European Journal of Soil Biology 55 (2013) 83e90

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European Journal of Soil Biology

journal homepage: http://www.elsevier.com/locate/ejsobi

Original article

Soil CO2 emissions from a cultivated Mollisol: Effects of organic

amendments, soil temperature, and moisture
Lu-Jun Li a, *,1, Meng-Yang You a,1, Hong-Ai Shi a, b, Xue-Li Ding a, Yun-Fa Qiao a, Xiao-Zeng Han a, *
a
b

Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, China
Northeast Agricultural University, Harbin 150030, China

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 22 June 2012
Received in revised form
25 December 2012
Accepted 31 December 2012
Available online 10 January 2013
Handling editor: Yakov Kuzyakov

A eld experiment was conducted to examine the inuences of long-term applications of maize straw
and organic manure on carbon dioxide (CO2) emissions from a cultivated Mollisol in northeast China and
to evaluate the responses of soil CO2 uxes to temperature and moisture. Soil CO2 ux was measured
using closed chamber and gas chromatograph techniques. Our results indicated that the application of
organic amendments combined with fertilizer nitrogen, phosphorus and potassium (NPK) accelerated
soil CO2 emissions during the maize growing season, whereas NPK fertilization alone did not impact
cumulative CO2 emissions. Cumulative CO2 emissions were higher from soils amended with pig manure
relative to those with maize residue. Cumulative CO2 emissions during the growing season were 988 and
1130 g CO2 m
2 under applications of 7500 and 22,500 kg ha
1 pig manure combined with NPK,
respectively, which were 42 and 63% higher than the emissions from the control (694 g CO2 m
2). The
applications of 2250 and 4500 kg ha
1 maize straw combined with NPK marginally increased soil CO2
emissions by 23 and 28% compared with the control, respectively. A log-transformed multiple regression
model including both soil temperature and moisture explained 50e88% of the seasonal variation in soil
CO2 uxes. Cumulative soil CO2 emissions were affected more by applied treatments than by soil temperature and moisture. Our results suggest that the magnitude of the impact of soil amendments on CO2
emissions from Mollisols primarily depends on the type of organic amendments applied, whereas the
application rate has limited impacts.
2013 Elsevier Masson SAS. All rights reserved.

Keywords:
Mollisols
Soil organic amendment
Soil respiration
Temperature sensitivity
Water-lled pore space

1. Introduction
Increased atmospheric carbon dioxide (CO2) has been considered a major contributor to global warming as well as climatic
change [1,2]. Although arable soil has been identied as one of the
main CO2 sources in agroecosystems due to inappropriate management practices, it can also serve as a net sink for atmospheric
CO2 through appropriate agricultural management [3,4].
Organic amendments (e.g., straw and organic manure) have
been widely used in agroecosystems due to their positive roles in
soil fertility improvement and climate change mitigation via soil
carbon sequestration [3,5,6]. Previous studies have shown various
responses of soil CO2 emissions to applications of organic

* Corresponding authors. Northeast Institute of Geography and Agroecology,

Chinese Academy of Sciences, 138 Haping Rd, Harbin 150081, China. Tel.: 86 451
8660 2940; fax: 86 451 8660 3736.
E-mail addresses: lilujun@neigaehrb.ac.cn (L.-J. Li), xzhan@neigaehrb.ac.cn
(X.-Z. Han).
1
These authors contributed equally to this work.
1164-5563/$ e see front matter 2013 Elsevier Masson SAS. All rights reserved.
http://dx.doi.org/10.1016/j.ejsobi.2012.12.009

amendments [7,8]. The amount of soil CO2 emissions is dependent

on many factors, primarily the type and level of applied organic
amendments [9], as well as the quantity of carbon already in the
soil [10]. In fact, soil management, plant cover and soil nutrient
status can not only alter soil respiration, but also change the temperature sensitivity of this process [11]. Thus, the overall response
of soil CO2 emissions to organic amendments is a complex process
and remains uncertain.
Soil temperature and moisture have been identied as the most
important environmental factors inuencing soil CO2 emissions
[12,13]. The temperature effect is commonly described as an
exponential equation [12], whereas the effects of soil moisture are
not always consistent [14]. The lack of consensus among trials could
result from the collective impacts of differences in soil types [15],
experiment duration and methods of CO2 emission measurement
[16], added to the confounded effects of soil temperature and
moisture [17,18]. Therefore, the roles of soil temperature and
moisture in soil CO2 emissions are still unclear.
Mollisols in northeast China are characterized by a high carbon content and ne texture. Due to intensive cultivation and

