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Ecological Engineering 81 (2015) 289297

Contents lists available at ScienceDirect

Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Mitigating net global warming potential and greenhouse gas intensities


by substituting chemical nitrogen fertilizers with organic fertilization
strategies in ricewheat annual rotation systems in China: A 3-year
eld experiment
Bo Yang a , Zhengqin Xiong a, * , Jinyang Wang a , Xin Xu a , Qiwei Huang b, * , Qirong Shen b
a
Jiangsu Key Laboratory of Low Carbon Agriculture and GHGs Mitigation, College of Resources and Environmental Sciences, Nanjing Agricultural University,
Nanjing 210095, China
b
Jiangsu Key Laboratory of Organic Solid Waste Utilization, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing
210095, China

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 30 October 2014
Received in revised form 18 March 2015
Accepted 9 April 2015
Available online xxx

A 3-year eld experiment was conducted to investigate the effects of different organic fertilization
strategies for ricewheat annual rotation systems on net global warming potential (net GWP) and
greenhouse gas intensity (GHGI) by incorporating methane, nitrous oxide emissions, the changes in soil
organic carbon (SOC) derived from the net ecosystem carbon budget (NECB), and the CO2 equivalent
emissions from manure and chemical nitrogen (N) fertilizer manufacturing. Six fertilization strategies
were studied, including control (CK), N fertilizer (CF), pig manure compost + N fertilizer (MC), straw + N
fertilizer (SC), straw + pig manure compost + N fertilizer (SM), and straw + straw-decomposing
inoculant + N fertilizer (SI). The results indicated that the application of organic amendments did not
change the seasonal pattern of GHG emissions but signicantly affected their seasonal quantities.
Averaged over the 3 cycles, the annual SOC sequestration rates contributed signicantly to the net GWPs
and were estimated to be 1.01 t C ha1 yr1 for the control and 1.131.27 t C ha1 yr1 for the fertilized
plots. Compared to CF, the MC strategy signicantly increased SOC while had similar size of net GWP and
GHGI, thus deserving recommendation regarding sustainable soil productivity and GHGs mitigations.
However, the other proposed organic strategies of SC, SM, and SI signicantly increased net GWP and
GHGI as well as SOC thus requiring further researches for GHGs mitigations. Therefore, we recommend
that the application of manure substituting half chemical fertilizer be an effective strategy while straw
returning in any currently studied strategies should be re-examined in the ricewheat annual rotation
system.
2015 Published by Elsevier B.V.

Keywords:
Soil carbon sequestration
Net ecosystem carbon budget (NECB)
Net global warming potential
Greenhouse gas intensity (GHGI)
Organic amendment
Rice agriculture

1. Introduction
Producing sufcient food to sustain the huge global population is
a priority for both governments and scientists. Rice (Oryza sativa L.)
and wheat (Triticum aestivum L.) are the worlds two most important
cereal crops and together contribute 45% of the digestible energy
and 30% of the total protein in the human diet (Timsina and Connor,
2001). There are 13 million hectares of ricewheat crop rotation
systems in China, which are predominantly located in the provinces
of Jiangsu, Anhui, Hubei and Sichuan along the Yangtze River Valley

* Corresponding authors. Tel.: +86 25 84395148; fax: +86 25 84395210.


E-mail addresses: zqxiong@njau.edu.cn (Z. Xiong), qwhuang@njau.edu.cn
(Q. Huang).
http://dx.doi.org/10.1016/j.ecoleng.2015.04.071
0925-8574/ 2015 Published by Elsevier B.V.

(Ma et al., 2009). The high level of crop production in China has been
obtained by increasing the use of fertilizers (Ju et al., 2009), and the
input of chemical nitrogen (N) fertilizer in the ricewheat rotation
system is as high as 550600 kg N ha1 yr1 (Zhang et al., 2012).
Chemical fertilizers have many advantages over organic manure
due to the solubility of the nutrients and their immediate
availability to plants as well as lower price and lower labor
requirements for their application. However, the excessive use of N
fertilizers may actually result in decreased N utilization efciency in
the crops (Vanlauwe et al., 2011) and also contribute to on-site land
degradation (Guo et al., 2010), nutrient pollution and eutrophication (Howarth et al., 2011; Liu et al., 2014) and the greenhouse gas
(GHG) emissions such as N2O (Hoben et al., 2011).
Organic fertilizers, such as farmyard manure and crop residues,
have long been proposed worldwide in agriculture to help to

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B. Yang et al. / Ecological Engineering 81 (2015) 289297

