vegetation cover and rain timing co-regulate the responses of soil

at SciVerse ScienceDirect

Soil Biology & Biochemistry 49 (2012) 114e123

Contents lists available

Soil Biology & Biochemistry

journal homepage: www.elsevier .com/locate/soi lbio

Vegetation cover and rain timing co-regulate the responses of soil CO2 effluxto rain increase in an arid desert ecosystem

Weimin Song a,b, Shiping Chen a, Bo Wu c, Yajuan Zhu c, Yadan Zhou a,b, Yonghua Li c, Yanli Cao c,Qi Lu c, Guanghui Lin d,*

a State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, ChinabGraduate University of Chinese Academy of Sciences, Beijing 100049, Chinac Institute of Desertification Studies, Chinese Academy of Forestry, Beijing 100091, ChinadMinistry of Education Key Laboratory for Earth System Modeling and Center for Earth System Science, Tsinghua University, Beijing 100084, China

a r t i c l e i n f o

Article history:Received 17 October 2011Received in revised form9 January 2012Accepted 31 January 2012Available online 14 February 2012

Keywords:Soil respirationPrecipitation changeSoil moistureTemperature sensitivityRoot activityNitraria tangutorum

* Corresponding author. Tel./fax: þ86 10 62797230E-mail address: [email protected] (G. Lin).

0038-0717/$ e see front matter � 2012 Elsevier Ltd.doi:10.1016/j.soilbio.2012.01.028

a b s t r a c t

Climate models often predict that more extreme precipitation events will occur in arid and semiaridregions, where C cycling is particularly sensitive to the amount and seasonal distribution of precipitation.Although the effects of precipitation change on soil carbon processes in desert have been studiedintensively, how vegetation cover and rain timing co-regulate the responses of soil CO2 efflux toprecipitation change is still not well understood. In this study, a field manipulative experiment wasconducted with five simulated rain addition treatments (natural rains plus 0%, 25%, 50%, 75%, 100% oflocal annual mean precipitation) in a desert ecosystem in Northwest China. The rain addition treatmentswere applied with 16 field rain enrichment systems on the 10th day of each month from May toSeptember, 2009. Soil water content, soil temperature and soil CO2 efflux rates were measured in bothbare and vegetated soils before and after the rain addition during a 3-week period for each rain treat-ment. The response magnitude and duration of soil CO2 efflux to rain addition depended not only on therain amount but also on the type of vegetation covers and the timing of rain addition treatments. Soilwater content responded quickly to the rain addition regardless of rain amount and timing, but soil CO2

efflux increased to rain addition only in MayeJuly but not in late growing season (September). Inaddition, soil CO2 efflux from the bare and vegetated soils showed similar increase to rain additions inMayeJuly, but they demonstrated distinct responses to rain addition in September. The differences in theresponses of soil CO2 efflux to rain addition between the bare and vegetated soils could be explained bythe root activities stimulated by added rain water, while the difference in soil CO2 efflux response to rainaddition among treatment times could be attributed to soil water condition prior to rain addition and/orsoil temperature drop following rain addition. Thus, both vegetation cover and rain timing can co-regulate responses of soil CO2 efflux to future precipitation change in arid desert ecosystems, whichshould be considered when predicting future carbon balance of desert ecosystems in arid and semiaridregions.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Desert and semiarid ecosystems cover about 35% (equivalent to5.2 billion hectares) of Earth’s land surface (Stone, 2008) and store15.5% of the world’s total soil organic carbon (SOC) (Lal, 2004).Restricted by high frequency drought stress, low nutrient levels andlow vegetation cover, desert and semiarid regions have long beenconsidered C-neutral or C-sources in the terrestrial carbon cycle.However, recent studies (Wohlfahrt et al., 2008; Xie et al., 2009)

.

All rights reserved.

suggest that desert ecosystems may be the “missing sink” foratmosphere CO2, but these findings were challenged by severaldesert ecologists (Schlesinger et al., 2009).

In desert and semiarid regions, many fundamental aspects ofecosystem structure and function are closely linked to spatial andtemporal patterns of water availability. IPCC (2007) has predictedmore extreme climate regimes would occur in mid-latitude regionswith increasing total precipitation amount and frequency ofextreme rainfall events. Changes in precipitation could alterdynamics of soil water availability, with significant consequencesfor ecology and biogeochemistry, particularly in these water-limited ecosystems (Fay et al., 2008; Knapp et al., 2008;

mailto:[email protected]

www.sciencedirect.com/science/journal/00380717

http://www.elsevier.com/locate/soilbio

http://dx.doi.org/10.1016/j.soilbio.2012.01.028



W. Song et al. / Soil Biology & Biochemistry 49 (2012) 114e123 115

Noy-Meir, 1973; Weltzin et al., 2003). Thus, quantifying likelyresponses of C cycling processes to changing precipitation patternsis critical to our understanding of the roles of desert ecosystems inregulating global C cycling.

Soil CO2 efflux, the main pathway of CO2 release from soil to theatmosphere, includes two components, the autotrophic respirationof roots, and the heterotrophic respiration from decompositionprocesses of soil microbes (Inglima et al., 2009; Kuzyakov, 2006;Ryan and Law, 2005). In general, precipitation pulses affect soil CO2efflux directly through a change in soil moisture content and soiltemperature, and indirectly through impact on soil organic matteravailability and/or plant physiological activities (Cable et al., 2008;Tang et al., 2005a). Previous studies have documented that the twocomponents of soil CO2 efflux varied with precipitation alongregional gradients (Rodeghiero and Cescatti, 2005; Zhou et al.,2009). Small rain events only favored the activity of microorgan-isms in the topsoil (Austin et al., 2004), while large rain eventscould reach the root zone and trigger assimilation processes(Reynolds et al., 2004), and then transfer more labile carbonsubstrates downward to soil for microorganisms (Aanderud et al.,2011). A further complication is that increased soil water contentdoes not only restrict the diffusion of oxygen into the soil but alsothe diffusion of belowground-produced CO2 out of the soil (Linnand Doran, 1984; Sponseller, 2007). Most of these studies wereconducted in a laboratory environment (Liu et al., 2002; Sponseller,2007) or focused on short-term artificial precipitation experiments(Chen et al., 2008; Jin et al., 2009). However, precipitation affectssoil CO2 efflux in complex ways. Firstly, effects of precipitation onsoil CO2 efflux are linked to the frequency and intensity of precip-itation; frequent drying and wetting may diminish the precipita-tion effects due to exhaustion of the accessible organic matter(Borken and Matzner, 2009; Fierer and Schimel, 2002, 2003).Secondly, the response of soil CO2 efflux to precipitation changediffered according to moisture conditions. In the Sonoran desert,Cable et al. (2008) found that soil CO2 efflux response to rainfalladdition amplified at drier antecedent soil conditions and damp-ened under wetter antecedent soil conditions. Finally, the seasonaldynamics of plant physiological activity may also impact the rate ofsoil CO2 efflux in the changing precipitation future. For example, inmany semiarid and arid ecosystems, precipitation and plantphenology can affect the two components of soil CO2 effluxspatially and temporally (Carbone et al., 2008; Tang et al., 2005b).