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L.-J. Li et al. / European Journal of Soil Biology 55 (2013) 83e90

low organic material return, a remarkable decline in soil organic

carbon (SOC) in croplands has occurred over the last several
decades in the Mollisols. To improve the ne texture and increase
the SOC content of these soils, organic amendments (e.g. crop
straw and organic manure) have been widely applied in the region. However, eld observations on the responses of soil CO2
emissions to long-term organic material incorporations into high
carbon soils are still limited. The objectives of this study were to
examine the inuences of long-term applications of organic
amendments combined with chemical fertilizers on CO2 emissions from Mollisols in China and to clarify the responses of soil
CO2 uxes to soil temperature and moisture. We hypothesized
that soil CO2 emissions might be enhanced by long-term applications of organic amendments due to the incorporation of
exogenous carbon.
2. Materials and methods
2.1. Site description
The experimental site was located at the Hailun National
Experiment Station of Agroecosystems of the Chinese Academy of
Sciences (47 260 N, 126 380 E). The mean annual temperature was
1.5  C, and the lowest and highest mean monthly values
were
23  C in January and 21  C in July, respectively. The mean
annual precipitation was 550 mm, more than 80% of which occurred from MayeSeptember. The frost-free period is approximately
120 days. The soil is a loamy loess and classied as Typic Hapludoll.
2.2. Experimental design
The eld site is on a at plain and was a native prairie before the
land was cleared for cropping more than 100 years ago. A long-term
eld experiment was established in a randomized block design in
1990 based on four treatments with three replicates: no fertilizer
(Control), chemical fertilizer made up of nitrogen, phosphorus and
potassium (NPK), NPK fertilizer plus maize straw (NPK MS1), and
NPK fertilizer plus double the maize straw of NPK MS1
(NPK MS2). In 2001, we added two additional treatments with
three replicates: NPK fertilizer plus pig manure (NPK OM1) and
NPK fertilizer plus triple the pig manure of NPK OM1
(NPK OM2). Each replicate covered a surface area of 12  5.6 m2
and was separated from other replicates by a 0.7-m buffer strip. A
maizeesoybeanewheat crop rotation was established, and the crop
was maize in 2011. Maize was sown on May 8 and harvested on
September 26, 2011. To increase soil temperature to stimulate
maize germination in early spring, the eld was split into ridges
(approximately 10 cm in height) and furrows using a ridge plow.
The distance between adjacent ridges was 70 cm. The depth of
tillage was approximately 20 cm.
The fertilizer applications were as follows: 1) 120 kg N ha
1,
60 kg phosphorus pentoxide (P2O5) ha
1, and 30 kg potassium
oxide (K2O) ha
1 for maize; 2) 20.25 kg N ha
1, 51.75 kg P2O5 ha
1,
and 30 kg K2O ha
1 for soybeans; and 3) 75 kg N ha
1,
60 kg P2O5 ha
1, and 30 kg K2O ha
1 for wheat. The maize straw and
organic manure were applied as follows (dry-weight basis):
2250 kg ha
1 in NPK MS1, 4500 kg ha
1 in NPK MS2,
7500 kg ha
1 in NPK OM1, and 22,500 kg ha
1 in NPK OM2 for
the 3 year rotation. Urea was split into two applications for the
treatments receiving N fertilizer, the basal and supplementary
fertilizers, with a ratio of 1:2 for maize. The pig manure was composted before application. Straw and organic manure applications
were performed in the previous year after crop harvest. The maize
straw contained 411 mg organic C g
1 and 6.7 mg total N (TN) g
1;
the pig manure contained 265 mg organic C g
1 and 31 mg TN g
1.