reduce dependence on synthetic chemical fertilizers as well as to


counteract soil degradation (Odhiambo and Magandini, 2008).
However, long-term or heavy application of organic fertilizers may
adversely affect plant growth (Jannoura et al., 2014), soil organisms
(Amin et al., 2013), water quality (Wang et al., 2008) and GHG
emissions such as CH4 (Datta et al., 2013). Traditional organic
inputs such as crop residues and animal manures cannot meet crop
nutrient demands for high yielding due to their low nutrient
contents. These will inevitably lead to adaptive strategies of
optimizing organic and inorganic fertilization to realize maximum
yield with minimal environmental costs, particularly GHG
emissions (Hillier et al., 2012).
The three GHGs associated with agriculture are CH4, N2O and
CO2. It is estimated that ca. 1012% of total global anthropogenic
emissions, or between 5120 and 6116 Mt CO2-equivalents, can be
attributed to direct agricultural GHG emissions in 2005. The
technical potential of the agricultural sector for mitigation is
considered to be substantial as high as 5.56.0 Pg CO2 equivalents
yr1 by 2030 (Smith et al., 2008). While the net emission of CO2
equivalents can potentially be decreased by increasing the soil
organic carbon (SOC) and/or decreasing GHG emissions. However,
there are complex trade-offs between SOC sequestration and GHG
emissions. For example, soil carbon sequestration from balanced
fertilizer inputs may be offset by increased GHG emissions (Shang
et al., 2011). Recently, greenhouse gas intensity (GHGI) has become
widely adopted as a means to relate the net global warming
potentials (GWP) with crop yields (Mosier et al., 2006; Zhang et al.,
2012). Thus, the trade-offs among improved soil health, yield,
carbon sequestration and GHG mitigation should be taken into
account when considering the substitution of organic amendments for mineral fertilizers.
However, the method for measuring SOC is not sensitive
enough to detect seasonal or annual changes (Zheng et al., 2008).
Recently, Zhang et al. (2014) reported that net ecosystem carbon
budget (NECB) is an alternative method for estimating SOC
changes after comparing to SOC changes over a 5-year eld
experiment. The NECB approach, which provides a simplied,
chamber-based technique for calculating changes in SOC on the
crop seasonal time scale, is particularly important for newly
established eld trials (Jia et al., 2012; Ma et al., 2013). The extent to
which the NECB, net GWP, and GHGI can be reduced by the
different organic fertilization strategies in comparison with
conventional chemical fertilizers in paddy eld remains unclear.
We hypothesize that: (1) different combinations of organic
fertilizer with chemical fertilizer may achieve comparably high
grain yields by providing the same amount of nutrients; (2)
different combinations of organic fertilizer with chemical fertilizer
may increase SOC sequestrations and offset the probable effects on
extra emissions of CH4 and N2O. The desired outcome is that the
results can be used to assess options of using agricultural wastes as
resources for maintaining soil fertility, improving crop yields and
mitigating greenhouse effects. Therefore, a eld experiment was
established in 2011 to gain insight into the effects of combining pig
manure compost and/or crop residues with chemical fertilizer on
soil C sequestration rates, GHG emissions and net GWP and GHGI
over three cycles of ricewheat annual rotations and to nd
feasible mitigation strategies utilizing agricultural wastes for
sustainable agriculture.
2. Materials and methods
2.1. Experimental sites
A eld experiment was performed in a typical ricewheat
rotation system from June 27, 2011 to May 18, 2014. The station was
located in Baimao Village (31320 N, 120 550 E), Suzhou City, Jiangsu

Province, China, which lies in the center of the Yangtze River Delta
in eastern China in the northern subtropical humid climatic zone.
The main cropping system is ooded rice and drained wheat on an
annual rotation. Soil samples from a depth of 020 cm were
collected in 2011 after the wheat was harvested for the analysis of
physicalchemical characteristics. The soil is classied as a uvisol
with a bulk density of 1.20 g cm3, a pH (1:2.5, H2O) of 7.60, a SOC
of 11.6 g C kg1, a total N of 2.30 g kg1, an available P of 39.0 mg
kg1 and an exchangeable K of 74.3 mg kg1. The monthly average
air temperature and precipitation during the three ricewheat
rotation cycles from 2011 and 2014 are shown in Fig. 1.
2.2. Field experimental treatments and crop management
The eld experiment was conducted in a randomized complete
block design of six treatments (see Table 1) with four replicates.
Each plot was 6.4 m  7.2 m, and adjacent plots were separated by
concrete ridges (30 cm width) with plastic covering. The blocks
were separated by irrigation furrows (50 cm width) and two ridges.
The treatments included control (CK), N fertilizer (CF), pig manure
compost + N fertilizer (MC), straw + N fertilizer (SC), straw + pig
manure compost + N fertilizer (SM), and straw + straw-decomposing inoculant + N fertilizer (SI) and are listed in detail in Table 1. For
the SM and SI treatments, the chopped straw of the previous crop
was incorporated into the top 20 cm of the soil at a rate of 3 t ha1
by ploughing. A straw-decomposing inoculant containing actinomycetes, lactic acid bacteria, bacillus, photosynthetic bacteria and
yeast (Xin Tiandi biological fertilizer Engineering Center Company,
Yixing, Wuxi, China) was sprayed onto the soil surface for the SI
treatment at a rate of 20.7 kg ha1.
Water management, fertilization and other managements in
this experiment followed local practices. The elds were submerged before the rice seedlings (cultivar Changyou 5) were
transplanted in late June. All of the remaining straw was removed
from the surface except in SC, SI and SM, and hand plowing to a
depth of 20 cm was carried out in late June. Subsequently, 23 rice
seedlings aged 25 days were transplanted to 1 hill in a 15 cm  20
cm space in the eld. All plots were kept ooded for approximately, 40 days after rice transplanting. The one week of mid-season
drainage was conducted before reooding followed by a dry
wet alteration without waterlogging till rice harvest. Approximately a month after the rice was harvested, winter wheat
(cultivar Yangmai 14) was seeded directly onto the soil surface
without mixing the seeds with the topsoil. There was no irrigation
during the period of wheat growth, so rainwater was the only
source of soil moisture. The wheat was harvested in late May.
The amounts of 240 kg N ha1 crop1 as the total of chemical
and organic fertilizers were applied to each crop of wheat and rice.
N fertilizer as urea was applied in four splits within each crop; 40%
was applied as basal fertilizer and 60% as supplementary fertilizer
during crop growth at 3, 6 and 9 weeks after rice transplantation
and 7, 13 and 16 weeks after wheat sowing. Also, calcium
superphosphate and potassium chloride were applied at 120 kg
P2O5 ha1 and 90 kg K2O ha1, respectively, as basal fertilizers to all
plots except the CK. All of the organic amendments (pig manure
compost and straw) were incorporated into the soil two weeks
before the transplanting of rice or the sowing of wheat for the
organic fertilizer application treatments. Only the basal fertilizers
were incorporated into the surface soil (015 cm), and the
topdressings were surface-broadcasted.
2.3. Chamber measurement of methane and nitrous oxide uxes and
ecosystem respiration (Re)
CH4 and N2O emissions and Re were determined simultaneously
and using the static-opaque chamber method described by

