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Soil Biology & Biochemistry 58 (2013) 332e340

Contents lists available at SciVerse ScienceDirect

Soil Biology & Biochemistry

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

Carbon ux in deserts depends on soil cover type: A case study in the

Gurbantunggute desert, North China
Y.G. Su, L. Wu, Z.B. Zhou, Y.B. Liu, Y.M. Zhang*
Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, South Beijing Road 818, Urumqi,
Xinjiang 830011, China

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 22 April 2012
Received in revised form
19 November 2012
Accepted 14 December 2012
Available online 2 January 2013

Carbon ux represents carbon uptake from or release to the atmosphere in desert ecosystems, yet the
changing pattern of carbon ux in desert ecosystems and its dependence on soil cover type and
rainfall amount are poorly understood. We measured net carbon uxes (NCF) in soil with four cover
types (moss crusted soil, cyanobacteria/lichen crusted soil, bareland and semishrub Ephedra distachyainhabited site) from April to October of 2010 and 2011, and NCF and dark respiration (DR) after four
rainfall amounts (0, 2, 5, and 15 mm) in cyanobacteria/lichen crusted soil, bareland and the
E. distachya-inhabited site. NCF in the E. distachya-inhabited site differed signicantly from those of the
other three soil cover types, while no difference was observed between the moss and cyanobacteria/
lichen crusted soils or between the two crusted soils and bareland on most measurement occasions.
NCF ranged from
0.28  0.14 to 1.2  0.07 mmol m
2 s
1 in the biologically crusted soils, and from

2.2  0.27 to 0.46  0.03 mmol m
2 s
1 at the E. distachya-inhabited site. Daily NCF in the biologically
crusted soils and bareland showed carbon release at most times and total carbon production ranged
from 48.8  5.4 gC m
2 yr
1 to 50.9  3.8 gC m
2 yr
1, while the E. distachya-inhabited site showed
a total carbon uptake of
57.0  9.9 gC m
2 yr
1. Daily variances in NCF were well-explained by
variances in surface soil temperature, and seasonal NCF showed a signicant linear relationship with
soil moisture in the two biologically crusted soils and bareland when soil volumetric water content
was less than 3%. Rainfall elicited intense carbon release in cyanobacteria/lichen crusted soil, bareland
and at the E. distachya-inhabited site, and both NCF and DR were positive in the rst two days after
rainfall treatments. Mean NCF and DR were not different between rainfall amounts of 2, 5 and 15 mm
in cyanobacteria/lichen crusted soil and bareland, while they were signicantly higher after 15 mm
rainfall treatment compared with 2 mm and 5 mm treatments at the E. distachya-inhabited site. Mean
NCF and DR in the rst two days increased logistically with rainfall amount. Based on our ndings, we
suggest that E. distachya-inhabited sites contribute to carbon uptake in the Gurbantunggute Desert,
while biologically crusted soils exhibit carbon release for most of the year. Even though photosynthesis
immediately following rainfall can be stimulated, carbon uptake effect in biologically crusted soil is
likely intermittent and conned to periods when moisture is available.
2012 Elsevier Ltd. All rights reserved.

Keywords:
Arid and semiarid regions
Biological soil crusts
Carbon sink
Rainfall
Vascular plants

1. Introduction
Accurate assessment of carbon budget in variable ecosystems is
vital to our understanding and accurate estimation of the global
carbon balance (Schime et al., 2001; Korner et al., 2003), especially
considering the ever-increasing nature of carbon emissions
resulting from fossil fuel usage and land use changes (IPCC, 2007).
Compared with other ecosystems, deserts have received much less

* Corresponding author. Tel./fax: 86 991 7823149.

E-mail address: zhangym@ms.xjb.ac.cn (Y.M. Zhang).
0038-0717/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.soilbio.2012.12.006

attention in this regard because of their lower vascular plant

biomass (Whittaker, 1975) and soil carbon storage (Ojima et al.,
1993; Jobbgy and Jackson, 2000). Indeed, profound variances in
the vegetation pattern and large spatial heterogeneity in available
resources in desert ecosystems contribute to signicant uncertainty
in evaluating their roles as carbon sources or sinks (Schlesinger
et al., 1996; Jasoni et al., 2005; Wohlfahrt et al., 2008; Xie et al.,
2009; Liu et al., 2012). Most studies conducted so far have shown
either that deserts are a source of carbon or that they are carbon
neutral (Schimel et al., 2001). However, some recent studies have
shown evidences of carbon sinks in deserts, and these ndings
make deserts potentially valuable in efforts to mediate climate