2.3. Measurement of CO2 uxes

Soil CO2 ux was measured using closed chamber and gas chromatograph techniques during the maize growing season. Gas sampling was initiated on May 27, 2011 at the time of emergence and
ended on September 30, 2011 with the maize harvest. During the
maize growing season, gas sampling was conducted once per week
between 9:00 and 11:00 am, the optimal sampling time to represent
the average daily CO2 efux in this region [19]. The CO2 ux was not
measured on July 30 due to heavy rain. Four gas samples were collected at 0, 10, 20, and 30 min after closure of the chamber from
a septum installed at the top of the closed chamber
(0.7 m  0.2 m  0.25 m) using a 20 ml gas-tight syringe. The collected
gas samples were immediately transferred to pre-evacuated vials and
transported to the laboratory for analysis. The collected gases included
the CO2 from both rhizosphere respiration and native soil respiration.
Carbon dioxide concentration was determined using a gas
chromatograph (GC-2010, Shimadzu Corp., Japan) equipped with
a ame ionization detector (FID) using an 80/100 mesh Chromosorb
102 column. Carbon dioxide ux was calculated from the change in
CO2 concentration in the chamber vs. closure time using the following formula:

f r  Dc=Dt  V=A  273=273 T

(1)

where f is the CO2 ux (mg CO2 m
2 h
1), r is the CO2 density under
standard conditions (mg m
3), Dc/Dt is the change in CO2 concentration in the chamber (m3 m
3 h
1), V is the chamber volume (m3),
A is the soil surface area (m2), and T is the air temperature inside the
chamber ( C). Cumulative soil CO2 emission (g CO2 m
2) was calculated by summing the average production of two neighboring
uxes, multiplied by the collection interval time.
2.4. Soil sampling and analyses and measurement of micro-climate
factors
Soil samples (0e20 cm) were collected within each block in
early October 2011. Eight soil samples were randomly collected and
then mixed thoroughly to form a composite. After the visible roots,
fauna and organic debris were removed by hand, soil samples were
sieved (<2 mm) and air-dried. Air-dried soil samples (<2 mm) were
used to determine soil pH from a 1:2.5 (w/v) mixture of soil and
water. A portion of the air-dried samples was ground (<0.25 mm)
prior to the SOC and TN analyses. Soil organic C and TN contents
were analyzed using an elemental analyzer (Vario EL III, Elementar,
Germany). Soil bulk density was measured using the core method.
The air temperature inside the chamber was measured with
a mercury thermometer; soil temperatures at 5 and 10 cm depths
were determined in situ simultaneously using a geothermometer.
Field soil moisture was gravimetrically determined from undisturbed soils within 1 m of the eld chambers for the calculation of
soil water-lled pore space (WFPS).
The maize crop was harvested on September 26, 2011. All
aboveground crop materials within a plot area of 2  1.4 m were
cut. The harvested materials were separated into grain and straw,
the latter including stems and leaves. Root biomass (0e20 cm) was
quantied at the same location used for aboveground sampling.
Roots were separated from soils by hand picking and washing with
water. All crop samples (grain, straw and root) were oven-dried at
70  C for 48 h and then weighed to determine the biomass.
2.5. Calculation and statistical analyses
The accepted signicance level was a 0.05. Homogeneity of
variance and normality tests were conducted on the gas and biomass

L.-J. Li et al. / European Journal of Soil Biology 55 (2013) 83e90

data at the 5% level. A one-way analysis of variance (ANOVA) with

least signicant difference was used to test the differences in maize
yield, biomass, soil property parameters, and cumulative CO2 emissions among the six treatments at P 0.05. The relationships between straw biomass, maize yield, root biomass, and SOC
concentration and cumulative CO2 emissions were examined using
linear regression. Nonlinear regression analyses were used to
determine the relationships between soil temperature, moisture,
and soil temperature combined with moisture and soil CO2 uxes.
The response of soil CO2 uxes to soil temperature was described by an exponential function:

f a expbT;

(2)

where f is the soil CO2 ux at soil temperature T and a and b are

regression coefcients. The temperature sensitivity (Q10), dened
as a multiplier of soil CO2 ux for a 10  C increase in soil temperature, was calculated as follows: Q10 exp (10b).
To clarify the effects of soil moisture on soil CO2 ux, we
removed the possible confounding effect of soil temperature on soil
CO2 ux by standardizing soil CO2 ux to a soil temperature of 10  C
using the following equation:

f f10 explnQ10  T
T10 =10;