Due to the complexity of responses of soil CO2 efflux toprecipitation pulses, manipulative experiments over a longer(seasonal or annual) timescale are needed to examine the effects ofprecipitation events on terrestrial C cycling. In addition, it isessential to distinguish the nature of the responses of soil CO2 effluxto the future precipitation scenario under different vegetationcovers. Any shift in dominant vegetation cover type and/or changein plant physiological activity can alter belowground nutrientsresources, and affect root and microbial activities (Huxman et al.,2004; Talmon et al., 2011). Thus, to predict responses of the Ccycle to future climate change, understanding how vegetationcover controls soil CO2 efflux is also important, particularly in dryand heterogeneous ecosystems.

In this paper, we conducted a manipulative experiment withfive levels of rain additions (natural rains plus0%, þ25%, þ50%, þ75%, þ100% of local annual mean precipitation)during a whole growing season of 2009 in a desert ecosystem ofnorthwestern China dominated by a shrub species Nitraria tangu-torum. Themain objective of this studywas to evaluate the combineeffect of rain timing and vegetation cover on the responses of soilCO2 efflux to rain addition. Our hypotheses were that: (1) theresponse of soil CO2 efflux to rain addition varies among treatmentmonths, considering the seasonal variation in environmental

conditions and vegetation activities, (2) soil CO2 efflux in thevegetated soils is more strongly affected by changes in rainfall thanthat in the bare soils, and (3) there is a synergistic effect betweenrain timing and vegetation cover on soil efflux response to rainaddition.

2. Materials and methods

2.1. Site description

The experiment was conducted in a desert ecosystem (Fig. 1),located between Badain Jaran Desert and Tengger Desert in MinqinCounty, Gansu province, China (102� 580 E, 38� 340 N). The area ischaracterized by arid continental climate, with an average annualtemperature of 7.8 �C (average maximum 23.2 �C in July andaverage minimum �9.6 �C in January). Annual average precipita-tion is 115 mm, mainly occurring between July and September. Thedominant soil type is aeolian sandy soil and the vegetation isdominated by a shrub species, N. tangutorum.

The experiment was carried out in a patchy landscape withN. tangutorum interspersedwith sand dunes, orientated northwest-southeast, and composed of two distinct types of vegetation covers.The northwest slope of the sand dunes was covered withN. tangutorum plants, while the southeast was bare soil (Fig. 1a andb). The mean height and size of the dunes was 0.9 � 0.1 m and14.2 � 1.4 m2, respectively. Plant cover was approximately 35%. Thephysiochemical properties of the 0e10 cm soil layer for the bare soiland vegetated soil are shown in Table 1.

2.2. Experimental design

A completely random design was used in this experiment, withfive rain addition treatments and four replicates for each treatment(113 m2 per plot, 20 plots in total). Five rain addition treatmentswere designed to simulate rain increase of 0% (CK), 25%, 50%, 75%and 100% of the long-term (1978e2008) average annual precipi-tation (115 mm) at the study site, respectively. During the growingseason (May to September) of 2009, the rain addition was appliedevery month and the rain amount added was 0, 5.8, 11.5, 17.3 and23.0 mm each time for the five addition treatments, respectively.Water was pumped into a tank from a well near the plots and thenirrigated into the plots via an irrigation systemwith a water-pump,water meters and spraying arms (Fig. 1c). The irrigation systemswere installed on the top of sand dune, and the two spraying armscould rotate freely approximately 0.3 m above the dune topuniformly sprinkling simulated rain over the treatment area. Theland area irrigated by each rain addition treatment system wasestimated at 113 m2, and the total land area receiving the same rainaddition treatment was about 450 m2. In order to reduce waterevaporation, the water treatments were carried out only in themorning when air temperature was relatively low and the air abovethe land surface was usually calm.

2.3. Soil CO2 efflux measurements

At the beginning of the experiment, two PVC soil collars (11 cmin diameter and 5 cm in height) were inserted into the bare andvegetated soil to a depth of 3 cm in each plot for measurement ofsoil CO2 efflux. Soil CO2 efflux (SR) was determined using anautomated soil CO2 flux system (LI-8100, LI-COR Inc., Lincoln, NE,USA). Soil CO2 efflux was measured on the day before the raintreatments and every two days afterward for a period of 20 dayseach month. In order to enhance the comparability of data, mostsoil CO2 efflux measurements were conducted only in the morningbetween 09:00 and 11:00 local time.

Fig. 1. Geographic location and Nitraria tangutorum desert ecosystem of the study site in Gansu Province, China. Bare soil (a) and Vegetated soil (b) represent the two dominantvegetation cover types at the study site where rain addition treatments were conducted using a spraying system.