B. Yang et al. / Ecological Engineering 81 (2015) 289297

291

35

Temperature ( )

30
25

2011-20 12 (a nnu al mea n 17.1

2012-20 13 (a nnu al mea n 17.2

2013-2014 (a nnu al mea n 18 .9

20
15
10

5
0
2011-2012 (18 34.9 mm yr-1)

Precipitation (mm)

400

2012-2013 (19 09.5 mm yr-1)


300

2013-2014 (1926.4 mm yr-1)

200

100

Jun.

Jul.

Aug.

Sep.

Oct.

Nov .

Dec.

Ja n.

Feb.

Ma r.

Apr.

Ma y.

Month
Fig. 1. Monthly mean air temperature (a) and rainfall (b) during the three annual ricewheat rotation cycles from 2011 to 2014.

Ma et al. (2013) during the three annual ricewheat rotation cycles


from 2011 and 2014. Re includes the respiration of plants and soil
microorganisms. A PVC chamber frame, which covered an area of
0.25 m2, with a water groove on top was randomly inserted into the
soil to a depth of 15 cm and kept in the same position throughout
the entire observation period, except when it was removed for
necessary farming practices. The top chamber, which ts exactly in
the groove with a bottom area of 0.5 m  0.5 m and a height of
0.5 or 1.1 m (depending on crop growth and plant height), was
temporarily installed on the gas ux measurement frame. The
chamber was equipped with a circulating fan to ensure complete
gas mixing and was wrapped with a layer of sponge and aluminum
foil to minimize air temperature changes inside the chamber. The
chamber top included a small, silicon-sealed vent for sampling.
The chamber measurements were conducted weekly during the
crop growing season. Adjustments in sampling dates and

frequency were made to include specic events such as heavy


rainfall, irrigation, high temperature, fertilizer application or
tillage. Gas samples were taken between 08:00 am and
10:00 am. Four gas samples from the chamber head space were
collected with a 20 ml syringe at 0, 10, 20, and 30 min after the
chambers were placed on the xed frames. The air temperature
inside the chamber was monitored during gas collection. Fluctuations in water depth and soil temperature at a depth of 5 cm were
simultaneously monitored for each plot. Mixing ratios of CH4, N2O
and Re, were simultaneously analyzed within 24 h with a gas
chromatograph (Agilent 7890A) equipped with two detectors. N2O
was detected by ECD (electron capture detector), and CH4 was
detected by FID (ame ionization detector). Re was reduced with
hydrogen to CH4 in a nickel catalytic converter at 375  C and then
detected by the FID. Argon-CH4 (5%) and N2 were used as the
carrier gases for the ECD and FID, respectively at a ow rate of

Table 1
Field management for different treatments of N chemical fertilizer, straw residues, and manure compost application necessary to yield 240 kg N ha1 crop1 for all fertilized
plots in the three annual ricewheat rotations from 2011 to 2014.
Treatment
code

CK
CF
MC
SC
SM
SI
a
b
c
d

Rice

Wheat

Wheat
residue
t ha1

N chemical
fertilizer
kg ha1

Pig manure
compost
t ha1

0
0
0
3b
3
3

0
240
120
219.6
99.6
219.6

0
0
6a
0
6
0

Straw-decomposing
inoculant
kg ha1

Rice
residue
t ha1

N chemical
fertilizer
kg ha1

Pig manure
compost
t ha1

Straw-decomposing
inoculant
kg ha1

20.7d

0
0
0
3c
3
3

0
240
120
201.6
81.6
201.6

0
0
6
0
6
0

20.7

Pig manure compost was applied at 6 t ha1 and consisted of 120 kg N ha1 and 1.8 t C ha1.
Dry wheat residue (C:N ratio = 68) was applied at 3 t ha1 and consisted of 20.4 kg N ha1 and 1.4 t C ha1.
Dry rice residue (C:N ratio = 46) was applied at 3 t ha1 and consisted of 38.4 kg N ha1 and 1.8 t C ha1.
Contained actinomycetes, lactic acid bacteria, bacillus, photosynthetic bacteria and yeast.

292

B. Yang et al. / Ecological Engineering 81 (2015) 289297

40 ml min1. Both FID and ECD temperatures were operated at


300  C.The oven and column temperatures were maintained at
50 and 400  C, respectively.
2.4. Estimation of the NECB, net GWP and GHGI of the croplands
The method for the estimation of the NECB in short-plant
croplands is based on studies by Ciais et al. (2010),Smith et al.
(2010), Ma et al. (2013) and Zhang et al., (2014) as following:

manufacturing and transportation and is calculated by multiplying


the amount of chemical N fertilizer used in each treatment by a
factor of 8.3 t CO2-eq t1 N for China (Zhang et al., 2013). In
addition, GWPmanure indicates the CO2 equivalent emissions from
the manufacture of pig manure compost and is calculated as the
difference in organic carbon content before (395.7 g kg1) and after
(312.4 g kg1) composting (Hao et al., 2004; Fukumoto et al., 2011).
An overall GHGI was calculated as the gross net GWP divided by
the grain yield:
netGWP
yield

NECB Cin  Cout  NEE

(1)

GHGI

Cin Cmanure Cstraw

(2)

2.5. Statistical analysis

Cout CH4 Charvest

(3)