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Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

change compared to temperate forests or grassland ecosystems

(Jasoni et al., 2005; Wohlfahrt et al., 2008; Xie et al., 2009). For
example, in a sandy desert ecosystem containing deciduous semishrubs (Caragana korshinskii and Artemisia ordosica), slight carbon
xation of 13.87e23.36 g C m
2 yr
1 has been observed. Moreover,
in the Mojave desert, which is dominated by the evergreen shrub
(Larrea tridentata (DC.) Cov.) and droughtedeciduous shrubs
(Lycium andersonii (A. Gray) and Ambrosia dumosa (A. Gray)),
carbon uptake of 102  67e185  15 g C m
2 yr
1 has been
observed (Jasoni et al., 2005; Wohlfahrt et al., 2008).
The species composition and vegetation cover of desert
ecosystems differ greatly (Noy-Meir, 1973). In mobile deserts,
vegetation cover is usually around 1% or less, and xeric shrubs or
semi-shrubs occur in these areas (Noy-Meir, 1973). By contrast, in
xed and semi-xed deserts, vegetation cover increases dramatically with precipitation, and can even exceed 40% when ephemeroid and ephemeral herbs are present under favorable soil
moisture conditions. Moreover, biological soil crusts develop and
are widely spread on the soil surface, where no vascular plants
develop in these regions (Belnap and Lange, 2003). In recent years,
articial planting in mobile sandy dunes (Li et al., 2003; Zhao et al.,
2010) and increasing annual rainfall (Wohlfahrt et al., 2008) have
changed vegetation structure, biomass as well as soil properties of
deserts. Such changes may potentially alter the magnitude of
carbon ux in desert ecosystems. In addition, vegetation structure,
which differs profoundly among deserts, interacts with environmental factors that control carbon cycling and affects carbon ux in
deserts (Raich and Schlesinger, 1992). For instance, greater vegetation cover usually induces more ecosystem carbon uptake
through increased photosynthesis (Wohlfahrt et al., 2008; Gao
et al., 2012) and reduced soil respiration, which is induced by
lower soil temperature (Luo and Zhou, 2006; Tesar et al., 2008). In
addition, since soil properties are always tightly associated with
vegetation patterns (Maestre and Cortina, 2002), changes in soil
properties may have signicant inuences on soil respiration,
which may indirectly alter carbon ux in desert ecosystems (Luo
and Zhou, 2006).
The carbon budget of deserts is largely driven by availability of
water to vegetation and soil microbes, as well as biological soil
crusts (Noy-Meir, 1973; Smith et al., 1997; Cable and Huxman,
2004). For instance, large carbon release is essentially conned to
a very limited period immediately after rainfall (Huxman et al.,
2004a, b; Veenendaal et al., 2004; Hastings et al., 2005; Potts
et al., 2006a, b; Kurc and Small, 2007), and signicant carbon
uptake may occur only several days after heavy rainfall events,
which increases the rate of photosynthesis in vascular plants (Gao
et al., 2012). Rainfall patterns in deserts also determine the tradeoff between carbon uptake (photosynthesis by autotrophs) and
carbon release (respiration by heterotrophs or dark respiration
from photoautotrophs) (Huxman et al., 2004b), specically, the
magnitude and duration of carbon ux are related to rainfall
amount (Huxman et al., 2004b) and the interval between consecutive rainfall events (Sponseller, 2007). For instance, biological soil
crusts are sensitive to all magnitudes of rainfall, whilst vascular
plants are only responsive to heavy rainfall, which can penetrate
into deep soil layers and reach the roots. Moreover, biological soil
crusts usually initially exhibit carbon release, then take up carbon
when moisture is available. Therefore, carbon balance in biologically crusted soil is affected by the duration of rainfall (Huxman
et al., 2004b).
The Gurbantunggute Desert is the biggest xed and semi-xed
desert in China. Its landscape is characterized by mosaic distribution of shrubs, semi-shrubs, biological soil crusts and bareland
(Zhang et al., 2007). As in the case of other dry lands, carbon
dynamics in the Gurbantunggute Desert is highly sensitive to

