forb 9, 10, 34
Vicia sativa L. Common vetch Vine/forb 11
Gentianaceae Exacum sp. Exacum Forb 21
Geraniaceae Geranium endressii Gayd Cranesbill Forb 21
Geranium maculatum L. Wild geranium Forb 34
Hydrophyllaceae Hydrophyllum virginianum L. Virginia waterleaf Forb 34
Nemophila menziesii Hook. & Arn. Baby blue eyes Forb 10, 16
Phacelia campanularia Gray Wild Canterbury bells Forb 10
Phacelia tanacetifolia Benth. Phacelia Forb 3, 5, 6, 7, 10, 11, 13, 17,
19, 27, 31, 32, 33
Iridaceae Iris germinica L.e Iris Forb 21
Lamiaceae Acinos arvensis Dandy Basil thyme Forb 21
Agastache foeniculum (Pursh) Kuntze Anise hyssop Forb 4, 21
Agastache nepetoides (L.) Kuntze Yellow giant hyssop Forb 34
Agastache rugosa Korean licorice mint Forb 13
Mentha spicata L. Spearmint Forb 2
Monarda citriodora Cerv. ex Lag. Lemon bee balm Forb 16
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271 261

Table 2 (continued)
Family Genus species Common name Growth habit References
Monarda punctata L. Horsemint Forb 34
Prunella vulgaris L. Selfheal Forb 19
Salvia farinacea Benth. Mealy-cup sage Forb 16, 21
Salvia uliginosa Benth. Bog sage Forb 21
Salvia viridis L. Clary sage Forb 21
Liliaceae Allium cernuum Roth Nodding wild onion Forb 34
Convallaria majalis L. Lily of the valley Forb 21
Linaceae Linum grandiflorum Desf. Scarlet flax Forb 10
Onagraceae Clarkia amoena (Lehm.) A. Nels. & J.F. Macbr. Farewell-to-spring Forb 10