W. Song et al. / Soil Biology & Biochemistry 49 (2012) 114e123116

2.4. Methods for estimating changes in soil CO2 efflux

In order to examine whether soil CO2 efflux rate was signifi-cantly affected by rain addition treatment relative to that in thecontrol plot, the following equation was used to describe the rela-tive change of soil CO2 efflux (DSR):

DSR ¼ 1n

Xn

i¼1

�ðSRti � SRt0Þtreat � ðSRti � SRt0Þck�

(1)

where SRti is soil CO2 efflux rate on the given day after rain additionand SRt0 represents soil CO2 efflux before rain addition treatment;the subscript “treat” and “ck” indicates the water addition treat-ment plots and the control plots, respectively; and n is the numberof days for each rain addition treatment. DSR > 0 means that after

Table 1Mean (�se) values of soil physiochemical properties at 0e10 cm depth and key biologic

Treatment Vegetation cover type SOM (%) Soil N (%)

CK Bare 0.10 (0.01) 0.006 (0.000)Vegetated 0.11 (0.01) 0.007 (0.000)

þ25% PPT Bare 0.12 (0.01) 0.007 (0.001)Vegetated 0.12 (0.02) 0.008 (0.000)




SOM: soil organic carbon; MBC: soil microbial biomass carbon; ANPP: aboveground netThe five treatments represent simulate rain increase of 0% (CK), 25% (þ25% PPT), 50% (average annual precipitation (115 mm) at the study site, respectively.

rain addition, soil CO2 efflux in the rain addition treatment wasincreased compared to the untreated control or the decrease in soilCO2 efflux was smaller than in the control.

2.5. Measurements of biotic and abiotic factors

At the same time when soil CO2 efflux measurements werecarried out, soil temperaturewasmeasured at the 10 cm depthwitha thermocouple connected to the LI-8100 system. In addition, soilsamples were collected in the 0e10 cm layer of the soils in each plotfor determination of soil gravimetric water content. The soilsamples were weighed immediately for wet weight and dried at105 �C for 48 h, then weighed for dry weight. The soil gravimetricwater content was calculated by the difference of wet and dryweight of soil samples.

variables of Nitraria tangutorum at the end of growing season in 2009 (n ¼ 4).

Soil C/N Soil pH MBC (%) ANPP (g m�2)

17.34 (2.45) 8.45 (0.13) 0.002 (0.0010)15.20 (0.15) 8.36 (0.12) 0.001 (0.0004) 57.6 (8.7)16.59 (0.07) 8.45 (0.10) 0.002 (0.0005)16.97 (2.29) 8.59 (0.13) 0.002 (0.0006) 61.5 (4.5)20.61 (2.60) 8.70 (0.14) 0.002 (0.0004)16.30 (1.72) 8.82 (0.01) 0.003 (0.0002) 83.2 (5.1)16.81 (1.05) 8.82 (0.02) 0.003 (0.0003)16.06 (2.06) 8.86 (0.04) 0.003 (0.0005) 105.6 (12.5)17.94 (2.12) 8.41 (0.13) 0.003 (0.0008)17.76 (1.82) 8.62 (0.14) 0.003 (0.0004) 211.0 (39.5)

primary productivity.þ50% PPT), 75% (þ75% PPT) and 100% (þ100% PPT) of the long-term (1978e2008)

Fig. 2. Daily precipitation and mean daily air temperature (Ta) during the experi-mental period from 1 May to 1 October, 2009 at the study site. The data were obtainedfrom an automatic weather station near the study site. Solid arrows represent thetiming of rain addition treatments.


At the end of the experiment, all plant material withina 1 m � 1 m quadrat from the vegetation covered area of each plotwas sampled to determine the aboveground biomass of plants.Leaves and new stems were separated. All of the plant sampleswere oven-dried at 70 �C for 48 h, and thenweighed. Abovegroundnet primary productivity (ANPP) was calculated as follow:

ANPP ¼ ðleaf dry massÞ þ ðnew stems dry massÞ (2)

Some ANPP could also occur as the growth of old stems, but thatwas not measured. However, the plants of N. tangutorum grow veryslowly in this arid region sowe assume that the growth of old stemswas negligible over a single growing season.

A small part of the dry leaf samples were used for leaf carbonand nitrogen content analyses. Soil samples of the 0e10 cm layerwere collected for soil organic carbon and nitrogen content anal-yses. Soil organic carbon contents were determined using thesulfuric acid and aqueous potassium dichromate (K2Cr2O7) mixturewith external heating (Nelson and Sommers, 1996). Leaf and soilnitrogen content were measured by the Auto-Kjeldahl method(Kjektec system 1026 Distilling Unit, Sweden). Soil microbialbiomass carbon (MBC) wasmeasured by the fumigationeextractionmethod (Vance et al., 1987). Briefly, a 30 g soil samplewas extractedby shaking for 30 min with 50 ml of 0.5 M K2SO4. Another 30 g soilsample was fumigated for 24 h with ethanol-free CHCl3, and thenthe CHCl3 was removed. Extractable C was determined by dichro-mate digestion as described by Lovell et al. (1995), and the differ-ence in the extracted C between the fumigated and non-fumigatedsoil was denoted as MBC. All the above measurements were con-ducted in the State Key Laboratory of Vegetation and Environ-mental Change, Institute of Botany, Chinese Academy of Sciences,Beijing, China.

2.6. Statistical analyses

One-way ANOVA was used to detect the effect of rain additionon soil water content, soil temperature and soil CO2 efflux, and todetect the differences between the bare soils and vegetated soilsunder a given rain addition treatment. Three-way ANOVAs wereused to examine the effects of vegetation cover type, samplingtime, rain addition amount, and their interactions on the threeresponse variables (i.e., soil water content, soil temperature and soilCO2 efflux) in the 1st, 2nd and 3rd week after each rain additiontreatment, respectively. Significances of the absolute change in soilCO2 efflux in comparison to the soil CO2 efflux in the control plot(DSR) in the 1st, 2nd and 3rd week after different rain additiontreatments were tested by repeated measurement analysis ofvariance. Regression analysis was used to evaluate a possible rela-tionship between soil CO2 efflux and soil moisture. All statisticalanalyses were performed using SPSS 16.0 (SPSS for Windows,Version 16.0, Chicago, IL, USA).