333

water availability (Xu et al., 2007). In the present study, two

hypotheses were proposed to explain the variances in net carbon
ux (NCF) in the Gurbantunggute Desert: (1) Photosynthesis in
vascular plants is usually higher than that of biological soil crusts
(Lange, 2003), in addition, though soil organic matter and soil
microbes in biologically crusted soils are higher than those in
vegetated sites and bareland (Table S1), soil respiration is usually
conned to very low values due to low soil moisture. Moreover,
soil moisture and temperature differ between measurement
periods, and variances in carbon ux might be linked with soil
moisture and temperature. Our rst hypothesis is that carbon ux
at different soil cover sites follows as the relationship: biologically
crusted soil > bareland > vegetated site, carbon ux varies with
soil temperature and soil moisture at different soil cover sites; (2)
Biological soil crusts can utilize a wide range of rainfall events to
initiate their physiological activities (Lange, 2003), and they
usually show respiration initially, and then photosynthesis occurs.
Vascular plants can only use large rainfall events that penetrate
into deeper soil layers and are accessible to roots, and small
amounts of rainfall only trigger carbon ux in the surface soil layer.
Our second hypothesis is then that rainfall translates into dramatic
increases in carbon efux from biologically crusted soil, bareland
and vegetated sites irrespective of rainfall magnitude, and that
carbon inux in biologically crusted soil and vegetated sites might
occur after relatively intense rainfall, which can trigger photosynthesis in crust organisms and vascular plants.
2. Materials and methods
2.1. Study site description
The Gurbantunggute Desert is located at the center of the
Jungger Basin in Xinjiang Uygur Autonomous Region of China. It is
the biggest xed and semi-xed desert in China with an area of
4.88  104 km2. Our experiment was conducted in the southern
part of the Gurbantunggute Desert (44.87 N, 87.82 E). Precipitation
occurs predominantly during spring, totaling approximately
79.5 mm. The mean annual evaporation is 2606 mm. The average
annual temperature is 7.26  C. Wind speeds are strongest during
late spring, averaging 11.2 m s
1 (Zhang et al., 2007). The well
developed soil surface cover contributes to the soil stability of the
Gurbantunggute Desert, which also benets from the native
vegetation and biological soil crusts. Ephedra distachya Linn. is one
of the dominant species in Jungger Basin, and is mainly distributed
on the sand slope and lower land between sand dunes. The average
canopy volume of an individual E. distachya is 44,602  1,0291 cm3
(Table S1), and its cover can reach 20% at the study site. Biological
soil crusts are widely distributed on soils between shrubs, usually
with a cover >60% (Table S1). Two types of biological soil crusts
dominate in this region: cyanobacteria/lichen and moss crusts
(Zhang et al., 2009). The cyanobacteria/lichen crusts usually exist in
every location in a sand dune, except at dune tops in some high
sand dunes. They are mainly composed of Microcoleus vaginatus
(Vaucher) Gomont ex Gomont, Microcoleus paludosus (Ktzing)
Gomont, Anabaena azotica Ley, Porphyrosiphon martensianus
(Meneghini ex Gomont) Anagnostidis & Komrek, Collema tenax
(Sw.) Ach., Psora decipiens (Hedw.) Hoffm., Xanthoparmelia desertorum (Elenkin) Hale., and Diploschistes muscorum (Schreb.) (Wu
et al., 2009). Moss crusts are typically located at the bottom of
dunes and form a mosaic with cyanobacteria/lichen crusts. They are
usually composed of Syntrichia caninervis Mitt., Bryum argenteum
Hedw., and Tortula muralis Hedw. The soil organic matter and total
nitrogen content, soil bulk density, and soil mechanical composition all differ largely among biologically crusted soil, bareland, and
E. distachya-inhabited sites (Table S1).

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Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

2.2. Experimental design

We selected the four most frequent soil cover types in the study
area to measure NCF from April to October in 2010 and 2011: (1) moss
crusted soil (with moss crusts cover >70%), (2) cyanobacteria/lichen
crusted soil (with cyanobacteria/lichen crusts more than 60%), (3)
bareland (biological soil crusts cover <5%), (4) E. distachya-inhabited
site. The cover of cyanobacteria/lichen crusts is usually more than ve
times that of moss crusts in the study area. We only investigated
the carbon ux in cyanobacteria/lichen crusted soil in the rainfall
treatment experiment. Consistent with other dryland (Sala and
Lauenroth, 1982; Loik et al., 2004), rainfall in this desert is small
and brief (2e5 mm). Small precipitation events (5 mm) account
for 87.5% of the total precipitation frequency and 47.5% of the
precipitation amount, while large precipitation events (10 mm)
account for 4.3% of the precipitation frequency and 26.6% of the
precipitation amount (Zheng et al., 2012). Therefore, we prescribed
four rainfall amounts, viz. 0 mm, 2 mm, 5 mm, and 15 mm in this study
with three independent replicates for each rainfall rate. Measurements of NCF, soil volumetric water content (SVWC), and soil
temperature (Ts) were taken based on a stratied random design. In
early April 2010, we randomly selected three plots in the moss crusted
site and 15 plots in the other three soil cover types (0.5 m  0.5 m)
(total n 48). Therein, three replicates were used for daily carbon ux
measurement from April to October in 2010 and 2011, and 12 replicates were used for rainfall treatments. In each plot, we inserted
a square aluminum frame (0.5 m  0.5 m) into the soil. Then, each plot
that fell within a distance of less than 3 m from an existing replicate
was discarded and reallocated to ensure a minimum distance of 3 m
between replicates. This was done to avoid potential inuences of
fertile islands of vascular plant and root respiration on carbon ux.
2.3. Carbon ux measurement
Carbon ux was measured using an infrared gas analyzer (IRGA;
LI-6400, Li-Cor, Lincoln, NE, U.S.) attached to a transparent polyvinylchloride chamber [0.5 m  0.5 m  0.25 m (height)]. The
chamber consisted of a parallelepiped of ve transparent polycarbonate walls (1.5 mm thick, allowing 92% photosynthetically
active radiation to pass into the plots) held together by a narrow
metallic angular frame (1 cm wide). During measurement, the
chamber was sealed to the frame surface. Two small electric fans
were installed and ran continuously in the chamber to promote air
mixing within the chamber during measurement. This method has
been validated by several previous studies (Steduto et al., 2002;
Huxman et al., 2004b; Potts et al., 2006b; Bubier et al., 2007; Risch
and Frank, 2007; Niu et al., 2010).
NCF was measured once a month for 24 h at 2 h intervals on
clear days from April to October in 2010 and 2011. For the rainfall
treatment experiment, carbon ux was initially measured at dry
conditions, then 0 ml (0 mm), 500 ml (2 mm), 1250 ml (5 mm), and
3750 ml (15 mm) distilled water was evenly sprayed over the soil
surface with a spray bottle. As for 5 mm and 15 mm rainfall
amounts, care was taken not to produce obvious runoff on the soil
surface. It usually took less than 1 min to spray 2 mm simulated
rainfall amount, and usually less than 7 min to spray 5 mm and
15 mm simulated rainfall amounts. After a simulated rainfall, dark
respiration (DR) was measured after NCF measurement. Initially, an
opaque cloth was placed on site for 10e15 min, and simultaneously,
the chamber was vented. DR was measured with the opaque cloth
covering the chamber. Carbon ux in rainfall treatments conditions
was measured at 0 min, 15 min, 30 min, 1 h, 2 h, 6 h, 12 h, 24 h, and
48 h after rainfall treatment.
For each measurement, nine consecutive CO2 concentration
recordings were taken at 10 s intervals over a 90 s period after