NEE Rh  NPP Rh  GPP  Ra Rh Ra  GPP


Re  GPP

(4)

GPP

NPP
0:52

NPP NPPgrain NPPstraw NPPlitter NPProot NPPresidual

(5)

(6)

where NEE is net ecosystem exchange; CH4 is the carbon emitted to


the atmosphere in the form of CH4; Cmanure and Cstraw denote the
carbon supplied to the soil by the pig manure and straw used in this
study; Charvest is the carbon removed by the harvest of the crops;
The ecosystem respiration (Re) of the cropland was the sum of crop
autotrophic respiration (Ra) and soil heterotrophic respiration (Rh);
GPP is gross primary production; NPP is net primary production,
where, NPPgrain is the carbon content in a grain of rice or wheat and
so on for the others. The grain and straw biomass NPP is converted
using the dry biomass weighed at harvest. Other components are
estimated using allometric relationships according to Huang et al.
(2007), in which the aboveground/root ratio was xed at 1.0/0.1 for
rice and 0.9/0.1 for wheat. Litter accounts for 5% of the
aboveground and root dry biomass (Kimura et al., 2004), and
rhizodeposits account for 15% (Mandal et al., 2008) and 18%
(Gregory, 2006) of the total biomass for rice and wheat,
respectively. The NPP/GPP ratio of 0.52 is deduced from the
resulting MODIS GPP and NPP product (Zhang et al., 2009).
Because only part of the NECB will eventually become
sequestered as soil carbon while a major part of the NECB will
decompose over the long term, we estimated the change in soil
organic C by converting NECB with Eq. (7) according to Cui et al.
(2013).

DSOC  162:8lnNECB  268:9

(7)

There are some hidden CO2-eq emissions from crop production, and one of the most important is the manufacture and
transportation of chemical N fertilizers. In this study, the net GWP
(kg CO2-eq ha1) of the croplands is calculated as the total CO2-eq
emissions from soil GHGs and agricultural fertilizer inputs minus
the change in SOC derived from the NECB (Ma et al., 2013).
netGWP

GWPCH4 GWPN2O GWPN GWPmanure  44


12  DSOC

(8)

Here, GWPCH4 and GWPN2O indicate the conversion of N2O and CH4
to equivalent CO2 on a 100-year time horizon (IPCC, 2007). GWPN
denotes CO2 equivalent emissions from chemical N fertilizer

(9)

In this paper, the CH4 and N2O uxes and Re rates for each
treatment on the sampling date were determined as the mean of
the four uxes from the four spatial replicates. The seasonal or
annual cumulative emissions of each gas were directly computed
from the measured uxes and were sequentially accumulated from
the emissions between every pair of adjacent measurement
intervals. The effective volume of the chamber was adjusted for
oodwater depth, and the temperature inside the chamber was
measured at each sampling. Seasonal and annual GHGs, grain
yields, NECB, net GWP, and GHGI resulting from fertilizer
application were examined by two-way analysis of variance
(ANOVA). Differences among treatments in seasonal CH4 and
N2O emissions, Re rates and grain yields were further examined
with Students multiple range tests. All statistical analyses were
carried out in JMP version 9.0, except that the multivariate analysis
was carried out using the SPSS software package for Windows
version 18.0. We report least-squared means and standard errors
with an n of 4. Statistical signicance was determined at the
0.05 probability level.
3. Results
3.1. CH4 emissions
The seasonal pattern of CH4 emissions varied with water regime
(Fig. 2a). The CH4 uxes were negligible during the wheat-growing
season (7.5018.04 kg C ha1). When the eld was waterlogged in
the rice season, CH4 uxes generally increased and peaked at
approximately 40 days after transplantation and then dropped off.
There were signicant differences in the rice seasonal patterns of
CH4 uxes; much higher emission peaks were observed in
2012 and 2013 than in 2011 (Fig. 2a).
Signicant differences in CH4 ux rates were observed among
years (p < 0.01) and treatments (p < 0.001), but the year  treatment interactions were not signicant as indicated by the results of
the ANOVA (Table 2). The highest CH4 daily ux emission rate came
from SC with a value of 69.10 mg C m2 h1, and the lowest was
from CK with a value of 1.96 mg C m2 h1 in the 2012 rice season,
which is an approximately 35.3-fold difference (Fig. 2a). In
comparison with CK (64.10 kg C ha1) with an organic amendment,
the seasonal cumulative CH4 emission was increased on average by
54%, 217%, 96% and 162%, for the MC, SC, SM and SI treatments,
respectively, during the three rice-growing seasons (Table 3).
3.2. N2O emissions
Nitrous oxide uxes showed a typical pattern throughout the
experimental period (Fig. 2b). Daily average emissions were
consistently low with the exception of some peaks. The effect of
fertilizer on daily N2O ux could be detected at each location
within a week of fertilizer application (Fig. 2b).

B. Yang et al. / Ecological Engineering 81 (2015) 289297

293

85

CH 4 flux (mg C m -2 h -1 )

CK

CF

MC

SC

SM

SI

70
55

40
25
10
-5
1190

N2 O flux ( g N m -2 h -1 )

990
790
590
390
190

-10
900

Re flux (mg C m -2 h -1 )

750
600
450
300
150
0
2011-06-27

201 1-12-27

201 2-06-27

201 2-12-27

201 3-06-27

2013-12-27

2014-06-27

Da te (yyy y-mm-dd )

Fig. 2. Seasonal variations in (a) CH4 uxes, (b) N2O uxes and (c) ecosystem respiration (Re) during the three annual ricewheat rotation cycles from 2011 to 2014. The arrow
indicates N fertilization.

the rice and wheat seasons amounted to 0.550.87 kg N ha1 and


1.872.64 kg N ha1, respectively, for the various fertilized plots
(Table 3).