Clarkia concinna (Fisch. & C.A. Mey.) Greene Red ribbons Forb 10
Clarkia unquiculata Lindl. Elegant clarkia Forb 10
Oenothera speciosa Nutt. Pinkladies Forb 16
Oenothera biennis L. Evening primrose Forb 16, 17, 34
Paeoniaceae Paeonia lactiflora Pallasf Peony Forb 21
Papaveraceae Eschscholzia californica Cham. California poppy Forb 16
Papaver rhoeas L. Corn poppy Forb 10, 16, 17, 19
Stylomecon heterophylla (Benth.) G. Taylor Wind poppy Forb 10
Polemoniaceae Gilia tri-color Benth. Bird’s eyes Forb 10
Linanthus grandiflorus (Benth.) Greene Mountain phlox Forb 10
Polygonaceae Eriogonum fasciculatum Benth. California buckwheat Forb 11
Eriogonum giganteum S. Wats. St. Catherine’s lace Forb 11
Fagopyrum esculentum Moench Buckwheat Forb 5, 10, 12, 13, 14,
15, 16, 17, 18, 19,
24, 25, 27, 28, 29,
30, 31, 32, 33, 34
Ranunculaceae Anemone canadensis L. Canada anemone Forb 34
Aquilegia canadensis L. Columbine Forb 34
Consolida ambigua (L.) P.W. Ball & Heywood Doubtful knight’s-spur Forb 16
Thalictrum aquilegifolium L. Meadow rue Forb 21
Rhamnaceae Ceanothus sp. California lilac Shrub 11
Ceanothus americanus L. New Jersey tea Shrub 34
Rhamnus californica Eschsch. Coffeeberry Tree 11
Rosaceae Fragaria virginiana Duchesne Wild strawberry Forb 34
Heteromeles arbutifolia (Lindl.) M. Roemer Toyon Tree 11
Potentilla fruticosa auct. non L. Shrubby cinquefoil Shrub 34
Prunus ilicifolia Nutt. ex Hook. & Arn.) Hollyleaf cherry Tree 11
D. Dietr.
Quillaja saponarea Molina Soapbark tree Tree 11
Rosa setigera Michx. Michigan rose Vine/shrub 34
Spiraea alba Duroi Meadowsweet Shrub 34
Rubiaceae Cephalanthus occidentalis L. Buttonbush Tree 34
Rutaceae Ruta graveolens L. Rue Forb 2
Salicacaeae Salix sp. Willow Tree 11
Saxifragaceae Astilbe x arendsii Bridal veil Forb 21
Heuchera americana L. Alum root Forb 34
Scrophulariaceae Collinsia heterophylla Buist ex Graham Chinese houses Forb 10
Linaria maroccana Hook. f. Toadflax Forb 10
Penstemon hirsutus (L.) Willd. Penstemon Forb 34
Scrophularia marilandica L. Late figwort Forb 34
Verbascum phlomoides L. Orange mullein Forb 17
Veronicastrum virginicum (L.) Farw. Culver’s-root Forb 34
Solanaceae Nicotiana alata x sanderae Link & Otto Flowering tobacco Forb 21
Petunia x hybrida Vilmg Petunia Forb 21
Tropaeolaceae Tropaeolum majus L. Nasturtium Forb 31
(continued on next page)
262 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271

Table 2 (continued)
Family Genus species Common name Growth habit References
Verbenaceae Verbena canadensis (L.) Brittonh Rose verbena Forb 21
Verbena stricta Vent. Hoary vervain Forb 34
Growth habit based on USDA plants database classifications (http://plants.usda.gov/). If more than one habit type was listed, the first type listed is shown
here. Plants classified as subshrubs counted as shrubs.
References: 1Bugg and Wilson (1989), 2Maingay et al. (1991), 3Lövei et al. (1992), 4Zhao et al. (1992), 5Lövei et al. (1993), 6White et al. (1995), 7Hickman
and Wratten (1996), 8Patt et al. (1997), 9Baggen and Gurr (1998), 10Chaney (1998), 11Freeman-Long et al. (1998), 12Stephens et al. (1998), 13Colley and
Luna (2000), 14Nicholls et al. (2000), 15Berndt et al. (2002), 16Braman et al. (2002), 17Denys and Tscharntke (2002), 18English-Loeb et al. (2003),
19
Fitzgerald and Solomon (2004), 20Frank and Shrewsbury (2004), 21Rogers and Potter (2004), 22Shrewsbury et al. (2004), 23Ellis et al. (2005), 24Lavandero
et al. (2005), 25Lee and Heimpel (2005), 26Rebek et al. (2005, 2006), 27Ambrosino et al. (2006), 28Begum et al. (2006), 29Berndt et al. (2006), 30Winkler et al.
(2006), 31Forehand et al. (2006), 32Irvin et al. (2006), 33Pontin et al. (2006), 34Fiedler and Landis (2007a,b).
a
Listed as Rudbeckia ratibida L.
b
cv. Moonbeam.
c
cv. Irish Eyes, Rustic Colors.
d
cv. Wargrave Pink.
e
cv. Gold Galore, Immortality, Royal Touch.
f
cv. Sarah Bernhardt, Duchessee De Nemours, Felix Crousse.
g
Red, white, and yellow hybrid petunia.
h
cv. Aztec mix.
i
cv. Snow Lady, Little Princess, Marconi.

production, provisioning services such as food, fiber, and
genetic resources, regulating services such as climate regula-
tion, pest suppression, and water purification and finally,
cultural services including spiritual/religious values, aes-
thetic, and recreational benefits.
3.2. Habitat management and ecosystem services
Within the context of established biological control
methods (i.e., importation, augmentation, and conserva-
tion), habitat management is unique in its ability to pro-
vide a wide variety of ecosystem services in addition to
pest population reduction. This fundamental difference is
a result of habitat management practices that establish
and maintain greater diversity of primary producers
within a particular system. By acting at this first trophic
level, habitat management is uniquely positioned to affect
many other ecosystem processes. Most habitat manage-
ment research to date has been focused at relatively small
scales. Examples include establishment of experimental
plots in home landscapes, urban, or golf course settings
(Ellis et al., 2005; Frank and Shrewsbury, 2004; Rogers
and Potter, 2004; Shrewsbury et al., 2004), or field level
studies of flowering plants in orchards (Bugg and Wadd-
ington, 1994; Fitzgerald and Solomon, 2004; Irvin et al.,
2006; Yan et al., 1997), vineyards (Begum et al., 2006;
Berndt et al., 2006; English-Loeb et al., 2003; Nicholls
et al., 2000), and annual crop fields (Baggen and Gurr,
1998; Carmona and Landis, 1999; Forehand et al., 2006;
Hickman and Wratten, 1996; Jmhasly and Nentwig,
1995; Lee and Heimpel, 2005; Lee et al., 2001). However,
there is no reason to limit application to these scales and
indeed several studies suggest that habitat management
may need to be practiced at larger landscape scales in
order to maximize its benefits (Gurr et al., 2003).
