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Soil Biology & Biochemistry 57 (2013) 135e143

Contents lists available at SciVerse ScienceDirect

Soil Biology & Biochemistry

journal homepage: www.elsevier.com/locate/soilbio

Predicting soil respiration using carbon stock in roots, litter and soil organic
matter in forests of Loess Plateau in China
Zhiyong Zhou a, b, *, Zhiqiang Zhang c, Tonggang Zha c, Zhongkui Luo d, Jingming Zheng a,
Osbert Jianxin Sun a, b
a
MOE Key Laboratory for Silviculture and Conservation, Beijing Forestry University, Beijing 100083, China
b
Institute of Forestry and Climate Change Research, Beijing Forestry University, Beijing 100083, China
c
MOE Key Laboratory for Soil and Water Conservation and Desertification Combating, Beijing Forestry University, Beijing 100083, China
d
CSIRO Land and Water, Canberra, Australian Capital Territory 2601, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Understanding the dominant variables driving soil respiration is critically important for predicting soil
Received 21 February 2012 CO2 emission and assessing the carbon balance of forest ecosystems. In a small catchment of the semiarid
Received in revised form Loess Plateau in China, soil respiration and soil biophysical factors were studied on sites of five forest
7 August 2012
types, comprising plots established in a pure Pinus tabulaeformis plantation, a pure Robinia pseudoacacia
Accepted 8 August 2012
plantation, a mixed P. tabulaeformis and R. pseudoacacia plantation, a pure Platycladus orientalis plantation,
Available online 28 August 2012
and a natural Populus davidiana stand. Soil temperature at the 10 cm depth was found to be the most
predominant factor controlling the temporal pattern of soil respiration, accounting for 11e40% seasonal
Keywords:
Soil respiration
variation in the rate of soil CO2 efflux across forest types. By applying an empirical model and the
Forest type calculated temperature sensitivity of soil respiration (Q10) and the rate of basal soil respiration (R10),
Environmental factor annual soil CO2 emission was estimated separately for each forest type using the automatically monitored
Carbon stock data of soil temperature at the 10 cm depth. The annual soil CO2 emission varied greatly with forest types
Semi-arid Loess Plateau and ranged from 647.71 g C m
2 y
1 in the P. orientalis plantation to 1448.50 g C m
2 y
1 in the natural
P. davidiana stand. Annual soil CO2 efflux is better predicted by soil organic carbon content and the amount
of carbon in roots, litter and top soil than soil temperature when data are pooled for all plots of the five
forest types. A first order exponential analysis indicates that about 77% of the variation in annual soil CO2
efflux is explained by root carbon stock, 63% by the combined carbon stock in roots, litter, and top soil, and
48% by the combined carbon stock in litter and top soil. We conclude that annual soil CO2 efflux can be
predicted by carbon pools in roots and soils rather than by soil temperature in watersheds where spatial
variation in soil temperature is relatively small in the semiarid Loess Plateau of China.
Crown Copyright Ó 2012 Published by Elsevier Ltd. All rights reserved.

1. Introduction identifying the driving biophysical factors of soil respiration in

Soil CO2 efflux from terrestrial ecosystems to the atmosphere
has been considered as the second largest global carbon flux, and is
the vital component of ecosystem respiration (Raich and Potter,
1995). Estimating the magnitude of CO2 emitted from soil surface
is of critical importance in evaluating the role of ecosystems in the
context of global warming, as soil respiration determines the net
ecosystem carbon balance. In order to accurately predict soil CO2
emission in time and space, great progress has been made in
* Corresponding author. MOE Key Laboratory for Silviculture and Conservation,
Beijing Forestry University, Beijing 100083, China. Tel./fax: þ86 10 62336985.
E-mail address: zhiyong@bjfu.edu.cn (Z. Zhou).
recent decades (Davidson et al., 1998; Buchmann, 2000; Campbell
et al., 2004). Yet, as a main biome of China, the Loess Plateau has
received little attention, and data on CO2 emissions are scarce for
forest ecosystems in this region (Zhou and Shuangguan, 2009).
Quantifying the rate and magnitude of soil CO2 emission and
understanding the dominant environmental constraints of soil
respiration are essential for improving our knowledge on the
ecological role of forests in the Loess Plateau of China, where it is
undergoing the rapid temperature increases in China (Wang et al.,
2003).
Soil respiration is a composite process integrating two major
carbon fluxes, i.e. autotrophic respiration of plant roots and
heterotrophic respiration through soil microbial activities (Janssens
and Pilegaard, 2003), and is influenced by multitudes of