(3)

where f is the soil CO2 ux measured in the eld, f10 is the soil CO2
ux at 10  C (T10), Q10 is the temperature sensitivity listed in Table 2,
and T is the soil temperature measured in the eld at a 5 cm depth.
3. Results
3.1. Soil properties, crop yield and biomass
The NPK OM2 fertilization increased SOC content by 12%
compared with the control (P < 0.05, Table 1). However, the SOC
contents in treatments NPK, NPK MS1, NPK MS2, and
NPK OM1 were not signicantly different from that in the control
(P > 0.05; Table 1). Total N content signicantly increased by 24%
over the control under the NPK OM2 treatment (Table 1). The pH
value under the NPK OM2 treatment was higher than that under
NPK MS1 (P < 0.05; Table 1).
Crop grain, straw, and root biomasses in the control plots were
signicantly lower than in all other treatments (P < 0.05; Table 1).
Compared with the control, the applications of NPK, NPK MS1,
NPK MS2, NPK OM1, and NPK OM2 signicantly increased
straw biomass by 45, 46, 62, 11, and 20%, respectively and increased
root biomass by 50, 139, 138, 110, and 126%, respectively (all
P < 0.05; Table 1).
3.2. Soil temperature and moisture
Soil temperature varied from 4 to 37  C during the maize
growing season, with averages of 21  C and 18  C at 5 and 10 cm

85

depths, respectively (Fig. 1a, b). Soil temperatures at both 5 and

10 cm depths reached maxima on June 24 (Fig. 1a, b) when the soil
WFPS was lower than at most other sampling times (Fig. 1c). Mean
soil temperatures during the growing season were 19.5 and 19.3  C
at a 5 cm depth (Fig. 1a) and 17.4 and 17.5  C at a 10 cm depth for
NPK OM1 and NPK OM2, respectively (Fig. 1b), which were
lower values than those in the control treatment (5 cm: 22  C,
10 cm: 19.7  C). Soil moisture ranged from 25 to 51% WFPS during
the maize growing season and was higher on average in the control
than in the other treatments (Fig. 1c). Soil moisture was signicantly correlated with cumulative precipitation between two
neighboring measurement times (r2 0.54e0.63, n 18,
P < 0.001).
3.3. Seasonal variations in soil CO2 uxes and cumulative CO2
emissions
Soil CO2 uxes, regardless of organic or chemical fertilizer
application, increased gradually from the experiments beginning
in May and reached a maximum on August 6 (Fig. 2a). Soil CO2
uxes then declined gradually until the harvest at the end of September. The mean soil CO2 ux during the maize growing season in
the control treatment was 215 mg CO2 m
2 h
1, which was signicantly lower than those in the treatments of organic manure
applications (NPK OM1, 310 mg CO2 m
2 h
1; NPK OM2:
355 mg CO2 m
2 h
1; P < 0.05).
Based on soil CO2 uxes, cumulative CO2 emissions during the
maize growing season in the control, NPK, NPK MS1, NPK MS2,
NPK OM1, and NPK OM2 treatments were estimated to be 694,
678, 853, 889, 988, and 1130 g CO2 m
2 (Fig. 2b). Cumulative CO2
emissions in the NPK OM1 and NPK OM2 treatments were
signicantly higher than that in the control by 42 and 63%,
respectively (both P < 0.05); the NPK MS1 and NPK MS2
treatments marginally increased CO2 emissions by 23 and 28%,
respectively (P < 0.1). In contrast, NPK fertilization alone did not
signicantly impact cumulative CO2 emission (P > 0.05; Fig. 2b). In
addition, there was no signicant difference in soil CO2 emissions
between NPK OM1 and NPK OM2 or between NPK MS1 and
NPK MS2 (both P > 0.05; Fig. 2b).
3.4. Impacts of micro-climate factors on soil CO2 uxes
During the maize growing season, an exponential model
explained 26e34% of the seasonal variations in soil CO2 uxes in
only four out of the six treatments at a 10 cm depth (Table 2). Using
only the data from the elongation to the harvest stage, however, we
found improved relationships between soil temperature and CO2
uxes (R2 0.43e0.91, P < 0.05; Table 2). The temperature sensitivity (Q10) of soil CO2 uxes during the growing season ranged
between 1.87 and 3.00 (Table 2). Correlation analysis showed poor
relationships between soil CO2 uxes and WFPS during the growing
season (Table 3). After excluding the masking inuence of soil
temperature, we found greatly improved relationships between