3. Results

3.1. Micromet, soil properties and vegetation characteristics of thestudy site

Seasonal variations in daily precipitation and mean daily airtemperature during the growing season of 2009 are shown in Fig. 2.The growing season precipitation was 80.6 mm from May toSeptember and the annual precipitation was 105.7 mm, witha maximum rainfall event of 25.8 mm occurred on August 18, 2009.The mean air temperature during the growing season was 20.5 �Cwith the highest daily mean temperature of 29.0 �C on July 18 andthe lowest one of 9.6 �C on September 20. Soil organic carbon and

nitrogen contents were very low in presence of both vegetationcover types, and there were no significant differences in these soilcharacteristics between the bare and vegetated soils (Table 1). Rainaddition treatments had no significant effects on soil microbialbiomass in both bare and vegetated soils. The aboveground netprimary productivity (ANPP) of N tangutorum was significantlyincreased by the rain addition treatments in the vegetated soils(Table 1) and no obvious aboveground biomass was detected in thebare soils.

3.2. Changes in soil water content and soil temperature

Soil water content (SWC) increased significantly in the bare andvegetated soils after the rain addition treatments in all monthsfrom May to September [showed here only for May (Fig. 3a and b),July (Fig. 4a and b) and September (Fig. 5a and b)]. The changemagnitude and duration of SWC in both bare and vegetated soilsdepended on the amount of rain added. As the rain additionamount increased, SWC increasedmore and the treatment-inducedhigher SWC lasted longer. During the 2009 growing season, therewas no significant difference in the mean SWC between the bareand vegetated soils. Both sampling time and rain addition amountshowed significant positive effects on SWC in both bare andvegetated soils in three weeks after rain addition treatments.However, no significant interactive effect on SWC was foundbetween vegetation cover type and sampling time or amongvegetation cover type, sampling time and rain addition amount inthe three weeks after each rain addition treatment (Table 2).

The time course of soil temperature (Ts) showed similar trendsto air temperature (Ta) during the rain addition treatment period inboth bare and vegetated soils in May (Fig. 3c and d), July (Fig. 4c andd) and September (Fig. 5c and d), respectively. Rain additiontreatment significantly decreased the Ts in the 1st week, but had noeffects on Ts in the 2nd and 3rdweek in both vegetation cover types(Table 2). There were no significant differences in Ts between thebare and vegetated soils during the entire experimental period. Nosignificant interactions were detected among vegetation covertype, sampling time and rain addition amount (Table 2).

3.3. Responses of soil CO2 efflux (SR) to rain addition treatments

Pulse response capability of SR after rain addition treatmentshowed clear seasonal variability in both bare and vegetated soils.Positive responses of SR occurred after rain addition treatment in

a b

c d

e f

Fig. 3. Changes of soil water content (SWC), soil temperature (Ts) and (SR) following different rain addition treatments in May in the bare soil and vegetated soil of a Nitrariatangutorum dominated desert ecosystem. Data are means � 1 se (n ¼ 4 soil CO2 efflux). SWC and Ts are the means for the 0e10 cm soil layer. Dotted arrows represent naturalprecipitation evens and solid arrows represent rain addition treatments.


May, June and August in both vegetation cover types. In July,decreased SR after rain addition treatment was found in bothvegetation cover types, where there were significant oppositetrends between the bare soils and vegetated soils in September. Thepeak of SR occurred in the first day after rain addition in May, Juneand August. In July, no peak pulse responses were found in bothvegetation cover types. In September, the peak pulse responseoccurred in the 7th day, while no response was detected in thevegetated soils. Due to these results, we selected May, July andSeptember for future analysis.

In May, rain addition treatment stimulated SR in both bare andvegetated soils for all treatments (Fig. 3e and f). SR increasedrapidly after each rain addition and then decreased gradually in alltreatment plots, but the magnitude and duration of such increasedepended on the amount of rain added (Fig. 3e and f). A smallnatural event of 3.1 mm onMay 13 increased SR in the control plotsbut did not have any obvious effects in the treatment plots (Fig. 3eand f). However, another natural rain event of 4.4 mm on May 27increased SR in both of the control and the treatment plots (Fig. 3eand f).

In July, there were several natural rainfall events (a total of8.9 mm of precipitation from July 7 to July 10) prior to the rain

addition treatments, and the rates of SR maintained at relativelyhigh levels in both bare and vegetated soils (Fig. 4e and f). Rainaddition treatment resulted in declined rates of SR in both bare andvegetated soils, but the trend decreased with increased rainfalltreatment (Fig. 4e and f).

In September, the rate of SR in the bare and vegetated soilsshowed different responses to rain addition (Fig. 5e and f). In thebare soils, SR under all rain addition treatments increased duringthe course of the experiment, and there were no significantdifferences in the mean rate of SR within the three weeks amongthe five rain addition treatments. The rain addition causeda decrease in SR in the vegetated soils, and in the treatment plotsthe rates of SR decreased more significantly than in the control plot(Fig. 5e and f).

During the growing season of 2009, the rain addition causedincreased seasonal mean SR. There were significant differences inthe rates of SR between the bare soils and vegetated soils under fiverain addition treatments, and the rate of SR in the vegetated soilswere significantly higher than those in the bare soils. The rainaddition amount, sampling time and vegetation cover type allshowed significant effect on SR in three weeks right after each rainaddition (Table 2). Significant interactions between vegetation

a b

c d

e f

Fig. 4. Changes of soil water content (SWC), soil temperature (Ts) and soil CO2 efflux (SR) following different rain addition treatments in July in the bare soil and vegetated soil ofa Nitraria tangutorum dominated desert ecosystem. Data are means � 1 se (n ¼ 4). SWC and Ts are the means for the 0e10 cm soil layer. Dotted arrows represent naturalprecipitation evens and solid arrows represent rain addition treatments.


cover type and sampling time or rain addition amount were foundonly in the 2nd week following the rain addition (Table 2). Therewere no significant interactions on SR among the rain additionamount, sampling time and vegetation cover type (Table 2).