steady state conditions were achieved within the chamber. During

the measurement period, increases in air temperatures within the
chamber were <0.2  C. Only the data from the last 60 s were used to
calculate carbon ux following the soil-ux calculation procedure
described in the LI-6400 manual (LICOR Inc., 2004):

Fc

10VP0 1
W0 vC
RST0 273:15 vt

(1)

where Fc is the carbon ux rate (mmol m
2 s
1), V is the volume of

the assimilation chamber (cm3), P0 is the initial pressure (kPa), W0
is the initial water vapor mole fraction (mmol mol
1), R is the
universal gas constant (8.312 kJ mol
1 K
1), S is the soil surface area
(cm2), T0 is the initial air temperature ( C), and vC=vt is the slope of
least squares linear regression of CO2 concentration on time. During
the measurement of carbon ux, SVWC and Ts in the 0e5 cm soil
layer were also measured using a TDR (HH2-Delta T Device moisture meter, UK).
2.4. Statistical analysis
We rst calculated the daily mean value of NCF, then averaged
the daily values from April to October as seasonal mean values. We
calculated daily mean value multiplying days of a month, and
added values from April to October as total production in the
measurement year. We also calculated mean NCF and DR during the
rst two days after rainfall treatment, then averaged those values to
calculate average carbon ux. Values were ln-transformed prior to
the analysis to normalize their distribution. Repeated-measure
ANOVA was used with soil cover type (moss crusted soil, cyanobacteria/lichen crusted soil, bareland, and E. distachya-inhabited
site) as the subject factor to compare the effects of soil cover types
on NCF. One-way ANOVA was performed to test the effect of soil
cover types on total carbon production or uptake. The means were
compared with Tukeys honest signicance test. Two-way ANOVA
was used to compare the mean NCF and DR among the three soil
cover types (cyanobacteria/lichen crusted soil, bareland, and
E. distachya-inhabited site) and four rainfall amounts (0, 2, 5, and
15 mm). Subsequently, univariate analysis was performed for each
variable among different rainfall amounts. Exponential equations
were used to simulate the relationships between NCF and soil
temperature. Logarithmic regressions were conducted between
NCF and SVWC, and among mean NCF, mean DR and rainfall
amount. The signicance of regression coefcients were tested by
ANOVA. Statistical analyses were performed using SPSS software
(SPSS for Windows, Version 13, Chicago, IL).
3. Results
3.1. Net carbon ux and total carbon production in the four soil
cover types
NCF ranged from
0.28  0.14 to 1.18  0.09 mmol m
2 s
1 in moss
crusted soil, from
0.18  0.02 to 1.20  0.07 mmol m
2 s
1 in cyanobacteria/lichen crusted soil, and from
0.38  0.20 to
1.17  0.12 mmol m
2 s
1 in bareland. Daily NCF showed signal peak
curves for two biologically crusted soils and bareland, with the
highest values occurring in 14:00e16:00 (Fig. 1). NCF in two biological soil crusts and bareland was usually positive, with negative
values occasionally occurring at night (Fig. 1). Carbon ux uctuated
exponentially with air temperature at a day scale in both biologically
crusted soil and bareland, except in October 2010 (moss crusted soil:
r2 0.22e0.69, p < 0.01; cyanobacteria/lichen crusted soil:
r2 0.31e0.79, p < 0.01; bareland: r2 0.31e0.83, p < 0.01) (Fig. 1).
By contrast, E. distachya-inhabited sites showed carbon uptake

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Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

40

1.0 (a)

30

0.0

-1

10

-0.3
10
40
35
30
25
20
50

(c)

0.5
0.0
-0.5
-1.0
1.0 (e)

0
-2

20
40

0.5 (f)

30

-0.5

0.0

30

0.0

30

-1

40

0.5

40

1 (d)

Air temperature ( C)

-2

20

0.3

20

Net carbon flux (umol m s )

30

0.6 (b)

0.5
0.0
1.0

335

-1.0

-0.5
0.01 (g)
0.00

20
0.5 (h)
0.0
20
-0.5
Air temperature
MCS
CLCS
-1.0
BL
Ed S
-1.5
10
-2.0
8 10 12 14 16 18 20 22 0 2 4 6

20
15
10

-0.01
-0.02

5
8 10 12 14 16 18 20 22 0

Time of a day

Time of a day

Fig. 1. Temporal variations of net carbon ux (mmol m
2 s
1) and air temperature ( C) for moss crusted soil (MCS), cyanobacteria/lichen crusted soil (CLCS), bareland (BL) and
E. distachya-inhabited site (Ed S) in April (a, b), June (c, d), August (e, f), and October (g, h) in 2010 (a, c, e, g) and 2011 (b, d, f, h). Values are presented as the mean and standard error
of values on each sampling day.