0038-0717/$ e see front matter Crown Copyright Ó 2012 Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.soilbio.2012.08.010
 Author's personal copy
136 Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143
environmental factors during field investigation. To date, most
models for predicting the rate of soil respiration has been largely
based on the relationship of soil CO2 efflux with soil temperature,
especially in biomes with great fluctuations in temperature (van’t
Hoff, 1898; Janssens and Pilegaard, 2003; Campbell et al., 2004),
as soil temperature often positively correlates with soil respiration
and accounts for its temporal variation across a wide range of
circumstances (Buchmann, 2000). Compared to soil temperature,
soil moisture maintains a less clear relationship with soil respira-
tion because either excess or deficit in soil water content may
constrain the rate of soil respiration in a temperate region (Vincent
et al., 2006). Empirical models may be modified by incorporating
the parameter of soil water content when predicting soil respira-
tion under specific conditions with optimal soil water content
(Vincent et al., 2006).
The confounding effects of soil temperature and moisture
prohibit the widespread use of the empirical models established for
specific sites in estimating soil CO2 emissions across different
biome types (Davidson et al., 1998). Therefore, much effort has been
directed at understanding the role of other biophysical factors in
controlling soil respiration (Janssens et al., 2001). Vegetation type
was proven a predominant factor affecting soil respiration through
modification of soil chemical and physical properties (Boudot et al.,
1986), control of the quantity and quality of plant litter inputs
(Epron et al., 2004), and effects of plant roots and associated
microbial activities (Janssens et al., 1998). Many studies have found
positive relationships of soil respiration with forest floor mass, soil
carbon content and fine root biomass, and the spatial variation in
soil respiration across different vegetation types can be well
explained by the empirical models based on these variables (Søe
and Buchmann, 2005; Wang et al., 2006). It is evident that soil
temperature plays a predominant role in the spatial variations of
soil respiration across sites of climatically contrasting environ-
ments (Campbell et al., 2004), but on a local scale or under the same
climatic conditions, other biological and biophysical factors, such as
vegetation type, stand structure and development, and the size and
quality of various organic carbon pools, may prevail as dominant
drivers of soil respiration (Campbell et al., 2004; Epron et al., 2006).
Substrate quantity and quality have been shown to affect the Q10 in
forests and grassland ecosystems (Campbell et al., 2004; Xiao et al.,
2007), greatly modifying the soil respirationetemperature rela-
tionship when substrate supply is limiting. Therefore, reassessment
of controlling factors of soil respiration is necessary for biomes with
highly specialized climatic and environmental conditions, such as
the Loess Plateau.
The Loess Plateau in China is characterized by arid and semiarid
climate and severe aeolian erosions (Zhang et al., 2011). Plant root
growth and vertical transport of organic matter are highly pro-
hibited due to soil compaction and high clay content. On most
forest sites, development of forest floor litter layer and soil organic
matter are very poor because of restricted root growth and high
surface runoff. It is of typical conditions of substrate limitation to
soil respiration. To determine the control of biotic and environ-
mental factors on soil respiration in forests of the Loess Plateau, we
conducted an experiment within a hilly catchment in Shanxi
province of China and investigated seasonal variations of soil CO2
efflux across five forest types, i.e. a pure Pinus tabulaeformis plan-
tation, a pure Robinia pseudoacacia plantation, a mixed P. tabu-
laeformis and R. pseudoacacia plantation, a pure Platycladus
orientalis plantation, and a natural Populus davidiana stand. Two
major objectives were addressed in this study: the first was to
quantify the magnitude of annual soil CO2 emission under different
forest cover types; the second was to identify the role of selected
biophysical variables, e.g. carbon pools of soil, plant roots, and litter,
and soil temperature, in predicting annual soil CO2 efflux in
semiarid Loess Plateau. We predicted that, because of substrate
limitation, the variation in annual soil respiration across different
forest types could be well explained by the size of various carbon
pools in the semiarid Loess Plateau.
2. Materials and methods
2.1. Study sites and experimental design
This study was carried out in the Caijiachuan watershed (lati-
tude 36140 e36180 N, longitude 110 400 e110 480 E, elevation 904e
1592 m a.s.l.) of Jixian in Shanxi province, China. The topography of
this watershed is characterized by typical loess gullies and hills, and
the soil belongs to loess-derived Cinnamon soil (Bi et al., 2008).
Long-term average annual temperature is about 10  C. Mean annual
precipitation is 579.5 mm, almost 80% of which falls between June
and August (Fig. 1). Potential annual evapotranspiration is
1724 mm.
Five study sites were selected based on existing natural and
experimental forest types in the drainage basin, representing (1)
pure P. tabulaeformis plantation, (2) pure R. pseudoacacia planta-
tion, (3) mixed P. tabulaeformis and R. pseudoacacia plantation, (4)
pure P. orientalis plantation, and (5) natural P. davidiana forest. All
but the P. davidiana site were located in the same gully with
a similar elevation above the sea (1120 m). The natural P. davidiana
stand was located in the gully about 4 km southeast of other sites
with an elevation of about 1040 m a.s.l. All of the plantations were
established in 1993 on the natural slope of Loess Plateau (Zhang
et al., 2008), displacing the original natural shrubs. Detailed infor-
mation for these five sites is shown in Table 1. In early spring of
2008, three plots of 20  20 m were established for each forest type,
and the plots were spaced at least 10 m apart.
2.2. Forest survey and measurements of root and litter carbon stock
In mid-August 2008, survey was carried out on tree density,
height, and stem diameter at breast height (DBH; 1.37 m in height)
on each plot. In order to avoid the influence of root sampling on soil
respiration, root biomass was determined later in the experiment
when the final measurements of soil respiration were completed.
Soil cores for root biomass were collected at five locations and
every 20 cm to a depth of 100 cm by a handheld cylinder auger of
8 cm in diameter and 20 cm in height on each plot. Plant roots were
separated from the cores by washing off the soil within a 0.4 mm
mesh bag, and oven-dried at 80  C to constant weight. Litter
150 35
40
Precipitation (mm)
30
precipitation
25
20 temperature
120 15 30
10
5
0
90 0 60 120 180 240 300 360 20
Day of Year
60 10
30 0
-10
1 2 3 4 5 6 7 8 9 10 11 12
Month
Fig. 1. The meteorological conditions of the studied region during 2008.
 Author's personal copy

Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143 137

Table 1 Table 2
Site characteristics of five studied forest types. DBH: diameter at breast height. The soil respiration parameters calculated from the van’t Hoff Q10 model [Eq. (1)] for
different forest types in the Loess Plateau. R10 is basal rate of soil respiration at
Forest type Slop Slope Stand Tree DBH Tree a reference soil temperature of 10  C, Q10 is temperature sensitivity of soil respira-
aspect angle age density (cm) height tion rate (n ¼ 3).
(h m
2) (m)
(1) P. tabulaeformis plantation West 19 17 1175 10 5.6 Forest type R10 Q10
(2) R. pseudoacacia plantation East 17 17 1800 6.3 7.9 (1) P. tabulaeformis plantation 1.31  0.14 a 2.36  0.29 b
(3) Mixed P. tabulaeformis West 18 17 1167 7.7 5.6 (2) R. pseudoacacia plantation 1.06  0.14 a 3.24  0.47 b
and R. pseudoacacia (3) Mixed P. tabulaeformis and 2.09  0.01 b 2.19  0.23 b
plantation R. pseudoacacia plantation
(4) P. orientalis plantation East 19 17 1517 4.9 3.4 (4) P. orientalis plantation 1.51  0.15 ab 1.46  0.07 a
(5) Natural P. davidiana forest West 15 20 1400 9.25 9.12 (5) Natural P. davidiana forest 2.52  0.41 b 1.94  0.19 ab

Different letter means significant variance by T-test at P < 0.05.