3.3. Maximizing ecosystem services
Some measurable ecosystem services can be provided
from plot and perhaps even field-level habitat management
practices. These include the addition of floral strips which
provide enhanced biological control to individual fields
or vineyards (Berndt et al., 2002; Jacometti et al., 2007).
The latter approach has begun in New Zealand at the scale
of vineyards through the valley (see Section 4.2). However,
in landscapes in which management is more fully inte-
grated, the role of these habitats in providing a wider range
of ecosystem services becomes clear. For example, many
existing land uses within managed landscapes could be
modified to serve multiple roles. The potential incorpora-
tion of appropriate flowering plants to enhance natural
enemy populations in soil and water conservation practices
such as filter strips, riparian buffer strips, and hedgerows in
agricultural landscapes is an obvious choice (Bugg et al.,
1998; Henry et al., 1999; Lovell and Sullivan, 2006). Like-
wise, existing roadside vegetation which is frequently a
source of weed and disease pressure may be converted to
more suitable plant species with multiple benefits of pest
suppression, increased rural beauty, and less frequent
maintenance. In urban and suburban landscapes, many
types of green space could be utilized to include plants that
not only serve these goals but also support abundant natu-
ral enemies that contribute to pest management. Finally,
habitats where natural and managed areas interface pro-
vide a unique opportunity to meet multiple goals by cou-
pling biodiversity conservation with increased biological
pest suppression.
Viewed in this way, it is not difficult to imagine signifi-
cant proportions of managed landscapes containing plants
that enhance natural enemy function as well as providing
additional services. The New Zealand example (Section
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271 263

Table 3
Ecosystem services with examples of publications relating to provision of these services from habitat management
Ecosystem service Habitat management studies
I. Supporting services
Soil formation Altieri (1999), Gurr et al. (2003), Nicholls and Altieri, 2004, Pfiffner and Wyss, 2004
Photosynthesis
Primary production
Nutrient cycling
Water cycling
II. Provisioning services
Food Altieri (1999), Bugg et al. (1998), Landis et al. (2000), Nicholls and Altieri, 2004
Fiber
Genetic resources
Biochemicals, natural medicines, pharmaceuticals
Ornamental resources
Fresh water
III. Regulating services
Air quality regulation Altieri (1999), Bugg et al. (1998), Denys and Tscharntke (2002), Gurr et al. (2003),
Climate regulation Kinross et al. (2004), Landis et al. (2000), Nicholls and Altieri (2004), Pfiffner and
Water regulation (flooding, recharge) Wyss (2004)
Erosion regulation
Water purification and waste treatment
Disease regulation
Pest regulation
Pollination
Natural hazard regulation
IV. Cultural services
Cultural diversity Bugg et al. (1998), Frank and Shrewsbury (2004), Gurr et al. (2003), Kinross et al.
Spiritual/religious values (2004), Shrewsbury et al. (2004)
Knowledge systems
Educational values
Inspiration
Aesthetic values
Social relations
Sense of place
Cultural heritage values
Recreation
Eco and Agro tourism
Typology of ecosystem services is based on Reid et al. (2005).

4.2) shows current progress in this area. In the following agement services, can actually deliver a wide range of
sections we outline the types of benefits that may be derived ‘stacked’ ecosystem services, some of which are not pro-
from such approaches. vided by introduced species (Fig. 2).