during the day and carbon release at night, with values ranging
from
2.21  0.27 to 0.46  0.03 mmol m
2 s
1 (Fig. 1). Soil moisture
was highest in April and October, and lower values occurred in June
and August. Soil temperature was highest in August and lowest in
October. For these reasons, we only show NCF for April, June, August
and October of 2010 and 2011 in the present study (Fig. 1).
Seasonal NCF in biologically crusted soil and bareland
usually showed carbon release, ranging from
0.002  0.001 to
0.49  0.07 mmol m
2 s
1 in biologically crusted soils, and
from
0.001  0.001 to 0.44  0.01 mmol m
2 s
1 in bareland (Fig. 2).
Seasonal NCF at the E. distachya-inhabited site usually showed carbon
uptake, ranging from
0.58  0.13 to 0.09  0.02 mmol m
2 s
1

(a) 2010

20

60

-2

-2

1.0

40

TCP (gC m )

-2

(b) 2011
TCP (gC m )

1.5

-1

NCF (umol m s )

2.0

(Fig. 2). Repeated-measure ANOVA showed that NCF differed significantly among soil cover types (Table 1, p < 0.001) and measurement
times (Table 1, p < 0.001). Interactions between soil cover type and
measurement time had signicant effects on NCF (Table 1, p < 0.001).
When SVWC was lower than 3%, mean seasonal NCF was linearly
correlated with SVWC in both biologically crusted soils and bareland
(Fig. 3a, b and c, moss crusted soil: r2 0.47, p < 0.001; cyanobacteria/
lichen crusted soil: r2 0.73, p < 0.001; bareland: r2 0.37, p 0.001).
In contrast, when SVWC exceeded 3%, mean seasonal NCF did not
change with SVWC.
Total carbon production in the biologically crusted soils and
bareland ranged from 48.8  5.4 to 50.9  3.8 gC m
2 yr
1 (Fig. 2).

-20

MCS
CLCS
BL
Ed S

30
0

-30

0.5

-60

0.0
-0.5

MCS
BL

CLCS
Ed S

Apr. May Jun. Jul. Aug. Sep. Oct. Apr. May Jun. Jul. Aug. Sep. Oct.

Month of year
Fig. 2. Mean daily net carbon ux (NCF) (mmol m
2 s
1) from April to October in 2010 (a) and 2011 (b) and total carbon production (TCP) (gC m
2) from June to October in 2010 and
from April to October in 2011 in moss crusted soil (MCS), cyanobacteria/lichen crusted soil (CLCS), bareland (BL) and E. distachya inhibited site (Ed S). Different small letters indicate
signicant differences between soil cover types at p 0.05.

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336

Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

15 mm in cyanobacteria/lichen crusted soil and bareland (Table 4,

p > 0.05). Mean DR was well-described by logarithmic functions
incorporating rainfall for cyanobacteria/lichen crusted soil, bareland and the E. distachya-inhabited site (Fig. 4b), and mean NCF was
described by logarithmic functions incorporating rainfall at the
margin of signicance for cyanobacteria/lichen crusted soil and the
E. distachya-inhabited site (Fig. 4a).

Table 1
The effects of soil cover type (C), measurement time (T), and their interactions on
mean net carbon ux in a day (NCF) (mmol m
2 s
1) in 2010 and 2011.
Source of
variance

2010
df

2011
df

C
T
CT

3
4
12

52.9
31.8
8.5

<0.001
<0.001
<0.001

3
6
18

47.8
16.5
5.2

<0.001
0.001
0.001

4. Discussion
Our rst hypothesis was that carbon ux increases from vegetated site to bareland, is the highest in biologically crusted soil, and
varies with soil temperature and soil moisture availability. Our
ndings support this hypothesis. The variances in carbon ux were
large, and depended on the temporal and spatial scales. Due to the
close relation of NCF with soil organic matter, soil temperature, and
soil moisture, NCF showed both positive (carbon release) and
negative (carbon uptake) values, which is consistent with previous
reports (Unland et al., 1996; Emmerich, 2003; Maestre and Cortina,
2003; Hasting et al., 2005; Wohlfahrt et al., 2008; Gao et al., 2012).
In the present study, since no vascular plants and biological soil
crusts occurred in bareland, NCF in bareland results from soil
respiration and shows carbon releases for most of the year. By
contrast, carbon uptake occurred during the day at the E. distachyainhabited site, possibly because photosynthesis in E. distachya
offsets soil respiration. This indicates that E. distachya-inhabited
sites are responsible for carbon uptake in this region during most of
the year.
Moss crusted soil and cyanobacteria/lichen crusted soil showed
carbon release most of the time, which may be explained by the
following three mechanisms. First, photosynthesis in biological soil
crusts is rather low, and cannot offset soil respiration. Some laboratory studies and few eld experiments have reported photosynthesis in biological soil crusts (Lange, 2003), and biological soil
crusts have been reported to have an estimated median net carbon
uptake of 16 g m
2 yr
1 in drylands (Elbert et al., 2009). However, in