Two-way ANOVAs indicated that total N2O emissions were


signicantly affected by the treatments and years but not by their
interactions (Table 2). The mean cumulative N2O rates were
calculated as 0.26 kg N ha1 in the rice season and 1.16 kg N ha1 in
the wheat season for the control plots, which was signicantly
lower (p < 0.01) than those for the fertilized plots. The highest N2O
emissions were observed from the SC plots with a value of 2.64 kg
N ha1. Much higher N2O emissions occurred during the wheat
season than during the rice season although substantial N2O
emissions were also observed in the rice growing period. Over the
three ricewheat annual rotations, seasonal N2O emissions from

3.3. Re rates and crop yield


Seasonal variations in Re uxes are summarized in Fig. 2c. As
expected, the additional contributions of autotrophic respiration
and the decomposition of cover crop residues increased cumulative Re (Table 3). Unlike other ecosystems, the biomass in crop
elds exhibits large seasonal changes, which affect ecosystem

Table 2
A two-way ANOVA of the effects of treatment (T) and year (Y) on CH4 and N2O emissions, ecosystem respiration (Re) and grain yields in the three annual ricewheat rotations
from 2011 to 2014.
CH4 (kg C ha1)

N2O (kg N ha1)

Re (t C ha1)

Yield (t ha1)

Crop season

Factors

df

SS

Rice

T
Y
TY
Model
Error

5
2
10
17
36

141781.8
19066.10
12885.93
173733.9
44566.42

22.91
7.70
1.04
8.26

<0.001
<0.01
0.43
<0.001

2.49
2.20
1.10
5.80
1.03

17.41
38.54
3.86
11.93

<0.001
<0.001
<0.01
<0.001

39.19
3.17
14.32
56.69
60.67

4.65
0.94
0.85
1.98

<0.01
0.40
0.59
<0.05

87.20
5.80
5.26
98.26
18.61

15.44
7.44
1.04
6.03

<0.001
<0.01
0.45
<0.001

Wheat

T
Y
TY
Model
Error

5
2
10
17
36

802.63
106.31
672.51
1581.46
390.95

14.78
4.89
6.19
8.57

<0.001
<0.05
<0.001
<0.001

15.47
6.87
1.82
24.16
6.49

17.17
19.07
1.01
7.89

<0.001
<0.001
0.45
<0.001

41.24
32.50
11.63
85.37
43.56

6.81
13.43
0.96
4.15

<0.001
<0.001
0.49
<0.01

30.55
0.57
2.62
33.73
8.47

25.97
1.21
1.11
8.43

<0.001
0.31
0.38
<0.001

Ricewheat
cycle

T
Y
TY
Model
Error

5
2
10
17
36

157782.3
21138.02
15202.05
194122.4
43863.68

25.90
8.67
1.25
9.37

<0.001
<0.01
0.30
<0.001

29.00
16.47
3.13
48.59
7.92

26.34
37.41
1.42
12.99

<0.001
<0.001
0.21
<0.001

153.35
18.49
25.40
197.23
124.52

8.87
2.67
0.73
3.35

<0.001
0.08
0.69
<0.01

216.01
3.95
9.94
229.90
20.39

76.26
3.49
1.75
23.87

<0.001
<0.05
0.11
<0.001

SS

SS

SS

294

B. Yang et al. / Ecological Engineering 81 (2015) 289297

Table 3
Seasonal CH4 and N2O emissions, ecosystem respiration (Re), and rice and wheat grain yields during the rice- and wheat-growing seasons in the three ricewheat cycles from
2011 to 2014.
Treatment

Rice season
CH4
(kg C ha1)

CK
CF
MC
SC
SM
SI

64.10
81.82
98.81
203.25
125.41
167.74








26.03d
31.05d
33.33cd
58.52a
20.45c
50.70b

Wheat season
N2O
(kg N ha1)

Re
(t C ha1)

0.26 
0.55 
0.66 
0.74 
0.79 
0.87 

7.68
9.21
9.67
9.80
9.35
10.12

0.12c
0.26b
0.28ab
0.30ab
0.38ab
0.41a








0.38b
1.03ab
1.32a
1.29a
0.91ab
2.08a

Yield
(t ha1)
4.63
7.34
7.52
7.88
7.79
8.35








CH4
(kg C ha1)
0.69c
1.00b
0.92b
0.66ab
0.75ab
0.72a

7.50
10.92
18.04
16.18
15.90
16.06








3.14c
4.71bc
7.02a
5.69a
0.91ab
5.48a

N2O
(kg N ha1)
1.16
1.87
2.40
2.64
2.10
2.48








0.33c
0.41b
0.65ab
0.89a
0.56ab
0.66a

Re
(t C ha1)
4.31
5.58
5.86
5.58
5.35
6.97








0.79c
1.17b
1.47ab
1.35b
0.84bc
2.15a

Yield
(t ha1)
1.94
3.25
3.93
4.02
3.65
3.68

 0.55c
 0.52b
 0.53a
 0.44a
 0.62ab
 0.46ab

Mean  SD; different lowercase letters within the same column indicate signicant differences among treatments over the three crop seasons from 2011 to 2014 (Students
multiple range tests, p < 0.05).