Table 1
Soil properties, maize yield and biomass under different fertilization treatments. The values are the means (n 3) with SE.
Treatment
a

Control
NPK
NPK MS1
NPK MS2
NPK OM1
NPK OM2

SOC (g kg
1)
b

28.20(0.17)b
27.66(0.09)b
29.89(0.26)ab
28.75(0.10)ab
28.57(0.47)ab
31.56(0.74)a

TN (g kg
1)

pH

Grain (kg ha
1)

Straw (kg ha
1)

Root (kg ha
1)

2.06(0.03)b
2.06(0.02)b
2.21(0.11)b
2.14(0.05)b
2.18(0.08)b
2.55(0.08)a

5.91(0.02)ab
5.92(0.05)ab
5.69(0.02)b
5.76(0.17)ab
5.76(0.12)ab
6.01(0.04)a

5797(344)d
8384(146)b
8449(103)b
9394(312)a
6446(124)c
6981(120)c

3922(180)d
6348(341)c
7455(458)b
7177(181)bc
8173(455)ab
8700(195)a

517(30)c
775(42)b
1238(111)a
1232(98)a
1090(162)a
1166(125)a

a
Control: no fertilizer, NPK: chemical fertilizer NPK, NPK MS1: NPK plus maize straw, NPK MS2: NPK plus twice as much maize straw, NPK OM1: NPK plus pig
manure, and NPK OM2: NPK plus three times the pig manure.
b
The different letters in each column indicate the signicant difference at P < 0.05.

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L.-J. Li et al. / European Journal of Soil Biology 55 (2013) 83e90

L.-J. Li et al. / European Journal of Soil Biology 55 (2013) 83e90

87

Fig. 2. Seasonal variations of soil CO2 uxes (a) and cumulative CO2 emissions (b) from a Mollisol during a maize growing season. The vertical bars denote the standard error of the
mean (n 3). The arrows denote the application time of basal (BF) and supplemental (SF) fertilizers. A one-way ANOVA with LSD post hoc test was performed to examine the
differences in cumulative CO2 emissions among treatments. The different small letters indicate the signicant difference in cumulative CO2 emissions among treatments at P < 0.05.
Control, no fertilizer; NPK, chemical fertilizer NPK; NPK MS1, NPK plus maize straw; NPK MS2, NPK plus twice as much maize straw; NPK OM1, NPK plus pig manure; and
NPK OM2, NPK plus three time the pig manure.

soil CO2 uxes and WFPS in the 5 cm layer (Table 3), which
explained 30e60% of the seasonal variations in soil CO2 ux. Furthermore, a log-transformed multiple regression model including
both soil temperature and moisture [log(f) a b T log(W)]
accounted for 50e88% of the seasonal variation in soil CO2 uxes
(Table 4).
Cumulative CO2 emissions were signicantly correlated with the
harvested straw and root biomass (r2 0.62, n 18, P < 0.001 and
r2 0.46, n 18, P 0.002, respectively; Fig. 3a). A signicant
correlation was also found between cumulative CO2 emissions and
SOC (r2 0.40, n 18, P 0.005; Fig. 3b).
4. Discussion
4.1. Effect of long-term organic amendment applications on soil CO2
emissions
Consistent with our hypothesis, enhanced soil CO2 emissions
were observed under organic amendment treatments (NPK MS1,
NPK MS2, NPK OM1, NPK OM2) in comparison with the
unfertilized control in our study. Several studies have shown that
a long-term return of straw or addition of organic manure to soil
can result in substantial increases in the soil respiration rate [8,20].
The total CO2 ux from soils can be divided into two components:
rhizosphere-derived CO2 (rhizosphere respiration) and soil organic
matter (SOM)-derived CO2 in root-free soil (basal respiration) [21].
Rhizosphere respiration reects both the metabolic activities of the
living root tissue and SOM decomposition in the rhizosphere, and
both processes are proportional to root biomass [22]. Using a rootexclusion technique, a previous study observed that rhizosphere
respiration comprised the majority of soil respiration in croplands,
accounting for 67e80% of the overall CO2 emission from the Mollisols [23], and root respiration is an important contributor to rhizosphere respiration in situ [24]. Although the present study was
not capable of distinguishing the root respiration component of
total soil CO2 emissions, the increased root biomass with organic
amendment applications (Table 1) might have partly enhanced
cumulative CO2 emissions as reected by the positive correlation