samples were collected on five subplots of 20  20 cm within each
plot, and oven-dried at 80  C to constant weight. The carbon stock
in both roots and litter was estimated from the root biomass and
litter mass based on conversion factor of 0.5 (Ma et al., 2002).
2.3. Soil respiration measurement
Soil respiration was measured at monthly intervals from May
through November in 2008 with an automated soil CO2 flux system
(LI-8100, Li-Cor Inc., Lincoln, NE., U.S.A.). Measurements were made
during 10:00e16:00 h on each scheduled day on five PVC collars
placed every 3 m along a diagonal transect on each plot, and soil
temperature at 10 cm depth and volumetric soil moisture content
(VMC) of the top 10 cm layer were measured concurrently near
the PVC collars. Upon completion of the final soil respiration
measurements, soil cores were taken 30 cm from each PVC collar
for determination of root biomass. Each PVC soil collar is 10 cm in
diameter and 5 cm in height, and 3 cm of the collar was inserted
into soil. Continuous and independent measurements of soil
temperature at the 10 cm depth were also made with an
automated climate station on a fixed location at the study site at
hourly intervals throughout the year of 2008 for extrapolating the
periodic measurements of soil respiration to annual soil CO2
efflux, and the logged value of soil temperature was calibrated
against the on-site measurements for each forest type prior to
the calculation of annual soil CO2 efflux.
The rate of soil respiration for each of the five forest types were
regressed with soil temperature for the entire measurement period
using the following equation (van’t Hoff, 1898):
ðT
10Þ=10
Rs ¼ R10  Q10s
where Rs is the measured soil respiration, Ts is the absolute value of
soil temperature at the depth of 10 cm, R10 is the basal soil respi-
ration rate at a reference soil temperature of 10  C, Q10 is the
temperature sensitivity of Rs, which represents the proportional
change in the rate of soil respiration with a change in soil
temperature by 10  C. R10 and Q10 were calculated according to the
Eq. (1) using the measured values of soil respiration (Rs) and soil
temperature (Ts) separately for each plot (Table 2).
Annual soil CO2 efflux was derived by linearly interpolating the
basal factors (R10 and Q10) from Eq. (1) and the following model
(Campbell et al., 2004):
X X ðT
10Þ=10
R ¼ Rsi  3600 s=h ¼ R10  Q10i  3600 s=h
where Rsi is the estimated rate of soil respiration at hour i and Ti is
the corresponding soil temperature at 10 cm depth that had been
automatically logged throughout the study period, s represents
second, h represents hour.
2.4. Soil sampling and analysis
In early September 2008, five soil samples to a depth of 20 cm
were taken by a cylindrical soil driller (4 cm diameter, 20 cm
height) on each plot, and air-dried in the laboratory to a constant
weight for soil chemical analyses. The air-dried soil samples were
ground to pass through a 0.2 mm sieve after any visible plant
tissues and debris were manually removed. Soil organic carbon
(SOC) content was estimated by the standard Mebius method
(Nelson and Sommers, 1982). Soil total nitrogen (TN) content was
analyzed using the Kjeldahl digestion procedure and ammonium
nitrogen (NH4eN) was colorimetrically analyzed by the alkali
method with a Tector Kjeltec System 1026 Distilling unit (Gallaher
et al., 1976).
Concurrently, soil bulk density was sampled by a cylindrical soil
driller of 100 cm3 in volume, and oven-dried at 110  C to constant
weight in laboratory. Soil carbon stock to 20 cm depth was calcu-
lated on the basis of the measured SOC content and soil bulk
density for each plot.
2.5. Data processing and analysis
A nonlinear least square fitting was applied to determine the
temperature response of soil respiration after natural log trans-
formation of the soil respiration data. The means in tables and
figures for each forest type were calculated by averaging values
from three replicated plots, each with five measurements. Test for
independent samples (i.e. nonparametric test and T test) was used
to examine the effects of forest type on soil respiration, and soil
chemical and physical properties, and to determine the differences
of biophysical variables among forest types. A stepwise linear
(1) model with a method of backward selection was applied to
discriminate the contribution of each biophysical variable to annual
soil CO2 efflux. All statistical analyses were performed using the
SPSS 15.0 program.
3. Results
3.1. Variation of soil respiration by forest type
Significant variation in annual soil respiration was detected by
nonparametric test (Chi-Square ¼ 11.97, P ¼ 0.018) across forest
types. Annual soil CO2 efflux differed by several orders of magni-
tude among the five types of forests. The amount of CO2 released
from soil to atmosphere was highest in the natural P. davidiana
(2) stand, followed by the mixed P. tabulaeformis and R. pseudoacacia
plantation, and was lowest in the P. orientalis plantation. On
average, the cumulative carbon loss was consistently higher in the
natural forest stand than in plantations, and was 55% greater in the
mixed P. tabulaeformis and R. pseudoacacia plantation than in other
three types of plantation (Fig. 2).

138
1600
Annual soil CO2 efflux (g C m yr-1)
1400
b
-2
1200
1000
a a
800
600
400
200
0 P. orientalis plantation had the highest soil temperature of 20.37  C,
Pinus nia nia cladu
Robi nus/Robi Platy
Pi
Vegetation type
Fig. 2. The annual soil CO2 efflux of different forest types during 2008. Different letters
above the bars mean significant differences by T-test at P < 0.05 in annual soil
respiration rates between different forest types (n ¼ 3). Pinus: pure P. tabulaeformis
plantation; Robinia: pure R. pseudoacacia plantation; Pinus/Robinia: mixed
P. tabulaeformis and R. pseudoacacia plantation; Platycladus: pure P. orientalis planta-
tion; Populus: natural P. davidiana forest.
The basal rate of soil respiration at 10  C, R10, and the temper-
ature dependency of soil respiration, Q10, were also markedly
influenced by forest types (Chi-Square ¼ 11.40, P ¼ 0.02 for R10; Chi-
Square ¼ 10.83 and P ¼ 0.03 for Q10). R10 was lowest in the
R. pseudoacacia plantation and highest in the natural P. davidiana
stand, which was about 21% higher than in the mixed
P. tabulaeformis and R. pseudoacacia plantation. However, Q10
showed a reverse trend with forest types compared to R10; Q10
value was lowest in the P. orientalis plantation and highest in the
R. pseudoacacia plantation. The natural P. davidiana stand had
a consistently lower value of Q10 than the plantations (Table 2).
Annual soil CO2 efflux ¼ 0:27  Root carbon stock þ 0:45  Carbon stock of both top soil and litter
65:68
 Soil temperature at 10 cm depth
108:27  Soil organic carbon content
 