No difference was observed between the two biologically crusted

soils (Fig. 2, p > 0.05). Total carbon uptake at the E. distachyainhabited site was 57.0  9.9 gC m
2 yr
1 in 2011, which was
signicantly higher than that at the other three sites (Fig. 2,
p < 0.01).
3.2. Carbon ux in the three soil cover types in response to rainfall
amount
NCF and DR increased dramatically after rainfall (Fig. 4), and
returned to their original values after approximately 12 h in cyanobacteria/lichen crusted soil and bareland and after approximately 12 h of 2 mm and 5 mm rainfall at the E. distachya-inhabited
site. By contrast, their values remained high until 48 h after 15 mm
rainfall treatment at the E. distachya-inhabited site (Fig. 4). Rainfall
signicantly enhanced NCF (Table 3, p < 0.01) and DR (Table 3,
p < 0.01, Fig. 3b). Mean NCF differed signicantly among soil cover
types (Table 3, p < 0.01), and was the highest in cyanobacteria/
lichen crusted soil and lowest at E. distachya-inhabited site
(Table 2). By contrast, soil cover type had no inuence on DR
(Table 3, p 0.7). Mean NCF and DR in the three soil cover types
were signicantly higher at the sites that received rainfall
compared with the control sites (Fig. 4, p < 0.05). There was no
difference in mean DR among the three soil cover types under the
same rainfall amount (Table 4, p > 0.05). There was no difference in
mean NCF and DR between rainfall amounts of 2 mm, 5 mm, and

0.8

(a)

0.6

0.6

0.4

0.4

0.2

0.2

(b)

-2

-1

Mean net carbon flux (umol m s )

0.8

0.0

0.0

r =0.73, p<0.001

r =0.47, p<0.001
0.6
0.5

(c)

0.2
0.0

0.4

-0.2
O

0.3
0.2

-0.4

0.1

-0.6

0.0

r =0.37, p=0.001-0.8

-0.1

(d)

9 0

SVWC (%)

2
1

Fig. 3. Relationship of mean daily net carbon ux (NCF) (mmol m s ) with soil volumetric water content (SVWC) (%) in moss crusted soil (a), cyanobacteria/lichen crusted soil (b),
bareland (c), and E. distachya-inhabited site (d). Data were from April to October in 2010 and 2011 at each site, and were divided into two intervals of SVWC<3% (solid cycles) and
3% (open circles).

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Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

(a)

4
3

0 mm
5 mm

3
2
0

-1
4

-1
4

DR (umol m s )

-1

(b)

-2

-1

-2

(d)

4
2 mm
15 mm

NCF(umol m s )

337

2
1
0
-1
4

(c)

2
1
0
-1
4
2

-1

-1
0 0.25 0.5

(f)

-0.5

(e)

12

24

-0.5

48

Hour(s) after rainfall treatment

0 0.25 0.5

12

24

48

Hour(s) after rainfall treatment

Fig. 4. Dynamics of net carbon ux (NCF) (a, b, c) (mmol m
2 s
1) and dark respiration (DR) (d, e, f) (mmol m
2 s
1) in cyanobacteria/lichen crusted soil (CLCS) (a, c), bareland (BL)
(b, e), and E. distachya-inhabited site (Ed S) (c, f) after four precipitation treatments of 0 mm, 2 mm, 5 mm and 15 mm. Values are the mean  S.E.

a different study, no carbon uptake was found to occur in biologically crusted soil during a 3-month eld observation; even after
a 24 mm rainfall, biologically crusted soil was found to have
decreased carbon release compared with values prior to rainfall
(Maestre and Cortina, 2003). Secondly, photosynthesis in biological
soil crusts is not as persistent as that in vascular plants and likely
occurs intermittently and during specic conditions. Some studies
have shown that photosynthesis of biological soil crusts is intimately correlated with conditions prior to the availability of
moisture (Jeffries et al., 1993; Lange, 2003; Lange et al., 2007). Crust
organisms usually take several minutes to days (Lange et al., 1992;
Jeffries et al., 1993; Garcia-Pichel and Belnap, 1996; Harel et al.,
2004) to initiate photosynthesis after rainfall. We observed
carbon ux once a month, and did not observe carbon ux in
special weather conditions, such as periods of snow melting, dew
formation and rainfall, all of which may have stimulated photosynthesis in crusts organisms (Lange, 2003). Third, the frequent and
severe drought at our study site could explain the discrepancy
between our results and some previous studies (Thomas et al.,
2008). Precipitation was no more than 80 mm at our research
site, so biological soil crusts might have been dormant during our
measurements.
Soil water availability is a critical factor determining the alteration of plant species, plant physiological activity, and relative
ecological processes in deserts (Song et al., 2012). Consistent with
this, our study also shows dependence of carbon ux on soil water
availability when SVWC is less than 3% in both biologically crusted