between CO2 emissions and root biomass (r2 0.46, n 18,

P 0.002; Fig. 3a).
Aside from autotrophic root respiration, another important
source of total CO2 ux is heterotrophic respiration from soil microorganisms and macrofauna [21,25]. As the contribution of soil
macrofauna to total CO2 uxes from soils is usually only a few
percent [26], most of the CO2 derived from heterotrophic respiration is respired by soil microorganisms. Similar to an earlier
observation [23], we found that soil CO2 emissions were signicantly correlated to SOC (r2 0.40, n 18, P 0.005; Fig. 3b).
Soil CO2 emission related to microbial respiration is derived from
basal respiration and CO2 production as a consequence of a priming
effect [21]: organic manure and straw applications can greatly
increase the amount of substrates for soil microorganisms and also
alter soil microbial activity, subsequently accelerating SOM
decomposition [27]. Therefore, the increased CO2 emissions from
the organic amendment treatments in our study may be partly
attributed to the positive priming effect of substrate inputs compared to the control. In addition to the sources affecting soil CO2
emissions described above, rhizomicrobial respiration and the
decomposition of added organic amendments were also biogenic
sources of soil CO2 emissions. However, due to high turnover rates
and thus low residence times in soils [21], rhizomicrobial respiration and amendment decomposition probably make limited contributions to total CO2 emissions.
More cumulative CO2 was emitted from soils amended with pig
manure relative to those with maize residue (Fig. 2b), indicating
that the manure amendment led to an enhancement of microbial
activity in comparison with the maize residue. Microbial activity
can be inuenced by soluble carbon and nitrogen compounds in
soils [28]. The levels of soluble carbon and nitrogen compounds in
soils can be increased by consecutive applications of manure [29],
whereas they can be decreased by maize residue applications due
to the assimilation of available carbon and immobilization of
available nitrogen by microorganisms [30]. Manure applications
thus could provide more soluble carbon and nitrogen for microbial
activity than maize residue. In addition, microbial activity and the
related decomposition rate of organic amendments are partly

Fig. 1. Seasonal variations in soil temperature at 5 (a) and 10 cm (b) depths, soil water-lled pore space (WFPS) in the 5 cm layer (c), and daily precipitation and air temperature data
(d) from a meteorological station at the eld experiment site during a maize growing season. The vertical bars denote the standard error of the mean (n 3) for Fig. 1a, b, c. Control,
no fertilizer; NPK, chemical fertilizer NPK; NPK MS1, NPK plus maize straw; NPK MS2, NPK plus twice as much maize straw; NPK OM1, NPK plus pig manure; and NPK OM2,
NPK plus three time the pig manure.

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L.-J. Li et al. / European Journal of Soil Biology 55 (2013) 83e90

Table 2
Relationships between soil CO2 ux (f) and soil temperature (T) at 5 and 10 cm
depths during the maize growing season.
Treatment

Control

NPK

Depth Entire maize growing period From elongation to harvest

(cm) (n 18)
only (n 13)
(May 27eSeptember 30,
(July 1eSeptember 30, 2011)
2011)
Equation

R2

Q10b Equation

R2

Q10

0.43*

1.87

10

0.06 e

0.17 e

f 93.234
exp(0.0412T)
e

0.26* 1.51

10
NPK MS1

5
10

NPK MS2

5
10

NPK OM1

5
10

NPK OM2

5
10

0.14 e

f 88.912
exp(0.0530T)
e

0.33* 1.70
0.10 e

f 79.630
exp(0.0571T)
e

0.27* 1.77

f 101.244
exp(0.0566T)
e

0.34* 1.76
0.04 e

0.13 e

0.20 e

f 57.703
exp(0.0627T)
f 54.911
exp(0.0711T)
f 51.821
exp(0.0677T)
f 62.770
exp(0.0684T)
f 44.806
exp(0.0793T)
f 53.671
exp(0.0832T)
f 34.516
exp(0.1030T)
f 37.764
exp(0.1097T)
f 65.664
exp(0.0820T)
f 68.940
exp(0.0866T)
f 65.412
exp(0.0935T)
f 67.284
exp(0.0984T)