þ 1654:74 R2 ¼ 0:933; F ¼ 35:06; P < 0:0001
Annual soil CO2 efflux was calculated separately for each plot on
the basis of the empirical functions (Eqs. (1) and (2)) and the soil
temperature monitored automatically by an automated climate
station. To ensure the generalization of the empirical functions in
the study, estimated soil respiration rate from Eq. (1) was validated
by the corresponding value measured instantaneously in the field.
Measured soil respiration can be expressed as a linear function of
the estimated soil respiration (y ¼
0.40 þ 1.18x; R2 ¼ 0.56,
P < 0.0001). The regression analysis indicated good agreement
between the estimated and measured values of soil respiration.
3.2. Effects of forest types on biophysical factors
We analyzed the full data set on the basis of averages of each
forest type when all biophysical variables were available, i.e. soil
properties, and carbon stocks in roots, litter, and top soil. Soil
Author's personal copy
Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143
b
organic carbon (SOC) content varied from 4.61 g kg
1 in the
R. pseudoacacia plantation to 29.58 g kg
1 in the natural P. davidiana
forest (Chi-Square ¼ 13.87, P ¼ 0.016). Soil total nitrogen (TN)
content was highest at 0.92 g kg
1 in the natural P. davidiana forest,
followed by the P. tabulaeformis plantation at 0.62 g kg
1, and
lowest at 0.27 g kg
1 in the R. pseudoacacia plantation (Chi-
Square ¼ 14.47, P ¼ 0.013). Values of soil C/N ratio were ranked in
the order of natural P. davidiana forest at 35.06 > P. tabulaeformis
a
plantation at 20.66 > R. pseudoacacia plantation at 17.08 > mixed
P. tabulaeformis and R. pseudoacacia plantation at
16.70 > P. orientalis plantation at 12.93 (Chi-Square ¼ 15.36,
P ¼ 0.009).
Mean soil temperature at a depth of 10 cm over the surveying
period was also remarkably influenced by forest types. The
s lus followed by the R. pseudoacacia plantation at 19.08  C; the natural
Popu
P. davidiana forest had the lowest mean value of soil temperature at
13.59  C (Chi-Square ¼ 14.99, P ¼ 0.01). No significant effect was
observed of forest types on soil moisture content to a depth of
10 cm (Chi-Square ¼ 2.59, P ¼ 0.763).
Significant differences were observed among different forest
types in carbon stock of top soil (Chi-Square ¼ 12.93, P ¼ 0.01).
Carbon stocks of the top soil and roots in the natural P. davidiana
forest were almost three times higher than in plantations (Fig. 3B,
C). For plantations, top soil carbon stock was lowest on the
R. pseudoacacia site and highest on the P. tabulaeformis site. The root
carbon stock was lowest in the P. orientalis plantation and highest in
the mixed P. tabulaeformis and R. pseudoacacia plantation. No
significant difference in litter carbon stock was observed among
different forest types (Fig. 3A; Chi-Square ¼ 5.47, P ¼ 0.24).
3.3. Variation of soil respiration with forest type and biophysical
factors
General linear regression analysis of the resulting data indicated
that annual soil CO2 efflux was largely determined by biophysical
variables with the following order by the value of standardized
(3)
coefficient (SC): soil organic carbon content (SC ¼
3.24; t ¼
4.69,
P ¼ 0.001) > combined carbon stock in top soil and litter (SC ¼ 2.70;
t ¼ 4.18, P ¼ 0.002) > root carbon stock (SC ¼ 0.96; t ¼ 0.495,
P ¼ 0.001) > mean soil temperature (SC ¼
0.51; t ¼
3.25,
P ¼ 0.009). The best-fit model of the general linear regression
analysis could be expressed by the following equation:
A first-order exponential function was also applied to evaluate
the effect of a single variable on annual soil respiration. Across
forest types, 62.8% of the variations in the annual soil CO2 efflux
were explained by combined carbon stock in roots, litter, and top
soil, 47.8% by combined carbon stock in litter and top soil, and 76.9%
by root carbon alone (Fig. 4). In contrast to the spatial variation of
annual soil CO2 efflux, the temporal variation of instantaneous soil
respiration mainly attributed to soil temperature at the 10 cm
depth, and about 11e40% of temporal variations were accounted for
by soil temperature depending on forest types (Fig. 5).
 Author's personal copy

Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143 139

500 4. Discussion
A a
4.1. The variation of soil respiration for different forest types
a
Litter carbon storage (g m-2)

400 a
a On a global scale, no matter what types of ecosystem and biome,
a annually cumulated soil CO2 emission has been found to be closely
300 related to the instantaneous rate of soil respiration (Bahn et al.,
2010). Annul soil CO2 efflux is often estimated by empirical
models based on continuously monitored environmental variables,
200 such as soil temperature and soil water content (Wang et al., 2006).
Sometimes, the sum of soil CO2 efflux in an annual cycle is
extrapolated by daily or monthly averages of soil respiration and
100 soil temperature at a reference time (Davidson et al., 1998; Bahn
et al., 2010). In the present study, annual soil CO2 efflux was
calculated by an empirical function (Eq. (2)) using the estimated
0 basic parameters (Q10 and R10) and hourly measurements of soil
5000 B temperature on each plot. The estimated cumulative soil CO2 efflux
in 2008 averaged 978.15 g C m
2 y
1 in this study, which closely
matched the mean value of 975.5 g C m
2 y
1 nationwide and fell
Root carbon storage (g m-2)