respiration. It is therefore reasonable to take changes in plant


biomass into account when discussing ecosystem respiration. Rice
yields ranged from 4.63 to 8.35 t ha1 while those of wheat ranged
from 1.94 to 4.02 t ha1 (Table 3). Treatment with straw-decomposing inoculant (SI) resulted in the highest rice yields. However,
no signicant difference was found in wheat yields among the four
organic treatments of MC, SC, SM and SI.
The daily Re ux was high during the summer crop cultivation
period and low during the winter period. The total Re uxes were
signicantly affected by the treatments but not by the years or
their interactions (Table 2). All of the fertilized plots signicantly
increased the total Re for both the rice and wheat seasons. The
seasonal Re emissions varied from 4.31 t C ha1 in the CK plots to
6.97 t C ha1 in the SI plots during the wheat season but varied from
7.68 t C ha1 in the CK plots to 10.12 t C ha1 in the SI plots during
the rice season (Table 3). For the three rotations in total, the
cumulative Re for the ve fertilized treatments was signicantly
greater (p < 0.05) than that of CK (Table 3).
While no difference between SC and CF, the addition of rice
residues along with straw-decomposing inoculant (SI) increased
emissions by 24.8% compared to the CF, which could partly be
attributed to increased respiration from straw decomposition
agent. Moreover, substitution of 50% inorganic N with organic N
through pig manure compost (MC and SM) did not signicantly
increase Re ux compared to the CF (Table 3).
3.4. NECB and soil organic C changes
A positive NECB value represents ecosystem carbon gain at the
crop seasonal scale in this paper. On average, a NECB with a value of
1.606.99 t C ha1 yr1 was observed during the wheat growing
period, which was higher than that of 1.375.43 t C ha1 yr1
during the rice growing period (Table 4). The CK treatment
produced the lowest average NECB. In terms of the annual rotation
system, the four organic fertilized treatments of SC, SI, MC and SM
produced larger positive NECB values of 7.51, 7.68, 9.07, and
12.42 t C ha1 yr1, respectively, than CF. The two treatments with
pig manure compost application, SM and MC, had signicantly
larger NECB values than SC and SI with SM being the largest among
the treatments (Table 4). A multivariate analysis showed that
NECB = 0.654  manure + 0.496  straw + 5.35  CH4  0.14  Re +
0.274  yield + 1235.28 (n = 144, p < 0.001 for factors of manure,
straw and yield, p < 0.01 for factors of Re and CH4), indicating the
apparent main components of the NECB in this system.
Similar to the pattern in NECB, the sequestration of soil C was
statistically higher in the four organic fertilization treatments in
both single crop seasons and annual rotations than in the CF
treatment (Table 4). In particular, the increased SOC in the SM
treatment was 1.26 and 1.12 times greater than that in the CK and
CF treatments, respectively. The SI treatment that received straw-

decomposing inoculant showed no signicant changes in C


sequestration compared to SC.
3.5. Annual net GWPs and GHGIs
The net global warming potentials, which account for all GHG
emissions, soil C sequestration, and fertilizer production, in the
annual rotations ranged from 0.37 t CO2 ha1 yr1 in the CK to
+4.58 t CO2 ha1 yr1 in the SC. The annual net GWP was negative
for the CK eld treatment, suggesting that the C sequestration
exceeded the CO2-equivalents emissions without application of N
fertilizer and compost (Table 4).
The GWP due to chemical N fertilizer application ranged from
3.98 t CO2 ha1 yr1 in the CF to 1.65 t CO2 ha1 yr1 in the SM while
being 3.67 t CO2 ha1 yr1 in the SM and MC treatments due to
manure application. Although organic amendments increased N2O
and CH4 emissions, they remarkably increased assimilated
atmospheric CO2 into the agro-ecosystems, namely through
changes in SOC (p < 0.01, Table 4). Thus, no signicant difference
in the net GWP between MC and CF was observed although it was
numerically higher in the MC. However, the net GWPs of the SC, SM
and SI treatments, which received straw, were signicantly
increased by about 15 folds, 5 folds and 12 folds, respectively,
compared to CF in the annual rotations (Table 4).
Although annual GHGIs were increased due to the different
fertilizer applications compared to CK, no signicant difference
was found between CF and CK over the whole rotation cycle.
Relative to CF, the GHGIs of the SM, SI and SC treatments receiving
straw were signicantly increased by 412 folds while the MC
treatment produced a comparable GHGI (Table 4).
4. Discussion
4.1. Best fertilization strategies to increase soil C sequestration
potential
Experience with the measurement of SOC in long-term
experiments has shown unavoidable variability in SOC and/or
the bulk density measurements in elds/plots as well as from
anomalies within plots that inuence SOC decomposition or soil
loss, so the detectable differences between treatments are typically
13 t C ha1 yr1 (Van den Bygaart et al., 2010). Here, we use the
NECB approach for the entire soilcropatmosphere system to
estimate soil carbon sequestration or loss over crop seasonal term.
Our hypothesis was that nutrients supplied via chemical fertilizers,
animal manures, and the return of straw would increase SOC by
increasing C inputs from enhanced plant productivity and organic
amendments returned to the soil. The estimates in the current
study generally supported this hypothesis. Although the results of
SOC sequestration in our study (1.011.27 t C ha1 yr1) were

0.15  0.03b
0.32  0.11a
1.65  0.50bc
3.76  1.21ab
3.67
0
SM
SI

SC

MC

CF

Mean  SD; different lowercase letters within the same column indicate a signicant difference at p < 0.05 (Students multiple range tests).
a
NPP = NPPgrain + NPPstraw + NPPlitter + NPProot + NPPresidual.
b
NECB = NPP / 0.52 + Cmanure + Cstraw CH4 Charvest Re.
c
DSOC 162.8 ln (NECB) 268.9.
d
Net GWP = GWPCH4 + GWPN2O + GWPN + GWPmanure 44 / 12  DSOC.
e
GHGI = net GWP / yield.