3.3.1. Supporting services 3.3.2. Provisioning services

Habitat management could contribute to a variety of
supporting services (Table 3). If conducted at sufficiently
large scales, enhancement of habitats aimed at natural
enemy effectiveness could contribute to soil formation,
photosynthesis, primary production, nutrient cycling, and
water cycling in ways that other pest control practices can-
not. While these attributes have been pointed out by sev-
eral authors (Altieri, 1999; Gurr et al., 2003; Nicholls and
Altieri, 2004; Pfiffner and Wyss, 2004), they have not been
explicitly incorporated into habitat management research
efforts, as indicated by the limited ecosystem services
considered in plant selection. Using plants endemic to a
country to provide, initially, a limited range of pest-man-
In contrast, the ability of habitat management to
enhance provisioning services has received more attention
in habitat management research. Specifically, several
authors have suggested a role for the plants or plant
communities they established to provide food, fuel, or
ornamental resources (Frank and Shrewsbury, 2004;
Gurr et al., 2003; Lövei et al., 1993). Conservation of
genetic diversity in crop plants is well recognized (Negri,
2005), but incorporation of local genotypes of non-crop
plants could also increase genetic diversity in agricultural
systems. Plants with medicinal uses may also be incorpo-
rated into habitat management and harvested to provide
a direct provisioning service (Gurr et al., 2003). Increased
264 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271
Weed suppression
Biological control – insect pests
Biological control – disease
Biological control – ant/mealybug/virus
Conservation (related species)
Conservation (plant)
Erosion control
Eco-tourism
Reduce “greenhouse gases”
Aesthetics
“Kaitiakitanga” (cultural value)
Vine devigoration
Nutrient cycling
Soil water retention
Soil organic carbon
Soil biological activity
Fig. 2. ‘Stacked’ ecosystem services which may be provided by habitat
management plantings. Services that are offset to the right are not
provided by introduced species.
interest in biofuels provides a near-term opportunity for
increasing provisioning services via habitat management.
For example, switchgrass (Panicum virgatum L.) is con-
sidered a promising candidate for alternative energy pro-
duction in the US. Roth et al. (2005) concluded that
managed harvest of switchgrass could be compatible with
benefits to various grassland nesting birds. In many con-
texts, switchgrass could be grown in mixed culture with
prairie forbs, several of which have recently been shown
to be highly attractive to natural enemies (Fiedler, 2006).
Thus, it appears that biofuel production could be man-
aged for multiple benefits including increased biocontrol.
Alternatively, if approached inappropriately it could also
contribute to environmental degradation (Raghu et al.,
2006). The provision of ecosystem services by biofuel
crops can be an important factor influencing the eco-
nomic viability of this approach to energy production
(Sandhu et al., 2007b). The insights of biocontrol scien-
tists should continue to be added to this emerging
debate.
3.3.3. Regulating services
The primary role of habitat management is to provide a
specific regulatory service, i.e., pest regulation. However,
its potential role in other regulating services that ecosys-
tems can provide could be strengthened. Specifically, the
ability of agroecosystems to reduce erosion, improve activ-
ity of soil biota, and regulate water runoff and recharge
have been previously outlined (Nicholls and Altieri,
2004). Potential benefits of pest management schemes for
wildlife conservation and biodiversity, as well as habitat
connectivity, have also been considered (Kinross et al.,
2004). These benefits, however, could further be augmented
by linking with conservation incentive programs, e.g., Con-
servation Reserve Program (CRP) in the US (Landis et al.,
2000; Menalled et al., 2001), and agri-environment schemes
in the EU that already seek to provide other regulatory
services.
Biodiversity and regulatory ecosystem services are
tightly linked. The positive correlation between pest con-
trol and landscape diversity is well known (Bianchi et al.,
2006; Kleijn and van Langevelde, 2006; Marino and Lan-
dis, 1996; Menalled et al., 1999); however, it has not been
fully exploited in agri-environment schemes. For example,
in the US, the CRP and the Conservation Reserve
Enhancement Program (CREP) are funded through the
US Department of Agriculture. The CRP provides annual
rental payments and cost-sharing for agricultural landown-
ers to establish long-term resource conserving land covers,
and the CREP is similar, but targeted for ‘‘environmentally
sensitive land” (USDA, 2006). The primary anticipated
benefits include erosion prevention, water regulation, and
provision of wildlife resources, (USDA, 2006) with little
emphasis on pest regulatory services. In the EU, agri-envi-
ronmental schemes also are geared towards maintenance
and restoration of biodiversity and natural resource protec-
tion in farmlands. Twenty-six of 44 European countries
provide compensation for steps farmers take on their land
towards increasing biodiversity or benefiting the environ-
ment (Kleijn and Sutherland, 2003). To date, these prac-
tices have had mixed effects on ecosystem services and
biodiversity both in the US (Lovell and Sullivan, 2006)
and EU (Kleijn et al., 2006). They could, however, be mod-
ified to provide a suite of regulating, provisioning, support-
ing, and cultural services. With proper incentives it is not
difficult to envision such programs creating large-scale net-
works of woody species designed to reduce wind erosion,
provide wildlife habitat, and store large amounts of car-
bon, as well as containing flowering plants to enhance bio-
logical control in the surrounding landscape. Similarly, one
can imagine networks of interconnected wetlands, filter
strips, and riparian buffers that serve multiple roles: pro-
tecting against flooding hazards, increasing groundwater
recharge, decreasing nutrient and fertilizer runoff, and puri-
fying water, all while containing plants that also enhance
natural enemy function. Areas with added appropriate
plant biodiversity can also lead to greater soil porosity
and lower water content. These factors are known to
increase the populations of methanotroph bacteria in soils.