c
4000 well within the range from 236 g C m
2 y
1 to 3019 g C m
2 y
1
across different forest types in China (Chen et al., 2008). Compared
to temperate forests in northeastern China (Wang et al., 2006),
3000 warmer temperature may explain the higher annual soil CO2 efflux
of the forests in the semiarid Loess Plateau.
Within the same climate region, the site-to-site differences in
2000
ab vegetation type should be taken into account when evaluating the
variation in soil respiration (Borken et al., 2002). Normally, broad-
b ab leaved forests have higher rate of soil respiration than coniferous
1000 a
forests (Raich and Tufekcioglu, 2000). In our study, annual soil CO2
efflux was much higher in the natural P. davidiana forest than in
0 other plantations. This mainly attributed to the higher soil organic
8000
C carbon content and the higher carbon stocks in roots, litter, and top
soil in the natural P. davidiana forest, as it was shown in this study
Top soil carbon storage (g m-2)

d and other previous studies (Wang et al., 2006; Luan et al., 2011) that
6000 some biotic factors played a significant role in determining the
magnitude of annual soil CO2 efflux. For the plantations, the mixed
coniferous and broad-leaved forest site had a significant higher rate
of soil respiration than other types of forests. In a temperate region
4000 of northeastern China, Wang et al. (2006) also reported that annual
c soil respiration was almost 72% higher in broadleaved forests than
in coniferous forests. Therefore, soil carbon content and the amount
b of carbon in soil, roots and litter should be incorporated in models
2000 ab
predicting annual soil CO2 efflux.
a

4.2. The effects of soil variables on soil respiration and their

0 variations by forest types
Pinus nia nia us
Robi nus/Robi Platyclad
Pi
Vegetation type
Fig. 3. Organic carbon stocks in (A) litter, (B) root, and (C) top soil by different forest
types. Different letters above the bars mean significant differences by T-test at P < 0.05
between forest types (n ¼ 3). Bars are  SE of the means. Pinus: pure P. tabulaeformis
plantation; Robinia: pure R. pseudoacacia plantation; Pinus/Robinia: mixed
P. tabulaeformis and R. pseudoacacia plantation; Platycladus: pure P. orientalis planta-
tion; Populus: natural P. davidiana forest.
Except for a reverse trend, no statistical relationship was found
between volumetric soil moisture content and the instantaneous
rate of soil respiration for each forest type (data not shown). The
rate of soil respiration began to increase in late spring, peaked in
mid-August, and thereafter decreased to the minimum in early
winter. The volumetric soil moisture content was found to be
highest in early growing season and lowest in mid-August, and kept
slow increase until the measurement of soil respiration ended.
lus
Pop u
Soil environmental factors, including soil temperature and
moisture, and soil organic carbon content and microbial activities,
etc. (Wang et al., 2006; Luan et al., 2011), are essential for simu-
lating soil respiration of different vegetation types, because vege-
tation type influences soil respiration mainly through modification
of those variables (Raich and Tufekcioglu, 2000). Soil temperature
has been a predominant parameter used to construct the empirical
model of soil respiration (Pavelka et al., 2007), largely due to the
covariation of soil temperature and soil respiration in response to
the habitat perturbations. In this study, soil temperature well
explained the seasonal variations in soil respiration. Mean soil
temperature at the 10 cm depth during the study period was
significantly lower in the natural P. davidiana forest than in the
plantations, as soil temperature was reduced more by the dense
canopy in the natural P. davidiana forest than in other plantations
(Liu et al., 2005). No significant effect was exerted on the mean
value of volumetric soil moisture content by forest types at the
same time scale. This indicates that the soil moisture is mainly
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140 Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143

1800
Y = 1533.15 × (1 - e )
Annual soil CO2 efflux (g C m-2 yr-1)

Y = 1511.33 × (1 - e ) Y = 1437.74 × (1 - e )
1600 R = 0.628 R = 0.478 R = 0.769
P = 0.001 P = 0.0049 P < 0.0001
n = 15 n = 15 n = 15
1400

1200

1000

800 Pinus
Robinia
Pinus/Robinia
600 Platycladus

400
A B C Populus

0 2000 4000 6000 8000 10000 12000 0 2000 4000 6000 8000 0 1000 2000 3000 4000 5000
-2 -2 -2
Carbon storage of litter, root and top soil (g m ) Carbon storage of litter and top soil (g m ) Root carbon storage (g m )

Fig. 4. Relationships of annual soil CO2 efflux with organic carbon stock respectively in (A) litter, root and top soil, and in (B) litter and top soil, and in (C) root in the study region.