1.65
3.65
13.09  1.13ab 5.43  0.83a 6.99  0.85a
13.55  0.75a 3.33  1.54bc 4.45  0.84c
11.44  1.53bc
12.03  0.61a

12.42  0.81a 1.27  0.01a


7.78  1.52c
1.18  0.03c

0.39  0.21a
0
2.19  1.72cd
13.49  0.86a
11.90  0.73ab

5.32  0.49b 7.51  1.78c

3.65
1.18  0.05c

4.58  2.43a

0.09  0.11bc
3.67
1.22  0.02b 1.99
11.45  0.96abc 12.90  1.16ab 4.19  1.44ab

9.33  1.32b
5.14  0.86b

1.31  0.86cd

0.03  0.13cd
12.09  1.06b
10.59  0.99c

3.98

0
1.13  0.04d
2.71  0.63d 5.50  1.35d
2.79  1.28c

0.291.05de

0.08  0.13d
0.370.69e
7.60  0.93c
CK

71.60  27.68d

1.42  0.39c 11.99 


0.80c
92.74  34.62cd 2.42  0.61b 14.79 
1.55b
116.85 
3.06  0.86ab 15.53 
36.83bc
1.50ab
219.43 
3.38  1.04a
15.38 
58.43a
2.36ab
141.31  22.73b 2.89  0.86ab 14.70  1.65b
183.80  50.36a 3.35  0.97a
17.09  3.27a

6.57  0.91d

0
1.01  0.05e
2.97  0.79e
1.60  0.50e
1.37  0.90d

(t
(t
(t
(kg CO2eq kg1
CO2eq ha1 yr1) CO2eq ha1 yr1) CO2eq ha1 yr1) yield)
(t C ha1
yr1)
(t C ha1
yr1)
(t C ha1
yr1)
(t C ha1
yr1)
(t C ha1
yr1)
(t ha1 yr1)
(t C ha1
yr1)
(kg C ha1 yr1) (kg N ha1
yr1)

net GWPd
GWPmanure
GWPN

DSOCc
NECBrice
NECBwheat
NECBriceb
NPPa
Grain yield
Re
N2O
Treatment CH4

Table 4
Mean annual CH4 and N2O emissions, ecosystem respiration (Re), crop grain yield, NPP, NECB, DSOC, net GWP and GHGI over the three ricewheat cycles from 2011 to 2014.

wheat

GHGIe

B. Yang et al. / Ecological Engineering 81 (2015) 289297

295

generally greater than many studies (Schuman et al., 2002; Sun


et al., 2009), it still falls within the SOC sequestration rate in the
range of 0.132.20 t C ha1 yr1 estimated by Pan et al. (2003), who
evaluated the current SOC sequestration rates of China paddy soils
using the available data from national paddy soil monitoring sites
along with long-term pilot experiments. A number of other studies
have also shown similar results; the rate of SOC accumulation from
manure application was reported to be 0.961.43 t ha1 yr1 over
3 years in Hunan Province (Shang et al., 2011) and 1.03 g C kg1 yr1
over 20 years in Yunnan Province (Wang et al., 2005).
Management practices that lead to an increase in organic inputs
(manure and biomass) enhance microbial functions and promote
SOC sequestrations (Jarecki and Lal, 2003). Since addition of
organic amendment to soil means the addition of a source of extra
C, it is not surprise that SOC sequestration rates were greater in the
organic treatments. Moreover, the SM and MC treatments that
received manure sequestered more C compared to the straw
treatments of SC and SI due to higher C inputs as manure than
straw in the studied strategies (Table 4). Although the organic
amendments sequestered more carbon, the DSOC in the CF
treatment was positive (Table 4), indicating that the application of
chemical N fertilizer can also sequester carbon into the soil.
Possible reason is that chemical N fertilization increased the
above-ground and root biomass due to immediate and sufcient
supply of plant nutrients (Bostick et al., 2007). However, numerous
studies also have found that N fertilization does not signicantly
inuence SOC turnover (Dolan et al., 2006). The effects of N
fertilizer supply on SOC should greatly depend on the time extent
and we cannot derive simplistic assertion that application of
chemical fertilizer can increase soil carbon sequestration without
long-term eld observation.
4.2. Effect of alternative organic fertilization strategies on greenhouse
gas emissions
Numerous previous studies have demonstrated the inuences
of N supply on CH4 production, oxidation, transport and emission
(Cai et al., 2007). In our study no signicant difference in CH4
emission was observed between the CK and CF treatments
indicating no obvious effects of chemical N fertilizer on net CH4
exchange. However, in comparison with the control, CH4 emissions
were signicantly increased by the application of organic amendments (Table 2). Obviously, decomposition of organic matter was
the predominant source of the methanogenic substrates and thus
promoted CH4 production. The highest CH4 emissions were in the
SC and SI treatments that received straw. The application of straw
may also change soil microbial communities and alter their
activities, which would benet CH4 production (Watanabe et al.,
2010). It is noteworthy that CH4 emissions were less in the SM
which received the same amount of straw with the lowest
chemical fertilizer (Table 3). The possible reason is that the easily
decomposable substances in manure should have been utilized by
methanogenic bacteria during the pig manure composting process.
The underlying mechanisms were still complex due to the complex
mechanisms of chemical fertilizer, different organic sources and
microbial communities.
The seasonal patterns and intensities of N2O emissions in this
study were generally comparable to earlier measurements (Zou
et al., 2007; Qin et al., 2010). The synthetic N and organic
amendments led to a signicant increase in N2O emissions
(Table 3). Although there was no signicant difference between
the four organic treatments, the organic amendments led to higher
N2O emissions than the CF (Table 3). The N2O peaks occurred after
the second and third top dressings in the SC and SI treatments,
which can be attributed to the decomposition of crop residues. The
relatively high N2O emission factor of straw-N might be attributed