These bacteria oxidize methane. As this gas contributes to
global warming by a factor twenty-one times that of car-
bon dioxide (w/w), enhancing activity of these bacteria
has potential well beyond a particular cropping system
(Price et al., 2004).
3.3.4. Cultural services
Provision of cultural services through habitat manage-
ment has only begun to be explored; however, the possibil-
ities are extensive. Where indigenous peoples are living in
changing landscapes, preservation of native plants for
medicinal, cultural, or religious purposes is often critical
and these uses could be paired with habitat management
goals. The aesthetic value of the flowering plants used in
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271
habitat management has been noted (Ellis et al., 2005;
Frank and Shrewsbury, 2004; Rogers and Potter, 2004;
Shrewsbury et al., 2004). Few researchers, however, have
explicitly considered the potential impact of large displays
of native plants on human enjoyment of the landscape or
the potential to enhance eco- or agro-tourism. Below, we
examine two case studies where a more broad-based set
of ecosystem services have been considered in the context
of habitat management research.
4. Case studies
4.1. Michigan native plants to enhance multiple ecosystem
services
In 2003, a series of studies was initiated to screen native
plants for potential use in habitat management in southern
Michigan US (Fiedler, 2006; Fiedler and Landis, 2007a,b).
The primary crops produced in this area include corn, soy-
bean, wheat, and alfalfa and the landscape ranges from
highly simplified to very diverse (Menalled et al., 1999).
While wooded non-crop habitats persist in the form of for-
est remnants and woodlots, prairie and oak savanna eco-
systems that were once common in the region have been
almost completely lost from the landscape (O’Connor,
2006), primarily due to their historic ease in conversion
to agriculture (Hoekstra et al., 2005). Because these ecosys-
tems were structurally similar to open crop fields (prairies)
and orchards (savannas) we felt species that historically
grew in these communities may be particularly suitable
for habitat management. In addition, prairie and oak
savanna ecosystems are the target of extensive restoration
efforts and thus habitat management using species from
these communities has the potential to add to conservation
goals over broad spatial scales. If subsets of these plants
prove effective at enhancing natural enemies, farmers may
have an economic reason for preserving and restoring rem-
nant habitats or for re-creating similar communities on
their farms. Likewise, organizations involved in natural
areas restoration may gain better cooperation from adja-
cent landowners if the natural communities they are con-
serving have been shown to have benefits for important
natural enemies. Finally, because of their rarity in modern
landscapes, prairie and savanna plants have aesthetic and
cultural values that are highly prized by many individuals.
With these considerations in mind, we established exper-
iments to address whether prairie and savanna plants
native to the Midwestern US were as attractive to natural
enemy arthropods as widely researched non-native plants
(Fiedler and Landis, 2007a,b). In consultation with a native
plant nursery owner, we selected forty three species of
native perennial plants to contrast with five of the most fre-
quently recommended non-native annual plants for habitat
management: F. esculentum (cv. Mancan), V. faba (cv.
Windsor), C. sativum (Spice coriander), A. graveolens (cv.
Mammoth), and L. maritima (cv. Snow Crystals). From
May to October 2005, we vacuum-sampled arthropods
265
from 5 blocks of 1m2 single-species plots arranged in a ran-
domized complete block design at the Michigan State Uni-
versity Entomology Farm, East Lansing, Michigan, US.
This study identified 24 native perennial species of particu-
lar promise for habitat management in the Midwestern
USA (Fiedler and Landis, 2007a).