We used DSR to examine whether SR rate was significantlyaffected by the rain addition treatment relative to that in thecontrol plot. The rain addition caused significant increase in DSRduring the first three weeks after the rain addition treatment inboth vegetation cover types in May (Fig. 6aec) and July (Fig. 6def).In September, however, the rain addition resulted in a positiveresponse in the bare soils but caused a negative response in thevegetated soils (Fig. 6gei). The change of DSR was significantlydifferent between the bare and vegetated soils in May andSeptember. However, there was no significant difference in the DSRbetween the two vegetation cover types in July.

3.4. Relationship between soil CO2 efflux (SR) and soil watercontent (SWC)

In May and July, the rate of SR increased significantly withincreasing SWC (Fig. 7a and b). The relationships between SR andSWC could be well described by logarithmic functions in both bare

and vegetated soils. SWC variable alone could explain more than50% of the variations in SR rate during this period (Fig. 7a and b). InSeptember, the rate of SR was insensitive to the increase in SWC forthe bare soils (Fig. 7c). Although there was a significant logarithmicrelationship between SR and SWC in September for the vegetatedsoils, only 20% of the variations in SR could be explained by SWC(Fig. 7c).

4. Discussion

4.1. Response of soil CO2 efflux (SR) to rain addition treatments

We found that rain additions of 25e100% of the mean annualprecipitation (24e115 mm) during a growing season from May toSeptember caused about 22e47% increase in SR from the baresoils, and about 31e59% increase from the vegetated soils,respectively. This is strong evidence that soil water availabilitydetermines the carbon balance in this desert region. Similarfindings were also obtained in other arid and semiarid ecosystems(Jin et al., 2009; McCulley et al., 2007; Shen et al., 2009). Previousstudies documented that soils could accumulate labile organicsubstrates from microbial death and cell lysis, which stabilized soil

a b

c d

e f

Fig. 5. Changes of soil water content (SWC), soil temperature (Ts) and soil CO2 efflux (SR) following different rain addition treatments in September in the bare soil and vegetatedsoil of a Nitraria tangutorum dominated desert ecosystem. Data are means � 1 se (n ¼ 4). SWC and Ts are the means for the 0e10 cm soil layer. Solid arrows represent rain additiontreatments.


aggregates with soil organic matter during soil drying (Borken andMatzner, 2009; Harper et al., 2005; Unger et al., 2010). Further-more, soil microbial communities have the ability to survive andadapt to dry-rewetting cycles, so the quick response and recoveryof microbial activity and biomass to rain addition could contributeto the increase in carbon emission in arid ecosystems (Lee et al.,2004; Sponseller, 2007). However, our soil microbial biomassdata showed that the biomass of microbial communities at the endof the growing season was not significantly enhanced by the rainaddition. Because microbial respiration was the main componentof carbon emission in the bare soil, we hypothesized that high SRfollowing rain addition treatment was due to the enhancedmicrobial activities associated with mineralization of organicmatter. In addition, several previous studies showed that there wasa tight linkage between plant photosynthetic activity and soil CO2efflux (Gorissen et al., 2004; Harper et al., 2005; Tang et al.,2005a). In this study, aboveground net primary production(ANPP) of N. tangutorum was significantly enhanced by rainaddition. The increase in plant growth might supply more carbonsubstrate to roots, which could induce rhizosphere “primingeffect” (Kuzyakov and Domanski, 2000). Therefore, the increase in

SR in the vegetated soils was likely caused, at least in part, by plantresponses to the rain addition treatments.

In desert ecosystems, the landscape is frequently characterizedby a mosaic of bare and vegetated patches. Our results showed thatthe soils underneath shrub plants have higher rates of SR than thebare soils. Similar results were also reported in other arid ecosys-tems (Potts et al., 2008; Sponseller, 2007; Talmon et al., 2011). Weproposed that two factors could be responsible for the higherresponses of SR to rain addition in the vegetated soils than in thebare soils. The first factor is the contribution of root respiration. Thebare SR resulted mainly from heterotrophic respiration since therewere no obvious roots. In the vegetated soils, however, SR was thecombination of autotrophic and heterotrophic respiration. Raichand Tufekcioglu (2000) reported that about 10e90% of total SRwas derived from root respiration for most terrestrial systems. Thecontribution of root respiration in the vegetated soils resulted inthe difference in SR between the two cover types. The second factoris the availability of soil organicmatter. In comparisonwith the baresoils, the higher root biomass in the vegetated soils could supplylarger amounts of labile carbon for microbial respiration (Raich andTufekcioglu, 2000; Steenwerth et al., 2010).

Table 2Results of three-way ANOVA on the effects of vegetation cover type (V), rain additiontime (individual month, M), rain addition treatment (T) and their interactions on soilwater content (SWC), soil temperature (Ts), soil CO2 efflux (SR) for the threeresponse periods after rain addition treatments.

df SWC Ts SR

P P P

The 1st Week V 1 0.198 0.189 <0.001M 2 <0.001 <0.001 <0.001T 4 <0.001 <0.001 0.010V�M 2 0.520 0.789 0.048V �T 4 0.001 0.997 0.445M �T 8 <0.001 0.103 0.172V�M � T 8 0.674 0.999 0.980

The 2nd Week V 1 0.268 0.207 <0.001M 2 <0.001 <0.001 <0.001T 4 <0.001 0.456 <0.001V�M 2 0.044 0.388 <0.001V �T 4 0.299 0.802 0.040M �T 8 0.167 0.423 0.500V�M � T 8 0.662 0.656 0.904

The 3rd Week V 1 0.883 0.181 <0.001M 2 <0.001 <0.001 0.013T 4 <0.001 0.107 <0.001V�M 2 0768 0.629 0.036V �T 4 0.145 0.971 0.101M �T 8 0.467 0.816 0.716V�M � T 8 0.987 0.965 0.540