296

B. Yang et al. / Ecological Engineering 81 (2015) 289297

to the possibility that the high C input enhanced N2O release


(Frimpong and Baggs, 2010). However, the N2O emission factor for
manure-N was low. Apparently, the composted manure provided
little easily degradable carbon and therefore did not stimulate N2O
release via denitrication processes (Murphy et al., 2003).
4.3. Effects of alternative organic fertilization strategies on net GWP,
GHGI and crop yield
Typically, the net GWP estimates should include the CH4 and
N2O uxes and the sequestration of soil C. Here, we calculated net
GWP (kg CO2-eq ha1) to assess the combined climatic impacts of
GHG emissions from chemical N fertilizer and pig manure compost
production. The C loss from the manufacture of chemical N
fertilizer (GWPN) and pig manure compost (GWPmanure) was one of
the dominant factors determining net GWP. This scenario
considers whether adding organic amendments would reduce
net GWP compared with the continuing use of chemical N
fertilizer. In our study, chemical fertilizer had an edge over
feedstock conversion (i.e., GWPN = 1.99 t CO2 ha1 yr1; GWPma1
yr1) at the same N-fertilizer of 240 kg N ha1.
nure = 3.67 t CO2 ha
Although, the gases produced during manure compost can be
utilized as energy source, it is still not in practice in China. All
treatments were GHG sources except the control.
The positive annual net GWP for all of the eld treatments in
this study is similar to some previous eld and modeling studies of
rice paddies. Earlier, Grace et al. (2003) estimated an annual GWP
of 3.507.12 t CO2-eq ha1 yr1 for an irrigated ricewheat system
in the Indo-Gangetic plains depending on crop management
practices. However, they adopted the Inter-Governmental Panel of
Climate Change (IPCC) default emission coefcients and included
only N2O and CH4 emissions. Adviento-Borbe et al. (2007) gave an
estimate of GWP ranging from 0.54 to 1.02 t CO2-eq ha1 yr1 in a
maize and soybean cropping system. Recent studies have begun to
consider GWP based on the accounting of annual changes in SOC
and CH4 and N2O emissions (Shang et al., 2011). Clearly, the
divergent GWP results mentioned above are due to the methods for
estimating ecosystem C balance.
Average crop yields in this experiment (Table 3) were close to
the yield potential of rice and wheat at this location (Ladha et al.,
2003). Grain yield increased by an average of 8.5% in the organic
amendment treatments compared with the CF (Table 4), suggesting that the demand for plant growth could be satised by
substituting chemical N fertilizers. This nding is consistent with
the ndings of Chen et al. (2008) and Zhang et al. (2011) for maize
in the north of China. Combining results of net GWP and grain yield,
the GHGIs showed a similar pattern with net GWP and ranged from
0.08 to 0.39 kg CO2eq kg1 yield in this study (Table 4). These
values were comparable to previous estimates of 0.240.74 kg CO2eq kg1 yield with organic manure incorporation in rice paddies
(Qin et al., 2010) and of 0.410.74 kg CO2-eq kg1 yield with
integrated soil crop system management in rice paddies (Ma et al.,
2013).
All in all, the current CF treatment seems to be a proper strategy
with the lowest net GWP and GHGI, an increasing DSOC and an
acceptable grain yield (Table 4). However, Su et al. (2006) proved
that under conventional farming the inadequacy of chemical
fertilizers could not sustain high SOC levels in the long-term.
Moreover, such a high annual chemical N input of 480 kg N ha1
yr1 can be hazardous for water pollution and soil quality such as
soil acidication (Guo et al., 2010). When we compared the overall
effects of MC to those of CF, the MC produced higher grain yield and
sequestered more SOC with similar size of net GWP and GHGI,
although their values were higher. Moreover, the MC strategy
received only half of the current applications of chemical fertilizer
as in CF. Therefore, we recommend that the application of manure

substituting half chemical fertilizer be an effective strategy in the


ricewheat annual rotation system.
However, the other proposed organic strategies of SC, SM, and SI
signicantly increased net GWP and GHGI as well as SOC in our
study. Compared to manure treatments, the straw treatments have
higher net GWPs and GHGIs, which were mostly resulted from the
higher CH4 emissions (Table 4). Consistent with numerous
previous studies (Yan et al., 2005; Wang et al., 2012), straw
incorporation stimulated CH4 emissions from rice elds. Therefore,
straw returning in any currently studied strategies should be reexamined in the ricewheat annual rotation system. Yan et al.
(2005) found that straw returned off-rice season decreased CH4
emissions by 42% compared with conventional straw returning.
Composting straw as pretreatment might serve as another option
(Yang et al., 2007). Straw derived biochar amendment could also
serve as a potential way for GHG mitigations (Li et al., 2015). Thus,
alternative straw return practices should be taken into account and
deserve more attentions.
5. Conclusion
Considering the higher SOC rates and comparable net GWP and
GHGI in the MC strategy compared to the conventional chemical
fertilizer treatment of CF, we conclude that the application of pig
manure compost substituting half of the conventional chemical
fertilizer urea can serve as a mitigation strategy. This is practically
feasible through modication to the current local management
practice. However, the other proposed organic strategies of SC, SM,
and SI involving straw returning in the annual ricewheat rotation
system require further researches due to their obviously higher
GWP and GHGI though with higher food production as compared
to conventional chemical fertilizer. Alternative straw return
practices should be taken into accounts.
Acknowledgments
This work was supported by the National Science Foundation of
China (41171238, 41471192), the Ministry of Science and Technology (2013BAD11B01), and the Fundamental Research Funds for the
Central Universities(KYTZ201404).
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