3.0
0.09x
Y = 0.18 e Y = 0.14 e0.10x
2.5 R2 = 0.34 2
R = 0.22
P < 0.0001 P < 0.0001
2.0 n = 75 n = 75

1.5

1.0

.5

0.0

-.5 Pinus Robinia

-1.0
3.5
Soil CO2 efflux (umol m-2 s )

0.06x 0.04x
-1

Y = 0.45 e Y = 0.34 e
3.0 R2 = 0.24 R2 = 0.11
2.5 P < 0.0001 P = 0.004
n = 75 n = 75
2.0
1.5
1.0
.5
0.0
-.5
-1.0 Pinus/Robinia Platycladus

3.5
Y = 0.63 e0.05x 0 5 10 15 20 25 30 35
3.0 2
R = 0.4
P < 0.0001
2.5 n = 75
2.0
1.5
1.0
.5
0.0
-.5 Populus

-1.0
0 5 10 15 20 25 30

Fig. 5. Relationships between soil CO2 efflux and soil temperature (10 cm in depth) for five forest types in the study region. All of the individual values represent the instantaneous
measurements of soil respiration rate and soil temperature for each investigated soil spot within each plot over the surveyed period (n ¼ 75). Pinus: pure P. tabulaeformis plantation;
Robinia: pure R. pseudoacacia plantation; Pinus/Robinia: mixed P. tabulaeformis and R. pseudoacacia plantation; Platycladus: pure P. orientalis plantation; Populus: natural
P. davidiana forest.
 Author's personal copy
Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143
controlled by the precipitation in this area. Soil nutrient content
was higher in the natural P. davidiana forest than in other forest
types, mainly due to the faster rate of litter decomposition in
broadleaved forests than in coniferous forests (Landsberg and
Gower, 1997). Consequently, higher soil resources in the soil
surface layer ultimately result in a greater rate of soil respiration
(Wang et al., 2006; Zhou and Shuangguan, 2009). In the P. orientalis
plantation, lower soil resources perhaps weakened the correlation
between soil respiration and soil temperature.
The temperature dependency of soil respiration, Q10, is another
overwhelmingly important parameter in predicting the soil respi-
ration rate at a given temperature (van’t Hoff, 1898; Davidson et al.,
1998; Pavelka et al., 2007), which depends not only on soil
temperature at different profile depths (Pavelka et al., 2007) but
also on the soil water condition (Jassal et al., 2008). Q10 value
changes with forest types (Grogan and Jonasson, 2005). In this
study with the forests of the semiarid Loess Plateau, the natural
P. davidiana forest, with the highest basal rate of soil respiration,
had a relatively low Q10 value, whereas the R. pseudoacacia plan-
tation had highest Q10 value and lowest basal rate of soil respira-
tion. The values of the estimated Q10 for all forest types in this study
compare well with the averaged Q10 values for the Loess Plateau
(Zhou et al., 2009) and are consistent with the median value of 2.65
for forest types across China (Chen et al., 2008). Modification of the
soil microclimate is a principal mechanism by which the Q10 values
vary among different forest types, as shown by the constraints on
temperature sensitivity of soil respiration by an increased
temperature and a decreased soil moisture content (Janssens and
Pilegaard, 2003; Conant et al., 2004).
The two important components of soil microclimate, i.e. soil
temperature and moisture, also determine the magnitude of soil
respiration (Conant et al., 2004). They both varied with forest types,
but kept a constant correlation with soil respiration in this study.
The rate of soil respiration displayed a positive correlation with soil
temperature at the 10 cm depth for all forest types, but the
contribution of soil temperature to the seasonal variation in soil
respiration was somewhat lower than previously reported values
(Burton et al., 1998). This may be largely attributed to the
complexity of soil CO2 efflux. Changes in a single process may be
masked by the opposite changes in another (Buyanovsky and
Wagner, 1995). The effect of temperature on soil respiration was
perhaps constrained by soil water condition, as suggested by the
findings that soil water deficits not only inhibit the soil respiration
rate (Jassal et al., 2008) but also affect the relationship between soil
respiration and temperature (Davidson et al., 1998).
The effects of soil moisture need be further assessed in pre-
dicting soil respiration rate, because its relationship with soil
respiration still remains controversial (Conant et al., 2004; Jassal
et al., 2008). In this study, soil respiration rate increased with
declining soil moisture content during the survey period. This trend
is consistent with the finding for a well drained forest stand
(Davidson et al., 1998), but deviates from the relationship between
soil respiration and volumetric soil moisture content observed in
other studies (Yan et al., 2006). At the beginning of our measure-
ments, the melting ice and snow over the soil surface resulted in
a large amount of soil water in the region of the Loess Plateau,
which almost reached soil water saturation condition for several
plantations (Zhu et al., 2006) and corresponded to relatively low
soil temperature of about 10  C at the 10 cm depth. The high water
content modifies the physical transportation of gas in soil, exacer-
bates the soil oxygen condition, and limits the biological activities
and the diffusion of CO2 (Dreyer, 1994). In a temperate mixed forest,
soil CO2 efflux was found to be greatly influenced by the interaction
between anaerobiosis and low soil temperature (Davidson et al.,
1998). Another controlling factor for the low soil respiration rate
141
in early growing season may be the dormancy due to the low
temperature. When weather became warm, plant growth, espe-
cially root growth, would undoubtedly accelerate, and soil respi-
ration would begin catching up. During the time span in our study,