0.58** 2.04
0.72*** 1.97
0.81*** 1.98
0.58** 2.21
0.72*** 2.30
0.82*** 2.80
0.91*** 3.00
0.70*** 2.27
0.76*** 2.38
0.74*** 2.55
0.79*** 2.68

Correlation signicance levels: *P < 0.05, **P < 0.01 and ***P < 0.001.
a
Control: no fertilizer, NPK: chemical fertilizer NPK, NPK MS1: NPK plus maize
straw, NPK MS2: NPK plus twice as much maize straw, NPK OM1: NPK plus pig
manure, and NPK OM2: NPK plus three times the pig manure.
b
Q10: temperature sensitivity.

related to organic amendment quality, in which the C/N ratio has

been shown to be a good predictor of the decomposition of organic
amendments applied to soils [28]. The pig manure, with a low C/N
ratio (w9), could decompose more easily than the maize residue
with a higher C/N ratio (w61). Therefore, pig manure most likely
provided more easily degradable and potentially more soluble
carbon for microbial activity than the maize residue and thus led to
greater soil CO2 emissions. Our results suggest that the magnitude
of the impact of soil amendments on soil CO2 emissions primarily
depends on the type of organic amendments applied to the test soil,
whereas the rate of application has limited effects on cumulative
Table 3
Relationships between soil CO2 ux (f) and soil WFPS (W) in the 5 cm layer during
the maize growing season (n 13).
Treatment

Equation

R2

Excluding the inuence of soil

temperature
Equation

Control

NPK
NPK MS1
NPK MS2
NPK OM1
NPK OM2

f 10.005W

188.059
f 6.815W

32.567
f 16.631W

309.019
f 12.650W

134.627
f 12.657W

123.650
f 16.018W

163.948

0.31 0.048 f 17.777

exp(0.0423W)
0.20 0.127 f 39.393
exp(0.0246W)
0.46 0.011 f 15.485
exp(0.0524W)
0.20 0.121 f 26.696
exp(0.0369W)
0.20 0.128 f 40.125
exp(0.0312W)
0.19 0.142 f 54.677
exp(0.0309W)

R2

0.39 0.023
0.41 0.019
0.60 0.002
0.53 0.005
0.35 0.033
0.30 0.054

a
Control: no fertilizer, NPK: chemical fertilizer NPK, NPK MS1: NPK plus maize
straw, NPK MS2: NPK plus twice as much maize straw, NPK OM1: NPK plus pig
manure, and NPK OM2: NPK plus three times the pig manure.

Table 4
Relationships between soil CO2 ux (f) and soil temperature (T) at a 5 cm depth and
soil WFPS (W) in the 5 cm layer during the maize growing season (n 13).
Treatment
a

Control
NPK
NPK MS1
NPK MS2
NPK OM1
NPK OM2

Equation
log(f)
log(f)
log(f)
log(f)
log(f)
log(f)

1.732
1.709
1.628
1.538
1.812
1.819

0.018
0.019
0.023
0.029
0.023
0.026

T
T
T
T
T
T

log(W)
log(W)
log(W)
log(W)
log(W)
log(W)

R2

0.50
0.79
0.68
0.88
0.75
0.79

0.007
<0.001
<0.001
<0.001
<0.001
<0.001

a
Control: no fertilizer, NPK: chemical fertilizer NPK, NPK MS1: NPK plus maize
straw, NPK MS2: NPK plus twice as much maize straw, NPK OM1: NPK plus pig
manure, and NPK OM2: NPK plus three times the pig manure.