Weobserved dramatic pulses of SR in response to rain addition inboth bare and vegetated soils in the early growing season (May). Themagnitude of duration of increase in SR depended on the rainaddition amount. This is similar to findings reported in someprevious studies for Mediterranean ecosystems (Casals et al., 2007;Inglima et al., 2009; Steenwerth et al., 2010), semiarid grasslands(Chen et al., 2008; Yan et al., 2009) and incubation experiments (Liuet al., 2002; Sponseller, 2007). The rapid rewetting of extremely drysoil could increase availability of labile organic substrates through

a

b

c

Fig. 6. Mean relative change in soil CO2 efflux in comparison with the soil CO2 efflux in the cobare soil and vegetated soil of a Nitraria tangutorum dominated desert ecosystem. See the

microbial death and cell lysis (Huxman et al., 2004) and activatemicrobial metabolism (Borken and Matzner, 2009). Rain additiontreatments led to significant increases in SR (expressed as DSR) inboth vegetation cover types following the middle growing season(July) wet-up events, but the response magnitudes were muchsmaller than those in May. This result implied that prolonged soilwettingmight reduce substrate supply and availability for microbialmetabolism (Fierer and Schimel, 2002). The rates of SR of bothvegetation cover types showed significantly different responses torain addition treatments during the late growing period(September). A significant decrease in SR in the vegetated soilsfollowing rain addition in September suggested that, in addition toclimate, there are other factors that regulate the response of SR torain addition treatments. Generally, SR decreased in the late growingseason as a result of decreased plant photosynthetic activity (Harperet al., 2005). Therefore, the gradually decreased root activity andphotosynthetic substrate supply in the vegetated soilsmight explainthe significant decrease in SR observed in the late growing season.

4.2. Co-regulation of vegetation cover and rain timing on SRresponse to change in precipitation

We found a significant interactive effect between vegetationcover and rain timing on SR (Table 2), indicating that the vegetationcover type and rain timing co-regulate the responses of SR to rainaddition. In this study, rain addition tended to enhance the SRsimilarly in both vegetation cover types in May, indicating a soilwater availability limitation of the SR. However, the magnitude ofthe response was much smaller in July and even opposite (i.e. rainaddition reduced SR) for the vegetated soils in September. As thetwo main abiotic factors, soil temperature and water availabilityhave interactive effects on governing the seasonal trajectory of SR(Davidson et al., 1998). For example, in dry seasons, the responses ofSR to soil moisture were more significant than to temperature. Incontrast, SR was affected more by the soil temperature than soil

f

e

d g

h

i

ntrol plot (DSR) in the 1st, 2nd, 3rd week after different rain addition treatments in theMaterials and Methods section for detail calculation procedures of DSR.

September

SWC (%)0 2 4 6 8 10 12

0.0

0.5

1.0

1.5

July

-2 s

-1)

0.0

0.5

1.0

1.5

May

0.0

0.5

1.0

1.5

2.0

y = 0.16Ln(x) + 0.39 R2 = 0.57 P<0.001

y = 0.20Ln(x) + 0.57R2 = 0.51 P<0.001

y = 0.11Ln(x) + 0.39 R2= 0.60 P<0.001

y = 0.23Ln(x) + 0.72 R2 = 0.57 P<0.001

y = 0.10Ln(x) + 0.38 R2 = 0.20 P=0.001

Bare soilVegetated soil

Fig. 7. Relationships between soil CO2 efflux and soil water content in the bare soil (opencycles and dashed lines) and vegetated soil (filled cycles and solid lines) of a Nitraria tan-gutorumdominateddesert ecosystem in threemonths during the growing seasonof 2009.


moisture fluctuations under wet conditions (Almagro et al., 2009;Chen et al., 2008; Grüzweig et al., 2009). In this study, it was likelythat higher soil temperature in MayeJuly amplified respirationresponse to rain addition, while lower soil temperature inSeptember dampened respiration responses to rain addition. Inaddition, although increases in soil moisture induced by rain addi-tion were similar among the five rain addition treatments in bothvegetation cover types during the growing season, the responses ofsoil respiration were amplified by the dry antecedent conditionsrelative to wetter conditions. However, it has been previouslydemonstrated that there was a negative interaction between theresponse of soil respiration and antecedent soil water availability(Cable et al., 2008). We propose that high microbial activity underwetting soil may result in depletion of soil nutrients, which ulti-mately limits the response of the SR to episodic rain events.

As previously suggested, the soil could accumulate labile organicsubstrates, which stabilize soil aggregates with soil organic matterduring soil drying (Borken and Matzner, 2009; Harper et al., 2005;

Unger et al., 2010). Frequent drying and rewetting could diminish theeffects of a wetting pulse on heterotrophic component of SR due tolimitation of the labile substrate (Borken and Matzner, 2009; Fiererand Schimel, 2002). However, changes in the availability ofresources such as soil moisture could also modify plant growth andphysiological activity,which alsohave considerable consequences forsoil nutrient status. Given the evidence that SR is closely related toplant photosynthetic activity or phenological pattern at seasonaltimescales (Gorissen et al., 2004; Harper et al., 2005; Tang et al.,2005a), the presence of plants could stimulate autotrophic part ofSR by increasing C supply to the belowground (Huxman et al., 2004).Therefore, our study highlighted that short-term artificial rain addi-tion experiments are insufficient to adequately quantify seasonalvariation of SR. Furthermore, these results point to a novel findingthat rain timing and plant-driven changes in SR composition interactwith abiotic factors of the soil (temperature andmoisture) tomediatethe response of SR to rainfall variability in desert ecosystems.

Our results have important implications for constructingmechanistic models of SR in desert and semiarid ecosystems underthe influence of climate change. Global climate models predictfuture changes in precipitation scenarios with more extreme rainevents. Increasing heavy rainfall events will result in more soilcarbon emissions, while the photosynthetic activity of plants maybe triggered at the same time. This study contributes to a growingbody of evidence that a more precise prediction on the future rolesof desert ecosystems in terrestrial C balance should incorporate thebelow- and above-ground response of ecosystem components toepisodic water availability. Given the close relationship betweenplant physiological activity and SR at large temporal and spatialscales, additional study is required to scale results of case studiessuch as this to regional models.