soil and bareland, and that NCF does not change with SVWC when
SVWC exceeds 3%, This is closely related to the characteristics of
shallow distributions of soil organic matter, nutrients and soil
microbes in soil. Higher SVWC usually indicates that the deeper soil
is also wet, but deeper soil contributes considerably less carbon
release compared with shallow soil layer due to limited amount of
soil nutrients and soil microbes in them (Huxman et al., 2004b;
Thomas et al., 2008; Thomas and Hoon, 2010). In addition, higher
soil moisture may saturate soil pores, which impedes CO2 release to
the atmosphere (Sponseller, 2007; Thomas and Hoon, 2010). Our
ndings are consistent with the reports of a research study conducted in a desert grassland system in Arizona (Emmerich, 2003).
NCF varies from
22.6 to 5.6 mmol m
2 s
1 in the wet season, but
only has positive values in the dry season (Emmerich, 2003).
Variations in soil temperature alone can explain 22e83% of variances in daily NCF since soil moisture is almost consistent
throughout a day, and daily NCF in our study is comparable to
values measured at dry periods or in desert ecosystems with low
annual precipitations (Unland et al., 1996; Emmerich, 2003;
Hasting et al., 2005; Gao et al., 2012). In a shrub dominant desert,
carbon ux ranges from
0.75 to 0.5 mmol m
2 s
1 in a year with
annual precipitation of 147 mm (Hasting et al., 2005). Consistent
with this, daily NCF has been reported to range between
0.4 and
0.35 mmol m
2 s
1 prior to rainfall in the Sonoran desert (Unland
et al., 1996).
Carbon uptake in bareland and biologically crusted soil occasional occurred at night in August and September of both years in

Table 2
The effects of soil cover type (C), rainfall treatment (R), and their interactions
on mean net carbon ux (NCF) (mmol m
2 s
1) and dark respiration (DR)
(mmol m
2 s
1) in 48 h after rainfall treatments.

Table 3
Relationships between mean net carbon ux (NCF) (mmol m
2 s
1), mean dark
respiration (DR) (mmol m
2 s
1) and with rainfall amount (mm) in bareland (BL),
cyanobacteria/lichen crusted soil (CLCS), and E. distachya-inhabited site (Ed S).

Source of
variance

NCF
df

df

Soil cover NCF

type
Equation

C
R
CR

2
3
6

24.0
23.5
1.4

<0.01
<0.01
0.24

2
3
6

0.2
27.6
0.6

0.74
<0.01
0.69

BL
CLCS
Ed S

DR

DR
R2

Equation

R2

y 0.15Ln(x) 0.5 0.69 0.064 y 0.15Ln(x) 0.5 0.69 0.05

y 0.13Ln(x) 0.5 0.56 0.026 y 0.17Ln(x) 0.6 0.98 0.008
y 0.17Ln(x) 0.06 0.80 0.05 y 0.15Ln(x) 0.5 0.95 0.024

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Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

Table 4
Mean net carbon ux (NCF) (mmol m
2 s
1) and dark respiration (DR) (mmol m
2 s
1) in 48 h after rainfall amounts of 0 mm, 2 mm, 5 mm and 15 mm in cyanobacteria/lichen
crusted soil (CLCS), bareland (BL), and E. distachya-inhabited site (Ed S). Values are expressed as mean  S.E. Different small letters indicate signicant differences between
rainfall treatments, different capital letters indicate signicant differences between sites at p 0.05 level.
Rainfall
(mm)

NCF

0
2
5
15

0.23
0.68
0.88
0.87

DR

CLCS

BL





0.07Aa
0.19Ab
0.20Ab
0.09Ab

0.15
0.86
0.88
0.89

Ed S





0.02Aa
0.01Ab
0.04Ab
0.22Ab

0.26
0.02
0.27
0.67

CLCS





our study. In an adjacent study site, Xie et al. (2009) also observed
this carbon uptake at night. Moreover, they found that carbon
uptake was higher in drier soil, which was ascribed to alkaline soil
absorption (pH: 9.06  0.1e10.23  0.04). As no CAM plants grow in
our study area and soil pH in biologically crusted soil was
8.20  0.05, we speculate that the observed carbon uptake at night
might have resulted from alkaline soil absorption. However,
substantiating this speculation is difcult. On one hand, carbon
uptake is usually very low, and sometimes falls in the range of
instrument errors, making accurate detection with the analyzer
difcult. On the other hand, as this phenomenon occurred only
intermittently at our study site, measuring carbon uptake proved to
be difcult.
Partially in line with our second hypothesis, rainfall only translates into carbon release at the E. distachya-inhabited site, in cyanobacteria/lichen crusted soil and in the bareland. This is easily
explained in the case of bareland since they do not contain autotrophic species, and carbon ux observed after rainfall is actually soil
respiration. In biologically crusted soil, the effects of rainfall on
carbon ux are contradictory (Maestre and Cortina, 2003; Cable and
Huxman, 2004; Thomas et al., 2008; Thomas and Hoon, 2010).
Carbon release has been reported to occur in biologically crusted soil
irrespective of rainfall amounts (Cable and Huxman, 2004; Thomas
and Hoon, 2010). By contrast, Thomas et al. (2008) have shown
that cyanobacterial crusted soil exhibits carbon uptake at a rate of
0.14 mmol m
2 s
1 when the surface and subsurface soil is dry, and
carbon release at a rate of 1.3 mmol m
2 s
1 when the subsurface is
wet. Carbon ux in biologically crusted soil is the sum of photosynthesis or respiration in biological soil crusts and carbon release in the
soil below the biological crust layer. DR was usually higher than NCF
in cyanobacteria/lichen crusted soil in our study. This indicates that
rainfall has induced photosynthesis in crust organisms. Photosynthesis in cyanobacteria-dominated crusts is usually around or less
than 1 mmol m
2 s
1 (Lange et al., 1998; Zaady et al., 2000; Lange,
2003; Brostoff et al., 2005), Therefore, lower photosynthesis rate
cannot offset soil respiration in cyanobacteria/lichen crusted soil, and
cyanobacterial/lichen crusted soil has only shown carbon release.
There is no difference in NCF and DR among various rainfall amounts
in cyanobacterial/lichen crusted soil and bareland. This is primarily
due to soil organic matter and soil microbes distribution patterns at
those two sites. Soil organic matter and soil microbes mainly
concentrate at the soil surface (Table S1), and there is not enough
nutrient, substrate, and soil microbes to cause high soil respiration
even moisture is high at deep soil layers. No carbon uptake occurred
at the E. distachya-inhabited site after 15 mm rainfall. This could be
due to the short observation period after 15 mm rainfall, Photosynthetic rates of deep-rooted plants usually increase signicantly 1e5
days after an effective rainfall in arid regions (Hasting et al., 2005;
Hao et al., 2010; Gao et al., 2012; Liu et al., 2012).
In the Gurbantunggute Desert, rainfall is usually sporadic and
small, with the period between consecutive rainfalls being at least
several days or even weeks long (Zheng et al., 2012). Biological soil
crusts are dormant when they are dry, and they initially activate