In order to directly test the hypothesis that native plants
could be as or more attractive to natural enemies than non-
natives, we analyzed a subset of these 24 plants, selecting
only those whose bloom periods directly overlapped those
of the previously recommended non-natives in the field.
For all plants, natural enemy abundances were averaged
over three weeks and log (x + 1) transformed to homoge-
nize variances. We performed an ANOVA and LS means
comparisons to compare plant species attractiveness to nat-
ural enemies in mid-July, early-August, and late-August.
Block was a random factor and plant species a fixed factor
(PROC MIXED, SAS Institute, 2003). Of note is the fact
that the annual non-natives were only in full bloom during
mid to late summer, while individual native species (not
included in this analysis) bloomed from May through Sep-
tember (Fiedler and Landis, 2007a).
We observed significant differences among plant species
in mid July (F3, 12 = 12.4, P < 0.01) and late August
(F4, 13 = 16.3, P < 0.001), but not in early August
(F2, 8 = 0.3, P = 0.76). In mid-July, both native species,
Potentilla fruticosa auct. non L. (shrubby cinquefoil) and
Apocynum cannabinum L. (Indian hemp), were significantly
more attractive to natural enemies than either non-native
V. faba or C. sativum (Fig. 3a). In early August, there
was no significant difference between the native species
and the non-native F. esculentum (Fig. 3b). In late August,
the native Eupatorium perfoliatum L. (boneset) was signifi-
cantly more attractive to natural enemies than any other
plant species, including non-natives L. maritima and
A. graveolens (Fig. 3c). In this plant group, native Monarda
punctata L. (horsemint) and non-native L. maritima
showed no significant difference in attractiveness to natural
enemies. All plant species were significantly more attractive
to natural enemies than non-native A. graveolens.
This subset of the larger study (Fiedler, 2006) illus-
trates that screening even a modest number of native
plants can reveal species that attract equal or greater
numbers of natural enemies than the five most frequently
recommended plants in the habitat management litera-
ture. In addition, because of our initial selection criteria,
these species have the potential to enhance multiple eco-
system services beyond pest suppression. By including
native plant producers, conservation organizations, and
farmers in our project we have developed a broad base
of interest and support. Our project field days in 2005–
06 drew over 220 individuals including significant num-
bers of non-agricultural clientele, suggesting that broaden-
ing our approach also broadened its appeal to the public
(http://www.nativeplants.msu.edu). We anticipate that
working to build this coalition will aid in implementation
of these practices in the future.
266 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271

50 services in such habitats is now at a low level. However,

a. mid July a large-scale program funded by the New Zealand govern-
A Native
40
A Non-native ment is addressing these problems by carefully returning
appropriate endemic biodiversity to the vineyard land-
30 scape. This work is taking place in several key New Zea-
B land vineyard regions, between latitudes 35 and 45S. The
20 key site is the Waipara region, north of Christchurch in
C the South Island of New Zealand. Here, the work began
10 by enhancing biological control of the light-brown apple
moth, Epiphyas postvittana (Walker) by drilling the non-
0 New Zealand natives buckwheat (Fagopyrum esculentum),
sa m m
faba rutico abinu ativu phacelia (Phacelia tanacetifolia) and alyssum (Lobularia
Vicia tilla f cann um s
ia dr
Mean number of natural enemies / m2 + SE

t e n n u m n
Po Ap o c y C o r
maritima) (Fig. 4). Nectar provision by these plants
30 increases the fitness of a key parasitoid wasp (Dolichogeni-
b. early August dea tasmanica (Cameron)). This work, details of which can
25 A
A be found in Berndt and Wratten (2005) and Berndt et al.
20 A (2006) increases mortality of the pest to such an extent that
its populations are brought below the economic threshold.
15 The work has progressed beyond enhancing one ecosystem
service, that of biocontrol of a pest, to the use of New Zea-
10
land endemic plants to provide a suite of ecosystem services
5 associated with the vineyard. Such plants, when mulched,
can disrupt the life cycle of grey mold (Botrytis cinerea
0 Pers.) such that infection levels on the grapes are below
m a
lentu innat ea a
lba the economic threshold. Other ecosystem services provided
um escu ida p Spira
opyr Ratib by endemic plants in these vineyards include weed suppres-
Fag
250 sion, maintenance of soil moisture, enhancement of meth-
c. late August A ane-oxidizing bacteria (methonotrophs), conservation (of
200 the plants themselves and of insects and invertebrates asso-
ciated with them) and even ecotourism. Some of the key
150 Waipara vineyards are creating ‘biodiversity trails’ along
which visitors can take part in self-guided, educational
100 walks (http://www.waiparawine.co.nz).