Acknowledgments

This study was supported in part by grants from the Science andTechnology Foundation of the Chinese Academy ofForestry (CAFYBB2007008), the project of the State ForestryAdministration, the “Strategic Priority Research Program” of theChinese Academy of Sciences (201104077), Climate Change: CarbonBudget and Relevant Issues, the National Natural Science Founda-tion of China and a Selected Young Scientist Program of the StateKey Laboratory of Vegetation and Environment Change. GH Linwasalso supported by Tsinghua University’s start-up fund.

References

Aanderud, Z.T., Schoolmaster, D.R., Lennon, J.T., 2011. Plants mediate the sensitivityof soil respiration to rainfall variability. Ecosystems 14, 156e167.

Almagro, M., Lopez, J., Querejeta, J.I., Martinez-Mena, M., 2009. Temperature depen-dence of soil CO2 efflux is strongly modulated by seasonal patterns of moistureavailability inaMediterraneanecosystem.Soil Biology&Biochemistry41,594e605.

Austin, A.T., Yahdjian, L., Stark, J.M., Belnap, J., Porporato, A., Norton, U.,Ravetta, D.A., Schaeffer, S.M., 2004. Water pulses and biogeochemical cycles inarid and semiarid ecosystems. Oecologia 141, 221e235.

Borken, W., Matzner, E., 2009. Reappraisal of drying and wetting effects on C and Nmineralization and fluxes in soils. Global Change Biology 15, 808e824.

Cable, J.M., Ogle, K., Williams, D.G., Weltzin, J.F., Huxman, T.E., 2008. Soil texturedrives responses of soil respiration to precipitation pulses in the SonoranDesert: implications for climate change. Ecosystems 11, 961e979.

Carbone, M.S., Winston, G.C., Trumbore, S.E., 2008. Soil respiration in perennialgrass and shrub ecosystems: linking environmental controls with plant andmicrobial sources on seasonal and diel timescales. Journal of GeophysicalResearch-Biogeosciences 113, G09022.

Casals, P., Gimeno, C., Carrara, A., Lopez-Sangil, L., Sanz, M.J., 2007. Soil CO2 Effluxand Extractable Organic Carbon Fractions Under Simulated Precipitation Eventsin a Mediterranean Dehesa. 2nd International Conference on Rhizosphere.Pergamon-Elsevier Science Ltd, Montpellier, France, 1915e1922 pp.

Chen, S.P., Lin, G.H., Huang, J.H., He, M., 2008. Responses of soil respiration tosimulated precipitation pulses in semiarid steppe under different grazingregimes. Journal of Plant Ecology-Uk 1, 237e246.


Davidson, E.A., Belk, E., Boone, R.D., 1998. Soil water content and temperature asindependent or confounded factors controlling soil respiration in a temperatemixed hardwood forest. Global Change Biology 4, 217e227.

Fay, P.A., Kaufman, D.M., Nippert, J.B., Carlisle, J.D., Harper, C.W., 2008. Changes ingrassland ecosystem function due to extreme rainfall events: implications forresponses to climate change. Global Change Biology 14, 1600e1608.

Fierer, N., Schimel, J.P., 2002. Effects of drying-rewetting frequency on soil carbonand nitrogen transformations. Soil Biology & Biochemistry 34, 777e787.

Fierer, N., Schimel, J.P., 2003. A proposed mechanism for the pulse in carbon dioxideproduction commonly observed following the rapid rewetting of a dry soil. SoilScience Society of America Journal 67, 798e805.

Gorissen, A., Tietema, A., Joosten, N.N., Estiarte, M., Penuelas, J., Sowerby, A.,Emmett, B.A., Beier, C., 2004. Climate change affects carbon allocation to the soilin shrublands. Ecosystems 7, 650e661.

Grüzweig, J.M., Hemming, D., Maseyk, K., Lin, T., Rotenberg, E., Raz-Yaseef, N.,Falloon, P.D., Yakir, D., 2009. Water limitation to soil CO2 efflux in a pine forestat the semiarid “timberline”. Journal of Geophysical Research 114, G03008.

Harper, C.W., Blair, J.M., Fay, P.A., Knapp, A.K., Carlisle, J.D., 2005. Increased rainfallvariability and reduced rainfall amount decreases soil CO2 flux in a grasslandecosystem. Global Change Biology 11, 322e334.

Huxman, T.E., Snyder, K.A., Tissue, D., Leffler, A.J., Ogle, K., Pockman, W.T.,Sandquist, D.R., Potts, D.L., Schwinning, S., 2004. Precipitation pulses andcarbon fluxes in semiarid and arid ecosystems. Oecologia 141, 254e268.

Inglima, I., Alberti, G., Bertolini, T., Vaccari, F.P., Gioli, B., Miglietta, F., Cotrufo, M.F.,Peressotti, A., 2009. Precipitation pulses enhance respiration of Mediterraneanecosystems: the balance between organic and inorganic components ofincreased soil CO2 efflux. Global Change Biology 15, 1289e1301.

Intergovernmental Panel on Climate Change (IPCC), 2007. IPCC Fourth AssessmentReport e Climate Change 2007: the Physical Science Basis. Cambridge UnversityPress, Cambridge.

Jin, Z., Dong, Y.S., Qi, Y.C., Domroes, M., 2009. Precipitation pulses and soil CO2emission in Desert Shrubland of Artemisia ordosica on the Ordos Plateau ofInner Mongolia, China. Pedosphere 19, 799e807.

Knapp, A.K., Beier, C., Briske, D.D., Classen, A.T., Luo, Y., Reichstein, M., Smith, M.D.,Smith, S.D., Bell, J.E., Fay, P.A., Heisler, J.L., Leavitt, S.W., Sherry, R., Smith, B.,Weng, E., 2008. Consequences of more extreme precipitation regimes forterrestrial ecosystems. Bioscience 58, 811e821.

Kuzyakov, Y., 2006. Sources of CO2 efflux from soil and review of partitioningmethods. Soil Biology & Biochemistry 38, 425e448.

Kuzyakov, Y., Domanski, G., 2000. Carbon input by plants into the soil. Review.Journal of Plant Nutrition and Soil Science-Zeitschrift Fur PflanzenernahrungUnd Bodenkunde 163, 421e431.