soil CO2 emissions as shown by the absence of a remarkable difference in CO2 emissions under different application rates of a given
organic amendment (Fig. 2b).
Despite the increased soil CO2 emissions, the combined use of
organic amendments and chemical fertilizers improved or at least
maintained the SOC content of the studied Mollisols (Table 1). This
indicates that the carbon inputs to the soils were larger than or at
least in equilibrium with the carbon losses from soils induced by
the organic amendment applications.
4.2. Effects of soil temperature and moisture on the temporal
variation of soil CO2 uxes
The temporal variation in soil CO2 uxes is commonly related to
soil temperature, moisture or both [12,31,32]. In the present study,
however, only 26e34% of the seasonal variations in soil CO2 uxes
could be explained by soil temperature with an exponential
equation under certain treatments (Table 2), which implied that
other factors were affecting the CO2 uxes. In our study, enhanced
CO2 uxes were observed after the applications of both basal and
supplemental fertilizers (Fig. 2a). Moreover, an exponential equation described the relationship between soil temperature and CO2
uxes well under all treatments when we restricted the analysis to
the period from the elongation stage to the harvest time: R2 values
were also greatly improved (0.43e0.91) given this time restriction,
accompanied by increases in Q10 values (1.87e3.00; Table 2). Thus,
we believe that a disturbance, most likely related to plowing or
fertilization, affected soil CO2 emissions at the seedling stage and,
further, partly modied the inuence of soil temperature on CO2
uxes, as shown by a previous study [33].
Previous studies have shown that soil moisture status can also
inuence soil respiration [14,34]. However, the present study
found a poor relationship between soil CO2 uxes and WFPS.
There could be several reasons for this result. The narrow range
of soil WFPS (25e51%, Fig. 1c) in the studied eld might have
resulted in the observed weak inuence on soil CO2 uxes [35].
Soil temperature was also an important factor regulating the
effects of moisture on CO2 uxes [36]. Previous researchers have
noted that the effects of soil moisture on CO2 uxes are partly
obscured by soil temperature, because soil moisture and temperature usually change simultaneously [34,37]. In the present
study, we found improved relationships (R2 0.30e0.60) between soil CO2 uxes and WFPS after the masking inuence of
soil temperature was excluded (Table 3). Furthermore, the logtransformed multiple regression model including both soil temperature and moisture was much better able to explain the seasonal variations in soil CO2 uxes than the regression model with
moisture alone, with or without excluding the inuence of
temperature (Tables 3 and 4). Therefore, our results showed that
there was a signicant interdependence between soil temperature and moisture in their effects on soil CO2 uxes in the studied
Mollisols.

L.-J. Li et al. / European Journal of Soil Biology 55 (2013) 83e90

89

Fig. 3. Relationships between cumulative CO2 emissions during the maize growing season and maize biomass at harvest (a) and soil organic carbon concentration (b) (n 18).

When a separate analysis was conducted for each treatment

individually, the seasonal variations in soil CO2 ux rates could be
positively explained by the seasonal variations in soil temperature
and moisture. For all treatments together, however, we observed
that the treatments with lower mean soil temperatures and
moisture had higher CO2 emissions than others. These results,
combined with the positive relationships between soil temperature, moisture and CO2 uxes (Table 2), indicated that cumulative
CO2 emissions during the growing season were affected more by
the applied amendments than by soil temperature and moisture in
the cultivated Mollisols.
It is noteworthy that the closed chamber system is known to
underestimate soil CO2 uxes by approximately 10% due to the
effective volume being larger than the volume of the chamber itself
[38]. Thus, a further study comparing a closed- and an openchamber methodology is needed to obtain a calibration factor for
the Mollisols.
5. Conclusion
Applications of organic amendments combined with NPK
accelerated CO2 emissions from soils, whereas NPK fertilization
alone did not signicantly impact cumulative CO2 emissions. More
cumulative CO2 was emitted from soils amended with pig manure
relative to those with maize residue. The log-transformed multiple
regression model log(f) a b T log(W) including soil temperature
and moisture accounted for 50e88% of the season variation in soil
CO2 uxes. Cumulative soil CO2 emissions during the growing
season were affected more by the applied amendments than by soil
temperature and moisture in the cultivated Mollisols in northeast
China. Our results suggest that for the Mollisols, the magnitude of
the impact of soil amendments on soil CO2 emissions depends
primarily on the type of organic amendments applied, whereas the
application rate has limited impacts.
Acknowledgments
This work was funded by the Strategic Priority Research ProgramClimate Change: Carbon Budget and Related Issues of the Chinese
Academy of Sciences (no. XDA05050501), the National Key Basic
Research Program of China (no. 2011CB100506), the Natural Science
Foundation of China (no. 41101283 and 41101282), and the Key
Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences (no. 2011ZKHT01). We thank Gui-Dan Sun for laboratory assistance and Wei-Li Gao

and Xiu-Ling Wen for their participation in the eld sampling. We

also thank three anonymous reviewers for their helpful comments
and suggestions, which improved the manuscript.

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