B
B
C
50 5. Conclusions
D
0 Field studies of habitat management to enhance biocon-
ta
uncta perfoliat
um liatum olens ritima trol of pests have about a 20-year history and in that time
a r da p m iu m perfo um grave laria ma
n iu r h b u
Mo Silph Eupa
to Anet Lo major achievements have been made in understanding the
Plant species role of plant-provided pollen, nectar, shelter and alterna-
tive hosts in enhancing natural enemy effectiveness (Gurr
Fig. 3. A comparison of attractiveness of native and non-native Michigan
and Wratten, 2000; Landis et al., 2000; Wade et al., in
plants flowering at similar times. Bars with different letters are significantly
different (LS means, a = 0.05). There was no significant difference among press). These studies have naturally focused on exploring
plant species in early August. improved efficacy of natural enemies and have relied in
large part on a very limited set of plants that have proven
effective under varying conditions. These studies have been
4.2. New Zealand native plants to enhance multiple very helpful in elucidating the theory and practical consid-
ecosystem services: an example from vineyards eration in habitat management but have for the most part
not explored the additional benefits of the technique. Spe-
Most vineyards in the world occupy Mediterranean lat- cifically, ecosystem services beyond pest suppression have
itudes which originally held high levels of biodiversity. seldom been formally incorporated into habitat manage-
Apart from the Mediterranean basin, these areas include ment research. Society is increasingly recognizing the inter-
parts of Chile, California, South Africa, Australia and connectivity of its managed and natural landscapes and
New Zealand. Vineyards typically are extreme monocul- seeks to preserve and enhance the ecosystem services
tures with little remaining native vegetation, a suite of derived from both. Habitat management research, initially
introduced weeds, high herbicide use and high inputs of focused on biocontrol enhancement, stands poised to take
other agricultural chemicals. The provision of ecosystem advantage of this increased awareness in ways that can pro-
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271 267

Fig. 4. Phacelia tanacetifolia in a New Zealand vineyard to enhance biological control of leafroller caterpillars. Photo by Jean-Luc Dufour.

duce ‘stacked’ ecosystem services to provide multiple bene-
fits for society.
Our analysis indicates that relatively few plants have
been evaluated for use in habitat management and of those,
just a few species have received the most attention. We sug-
gest that increased screening of plants for multiple benefits
should be a high priority of future research. Specifically,
plants native to the region of study should be emphasized,
as these are most likely to have potential to provide addi-
tional ecosystem services. Perennial species, while requiring
additional effort to establish and screen, also may lead to
increased provision of ecosystem services. Finally, because
significant proportions of the world’s flora have localized
distributions there is unique opportunity for scientists
worldwide to contribute to this effort. Local plants may
well provide the best solutions to local needs in terms of
both habitat management and provision of ecological
services.
A central problem in implementing any pest manage-
ment practice is that land managers typically require that
the practice pay for itself in terms of reduced pesticide
use, reduced labor, or increased yield and quality or
improved markets for their products. This has proven
to be a difficult standard to achieve for habitat manage-
ment. As pointed out by Gurr et al. (2003) there is a
hierarchy of biocontrol-related benefits that can be
achieved from habitat manipulation. This hierarchy
incorporates steps which are increasingly difficult to
achieve. The stages are:
1. Natural enemies aggregate on the flowers (pollen and/or
nectar provision, mating platforms, shelter etc.
268 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271
2. The fitness (fecundity, longevity, sex ratio, searching
behavior etc.) of individual natural enemies increases.
3. Parasitism/predation rate increases.
4. Prey/host populations are reduced.
5. Prey/host populations are reduced below the economic
threshold.
However, if the non-biocontrol ‘stacked’ ecosystem ser-
vices are added, achieving the final and most difficult part
of that hierarchy (reducing variable costs) becomes one
of several goals. The usual challenges remain at that stage,
too, however. These include grower adoption (Warner,
2006) and the extent to which the state should be involved
in ameliorating the external costs of agriculture (Pretty
et al., 2001) through fiscal legislative instruments, subsidies,
or other, more persuasive, rather than direct monetary
practices. There is evidence that consumers exhibit a clear
willingness to pay for such environmental improvements.