Lal, R., 2004. Carbon sequestration in dryland ecosystems. EnvironmentalManagement 33, 528e544.

Lee, X., Wu, H.J., Sigler, J., Oishi, C., Siccama, T., 2004. Rapid and transient responseof soil respiration to rain. Global Change Biology 10, 1017e1026.

Linn, D.M., Doran, J.W., 1984. Effect of water-filled pore-space on carbon-dioxideand nitrous-oxide production in tilled and nontilled soils. Soil Science Societyof America Journal 48, 1267e1272.

Liu, X.Z.,Wan, S.Q., Su, B., Hui, D.F., Luo, Y.Q., 2002. Response of soil CO2 efflux towatermanipulation in a tallgrass prairie ecosystem. Plant and Soil 240, 213e223.

Lovell, R.D., Jarvis, S.C., Bardgett, R.D., 1995. Soil microbial biomass and activity inlong-term grassland e effects of management changes. Soil Biology &Biochemistry 27, 969e975.

McCulley, R.L., Boutton, T.W., Archer, S.R., 2007. Soil respiration in a subtropicalsavanna parkland: response to water additions. Soil Science Society of AmericaJournal 71, 820e828.

Nelson, D.W., Sommers, L.E., 1996. Total cabon, organic carbon. and organic matter.In: Page, A.L., et al. (Eds.), Methods of Soil Analysis, Part 2, second ed. Agronomy.Am. Soc. of Agron, Madison, WI.

Noy-Meir, I., 1973. Desert ecosystems: environment and producers. Annual Reviewof Ecology and Systematics 4, 25e47.

Potts, D.L., Scott, R.L., Cable, J.M., Huxman, T.E., Williams, D.G., 2008. Sensitivity ofMesquite Shrubland CO2 exchange to precipitation in contrasting landscapesettings. Ecology 89, 2900e2910.

Raich, J.W., Tufekcioglu, A., 2000. Vegetation and soil respiration: correlations andcontrols. Biogeochemistry 48, 71e90.

Reynolds, J.F., Kemp, P.R., Ogle, K., Fernandez, R.J., 2004. Modifying the "pulse-reserve" paradigm for deserts of North America: precipitation pulses, soil water,and plant responses. Oecologia 141, 194e210.

Rodeghiero, M., Cescatti, A., 2005. Main determinants of forest soil respiration alongan elevation/temperature gradient in the Italian Alps. Global Change Biology 11,1024e1041.

Ryan, M.G., Law, B.E., 2005. Interpreting, measuring, and modeling soil respiration.Biogeochemistry 73, 3e27.

Schlesinger, W.H., Belnap, J., Marion, G., 2009. On carbon sequestration in desertecosystems. Global Change Biology 15, 1488e1490.

Shen, W.J., Reynolds, J.F., Hui, D.F., 2009. Responses of dryland soil respiration andsoil carbon pool size to abrupt vs. gradual and individual vs. combined changesin soil temperature, precipitation, and atmospheric CO2: a simulation analysis.Global Change Biology 15, 2274e2294.

Sponseller, R.A., 2007. Precipitation pulses and soil CO2 flux in a Sonoran Desertecosystem. Global Change Biology 13, 426e436.

Steenwerth, K.L., Pierce, D.L., Carlisle, E.A., Spencer, R.G.M., Smart, D.R., 2010.A vineyard agroecosystem: disturbance and precipitation affect soil respirationunder Mediterranean conditions. Soil Science Society of America Journal 74,231e239.

Stone, R., 2008. Ecosystems - Have desert researchers discovered a hidden loop inthe carbon cycle? Science 320, 1409e1410.

Talmon, Y., Sternberg, M., Grunzweig, J.M., 2011. Impact of rainfall manipulationsand biotic controls on soil respiration in Mediterranean and desert ecosystemsalong an aridity gradient. Global Change Biology 17, 1108e1118.

Tang, J.W., Baldocchi, D.D., Xu, L., 2005a. Tree photosynthesis modulates soilrespiration on a diurnal time scale. Global Change Biology 11, 1298e1304.

Tang, J.W., Misson, L., Gershenson, A., Cheng, W.X., Goldstein, A.H., 2005b. Contin-uous measurements of soil respiration with and without roots in a ponderosapine plantation in the Sierra Nevada Mountains. Agricultural and ForestMeteorology 132, 212e227.

Unger, S., Maguas, C., Pereira, J.S., David, T.S., Werner, C., 2010. The influence ofprecipitation pulses on soil respiration e assessing the “Birch effect” by stablecarbon isotopes. Soil Biology & Biochemistry 42, 1800e1810.

Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuringsoil microbial biomass-C. Soil Biology & Biochemistry 19, 703e707.

Weltzin, J.F., Loik, M.E., Schwinning, S., Williams, D.G., Fay, P.A., Haddad, B.M.,Harte, J., Huxman, T.E., Knapp, A.K., Lin, G.H., Pockman, W.T., Shaw, M.R.,Small, E.E., Smith, M.D., Smith, S.D., Tissue, D.T., Zak, J.C., 2003. Assessing theresponse of terrestrial ecosystems to potential changes in precipitation.Bioscience 53, 941e952.

Wohlfahrt, G., Fenstermaker, L.F., Arnone, J.A., 2008. Large annual net ecosystemCO2 uptake of a Mojave Desert ecosystem. Global Change Biology 14,1475e1487.

Xie, J.X., Li, Y., Zhai, C.X., Li, C.H., Lan, Z.D., 2009. CO2 absorption by alkaline soilsand its implication to the global carbon cycle. Environmental Geology 56,953e961.

Yan, L.M., Chen, S.P., Huang, J.H., Lin, G.H., 2009. Differential responses of auto- andheterotrophic soil respiration to water and nitrogen addition in a semiaridtemperate steppe. Global Change Biology 16, 2345e2357.

Zhou, X.H., Talley, M., Luo, Y.Q., 2009. Biomass, litter, and soil respiration alonga precipitation gradient in Southern Great Plains, USA. Ecosystems 12,1369e1380.

vegetation cover and rain timing co-regulate the responses of soil

Documents