the majority of soil water was likely extracted by the plant root
system to support growth, resulting in the decreased soil moisture
content seen late in growing season for all forest types. Further-
more, it has been found that poor litter accumulation on forest floor
(Yu et al., 2006) and soil desiccation (Wang et al., 2008) are
responsible for reduced contribution of heterotrophic respiration to
total soil CO2 efflux in the semiarid Loess Plateau.
4.3. The effects of carbon stock on soil respiration and its variation
by forest types
Carbon stocks in soil, roots and litter significantly contribute to
ecosystem CO2 efflux through manipulating autotrophic and
heterotrophic respiration (Grogan and Jonasson, 2005; Jassal et al.,
2008), but these variables are less considered than soil temperature
and moisture in computing soil respiration. General linear regres-
sion analysis of resulting data show that annual soil CO2 efflux was
significantly correlated with the root carbon stock, the combined
carbon stock in litter and top soil, and the combined carbon stock in
roots, litter, and top soil in this study with forests of the semiarid
Loess Plateau. Combined carbon stock in roots, litter and soil
explained about 63% of spatial variations in the annual soil CO2
efflux; combined carbon stock in litter and top soil explained 48%;
and root carbon stock alone explained 77%. We found that annual
soil CO2 efflux could be well simulated by the empirical function
incorporating carbon stocks in addition to soil temperature for
temperate forest ecosystem at the semiarid Loess Plateau.
A recent study has demonstrated that annual soil CO2 efflux
positively correlates with soil organic carbon concentration and
root biomass in temperate forests of Northeast China (Wang et al.,
2006). This largely ascribes to the effects of carbon stocks in roots
and litter on the production of detritus and exudates for soil
microbial activities (Raich and Tufekcioglu, 2000). The amount of
CO2 released from soil microorganisms accounts for 10e90% of the
total soil CO2 efflux depending on the condition and types of forest
ecosystems (Hanson et al., 2000). Significant variations in carbon
stocks in roots and top soil were observed among different forest
types within the same catchment in this study. Carbon stocks in
both top soil and roots were significantly higher in the natural
P. davidiana forest than in plantations. The values of root biomass
for the five forest types in our study fell well within the range re-
ported by other studies for temperate forests (Li and Ren, 2004).
Intriguingly, the total carbon respired annually from these
forests, both forest floor and mineral soil, in this study almost
equaled root carbon stocks in plantations and accounted for about
50% root carbon stock in the natural forest stand, and was much
higher than the litter carbon stocks across all forest types. On
average, the mean annual soil CO2 efflux within the watershed
studied was slightly greater than the mean net primary produc-
tivity (NPP) at about 550 g C m
2 yr
1 for temperate forest
ecosystems of China (Jiang et al., 1999).
5. Conclusion
Soil temperature is the most predominant variable controlling
seasonal variation of soil respiration in the semiarid Loess Plateau
of China. The annual soil CO2 efflux, calculated by the empirical
model using the automatically monitored data of soil respiration at
the 10 cm depth, varied from 647.71 g C m
2 yr
1 in the P. orientalis
plantation to 1448.50 g C m
2 yr
1 in the natural P. davidiana forest.
In addition, a stepwise linear regression analysis of resulting data
 Author's personal copy
142 Z. Zhou et al. / Soil Biology & Biochemistry 57 (2013) 135e143
suggests that the estimated annual soil CO2 efflux could be well
predicted by carbon stocks in roots, litter, and top soil. The
magnitude of annual soil carbon emission was determined
primarily by soil organic carbon content, secondly by combined
carbon stocks in litter and top soil, and thirdly by root carbon stock;
whilst soil temperature played a weaker role in explaining the
variations of annual soil CO2 efflux across forest types. A first order
exponential analysis indicated that spatial variations of annual soil
CO2 efflux across different forest types was explained 63% by
combined carbon stocks in roots, litter, and top soil, 48% by
combined carbon stocks in litter and top soil, 77% by root carbon
stock alone. These findings highlight the greater importance of
various carbon pools in predicting annual soil CO2 emission than
soil temperature under the same climatic conditions, or within the
same watershed, in the semiarid Loess Plateau of China.
Acknowledgments
This study was funded by a grant from the Ministry of Science
and Technology of China for rural development in the 12th Five
Year Plan. Partial financial support was also provided by Beijing
Forestry University for innovative research and faculty develop-
ment. The authors gratefully acknowledge the Chinese National
Ecosystem Observation and Research Station (Jixian, Shanxi) for
giving access to conduct field work on its experimental sites and for
the supply of meteorological data. We thank Junting Guo, Caifeng
Liu, Min Yu, Na Zhao, Rui Zhang, Bo Zhang, Guangsong Shi, and
Gaomin Wang for their field assistance. Thanks also extend to
Xiangping Wang, Qing Zhang and Jingwen Li for their insightful
advices on data analysis. Two anonymous reviewers were greatly
appreciated for their constructive comments on the manuscript.
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