Carbon taxes, carbon credits and other monetary practices
add to this range of options for effecting change at the fed-
eral or international level (Takatsuka et al., 2005).
Conducting such research may require expanding tradi-
tional partnerships. Including stakeholders such as conser-
vation and land stewardship organizations in the initial
design of the research may help ensure that long-term goals
for multiple ecosystem services are met. Similarly, if native
plants are a focus of the research, incorporation of native
plant producers provides a natural synergy. These entre-
preneurs may be the best source of local plant materials
and genotypes. These groups are often eager to collaborate
as they ultimately stand to benefit from the increased use of
their products. Finally, incorporating land managers in the
research design is critical, as ultimately they will have final
control over implementation (Sandhu et al., 2007a; War-
ner, 2006). Broadening the research agenda may also open
new avenues for funding. By explicitly recognizing and
seeking out win-win scenarios (Rosenzweig, 2003) within
the context of ecosystem services, biological control
researchers may find their proposals and projects appealing
to a broader suite of funding agencies. This, however, will
probably require a shift on the part of habitat management
researchers from primarily considering the pest suppression
service of their work to adopting a broader perspective
including synergies with other ecological services (see Sec-
tions 4.1 and 4.2).
Maximizing ecosystem services through habitat manage-
ment will probably require implementing these practices
over much wider landscape and ecosystem service scales
than have currently been attempted. This can be accom-
plished by addressing a target landscape and asking where
habitat management practices best fit and how they can
accentuate ecosystem services. We suggest that habitat
management could be integrated into a wide range of land
use types to enhance a broad range of ecosystem services
with local, regional, national and global economic benefits.
Many landscapes already contain a variety of vegetated
habitats that could be managed for multiple purposes with-
out concern for losing land needed for production. For
example, in urbanized areas, parklands, green spaces, golf
course ‘‘roughs,” rain gardens, and home landscapes all
have the potential to be managed for multiple benefits.
Native plants may be reintegrated into suburban and rural
areas in the form of small-scale backyard restorations or
home landscaping with native perennials. A network of
such plantings could become a community resource with
educational possibilities near where humans live, work
and pursue recreation. In working landscapes, roadside
verges, utility rights of way, fencerows, woodlots, stream
corridors, and wetlands provide similar opportunities. At
present, providing for the needs of natural enemies is gen-
erally not part of the management plan for many of these
areas; however, with appropriate research on spatial
aspects, there is little biological reason it could not be.
Finally, high quality natural areas may provide core
reserves for many species in various landscapes, including
rare biota and pests’ natural enemies. Native plant restora-
tions may act as buffers around these areas to prevent deg-
radation of the conserved habitat while also enhancing
natural enemy activity in the surrounding working lands.
In conclusion, past biocontrol research has generally
approached habitat management as a stand-alone practice
aimed at providing a single ecosystem service, pest suppres-
sion. Society’s increasing understanding of the role of eco-
systems in providing a range of vital services to humankind
opens new avenues for habitat management research and
implementation. Broader views of the role of habitat man-
agement to not only enhance pest management but also to
contribute increased ecosystem services and reconnect peo-
ple to their surroundings may well contribute to the future
of this important component of conservation biological
control.
Acknowledgments
Michigan
We thank D. Richards and E. Knoblock for field re-
search assistance, G. Parsons, J. Steffen, and B. Nessia
for insect identification related to the native plant study,
and D. Sebolt and all Michigan-based undergraduate re-
search assistants for invaluable help with plant establish-
ment and maintenance. Plant expertise was provided by
B. Schneider and Wildtype Design, Native Plants & Seed,
Ltd. This study was funded by a Michigan State University
Plant Sciences Fellowship, an MSU Sustainable Agricul-
ture: Production and Food Ecology Systems Grant and
USDA NC SARE Project LCN 04-249.
New Zealand
We thank a large number of graduate students, post-
doctoral scientists and collaborators who helped generate
ideas and data for this paper and Professor Ross Cullen
who provided valued help with environmental economics
aspects. This work was largely funded by the New Zealand
Foundation for Research, Science and Technology (Con-
tract number: LINX 0303).
 A.K. Fiedler et al. / Biological Control 45 (2008) 254–271
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