0.02Ba
0.04Bb
0.12Bb
0.08Ac

0.22
0.67
0.96
1.09

BL





0.04Aa
0.18Ab
0.22Ab
0.10Ab

0.15
0.84
0.88
0.89

Ed S





0.02Aa
0.02Ab
0.04Ab
0.22Ab

0.23
0.57
0.89
0.99






0.04Aa
0.05Ab
0.06Ac
0.05Ac

respiration prior to photosynthesis when moisture becomes available. The longer the drought is before moisture availability, the
longer the respiration lasts in biological soil crusts (Lange et al., 1992;
Jeffries et al.,1993; Garcia-Pichel and Belnap,1996; Harel et al., 2004).
In contrast, E. distachya-inhabited site usually shows carbon uptake
when the surface soil is dry or after a large rainfall, and exhibits
carbon release after a small rainfall. Combining the physiological
activities of both biological soil crusts and E. distachya with the
rainfall pattern in this desert ecosystem, we can infer that
E. distachya-inhabited sites show carbon uptake and biologically
crusted soil acts as a carbon source for most of any given year.
However, carbon uptake in biologically crusted soil may be intermittent and is usually conned to special weather conditions, such as
melting of snow, consecutive rainfall, and heavy rainfall in deserts.
5. Conclusion
Arid and semiarid areas are characterized by a mosaic distribution of vascular plants and biological soil crusts. A better
understanding of carbon ux in fundamentally different soil covers
is necessary for identifying and studying the relationships between
carbon sinks and sources of desert ecosystems. Our study has
revealed that carbon ux differs considerably among sites with
different soil covers and among measurement times. Biologically
crusted soil typically showed carbon release during regular daily
measurement times from April to October in 2010 and 2011. In
contrast, the E. distachya-inhabited site showed carbon uptake for
most of the year. Rainfall elicited only carbon release in bareland,
cyanobacterial/lichen crusted soil and the E. distachya-inhabited
site. The magnitude of carbon release in cyanobacterial/lichen
crusted soil and bareland were the same irrespective of rainfall
amount. These ndings suggest that E. distachya-inhabited sites
contribute to carbon absorption while biologically crusted soil plays
an important role in carbon release for most of the year in the
Gurbantunggute desert. Moreover, since our experiments were not
conducted continuously throughout the year, and carbon ux
under special weather conditions when moisture became available
to biological soil crusts was ignored, biologically crusted soil might
have shown carbon uptake under these conditions. The novelty of
our study lies in the revelation that it is the vegetated sites, not
biologically crusted soil, that contributes to carbon uptake during
most of the year in the Gurbantunggute desert. This is in contrast to
previous studies implicating that biologically crusted soil, owing to
their extensive distribution and high photosynthetic capacity
(Austin et al., 2004; Belnap et al., 2004; de Soyza et al., 2005;
Sponseller, 2007), is responsible for carbon uptake in desert
ecosystems that show net annual carbon uptake (Jasoni et al., 2005;
Wohlfahrt et al., 2008; Xie et al., 2009).
Acknowledgments
The authors would like to thank Dr. Gang Huang for his
constructive suggestions during the realization of the manuscript,

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Y.G. Su et al. / Soil Biology & Biochemistry 58 (2013) 332e340

Junhui Chen for his eld work, as well as the two anonymous
reviewers for valuable comments on the manuscript. This work was
sponsored by the Chinese National Natural Scientic Foundation
(41001067, 31000217, U1203301, 2010FA92720-06), and West Light
Foundation of the Chinese Academy of Sciences (RCPY201101,
XBBS201007).
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.soilbio.2012.12.006.
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