SHORT COMMUNICATION

Effects of warming and increased precipitation on soil carbonmineralization in an Inner Mongolian grassland after 6 yearsof treatments

Xiaoqi Zhou & Chengrong Chen & Yanfen Wang &

Zhihong Xu & Zhengyi Hu & Xiaoyong Cui & Yanbin Hao

Received: 29 December 2011 /Revised: 28 March 2012 /Accepted: 29 March 2012# Springer-Verlag 2012

Abstract Understanding the responses of soil C mineraliza-tion to climate change is critical for evaluating soil C cyclingin future climatic scenarios. Here, we took advantage of amultifactor experiment to investigate the individual and com-bined effects of experimental warming and increased precip-itation on soil C mineralization and 13C and 15N naturalabundances at two soil depths (0–10 and 10–20 cm) in asemiarid Inner Mongolian grassland since April 2005. Foreach soil sample, we calculated potentially mineralizable or-ganic C (C0) from cumulative CO2-C evolved as indicators forlabile organic C. The experimental warming significantlydecreased soil C mineralization and C0 at the 10–20-cm depth(P<0.05). Increased precipitation, however, significantly in-creased soil pH, NO3

−-N content, soil C mineralization, andC0 at the 0–10-cm depth and moisture and NO3

−-N content atthe 10–20-cm depth (all P<0.05), while significantly de-creased exchangeable NH4

+-N content and 13C natural abun-dances at the two depths (both P<0.05). There weresignificant warming and increased precipitation interactionson soil C mineralization and C0, indicating that multifactorinteractions should be taken into account in future climaticscenarios. Significantly negative correlations were found be-tween soil C mineralization, C0, and

13C natural abundancesacross the treatments (both P<0.05), implying more plant-derived C input into the soils under increased precipitation.Overall, our results showed that experimental warming andincreased precipitation exerted different influences on soil C

mineralization, which may have significant implications for Ccycling in response to climate change in semiarid and aridregions.

Keywords Warming . Increased precipitation . Soil carbonmineralization . 13C natural abundance . Potentiallymineralizable organic carbon . Grassland

Introduction

As consequences of the rising concentrations of atmosphericgreenhouse gases, we are facing ongoing climate change(IPCC 2007). Global mean temperature has increased by0.76 °C and will continue to increase by up to 4 °C at theend of this century (IPCC 2007). Together with the risingtemperature, global and regional precipitation regimes arepredicted to change as well (Shen et al. 2009). As soilcontains twice as much as the amount of C in the atmo-sphere (Amundson 2001), a small change in soil C stockscan result in a large change in concentrations of atmosphericcarbon dioxide, thus exerting a feedback on climate change(Cox et al. 2000). Therefore, much research has been devot-ed to examine the effects of climate change on soil Cdynamics in terrestrial ecosystems (Bardgett et al. 2008;Davidson and Janssens 2006).

Many warming experiments have reported increases insoil C mineralization in ecosystems (Bardgett et al. 2008).By decomposing plant litter and soil organic matter, soilmicroorganisms contribute substantially to soil C minerali-zation (Wan et al. 2007; Zhou et al. 2007). Elevated tem-perature can directly stimulate soil microbial activities, but itsimultaneously enhances evapotranspiration, thus exacer-bating soil water stress, especially in semiarid and aridregions. Until now, few warming studies have been found

X. Zhou (*) :Y. Wang : Z. Hu :X. Cui :Y. HaoGraduate University of Chinese Academy of Sciences,Beijing 100049, Chinae-mail: zhou318@yahoo.com.cn

X. Zhou : C. Chen : Z. XuEnvironmental Futures Centre, Griffith University,Nathan 4111, Australia

Biol Fertil SoilsDOI 10.1007/s00374-012-0686-1

to inhibit soil C cycling in the field (Allison and Treseder2008; Liu et al. 2009) or under laboratory incubations(Zhang et al. 2005). Increased precipitation has been foundto increase soil C mineralization via increases in soil wateravailability (Wan et al. 2007). The majority of these studieshave focused on one single climate-changing factor. How-ever, little is known about the interactive effects of warmingand increased precipitation factors on soil C mineralizationin arid and semiarid ecosystems.

Soil organic C (SOC) can be modeled as several discretepools characterized by distinct mean residence time (Davidsonand Janssens 2006; von Lützow and Kögel-Knabner 2009).Labile organic C pool is the most active fraction of soilorganic matter and acts as a direct reservoir of readilyavailable nutrients for plants and microbes (Zhou et al.2011). Additionally, labile organic C pool exerts consid-erable control on soil C flux and ecosystem functioning(Allison and Treseder 2008). Cumulative CO2-C evolvedfrom laboratory incubations can be used to estimate soillabile organic C pool (Conant et al. 2008). In addition,laboratory incubations in combination with modeling fit-ting have been widely used to characterize soil potentiallylabile organic C (C0), which can be used as an indicatorfor labile organic C (Zhou et al. 2012a). Given that labileorganic C pool is closely associated with plant communitycomposition, soil 13C and 15N natural abundances follow-ing changes in vegetation offer an approach to betterunderstand soil organic matter dynamics in response toclimate change (Bijoor et al. 2008). In general, labile SOCderived from recent plant residues has lower 13C naturalabundances compared with SOC derived from old plantmaterials (Lynch et al. 2006). Differences in labile organicC under climate change may lead to differences in soil13C natural abundances.

The semiarid Inner Mongolian grassland in northern Chinais a part of the Eurasian grassland, which is the largest grass-land biome around the world. A long-term, ongoing multifac-tor experiment with experimental warming and increasedprecipitation has been conducted since April 2005 (Yanget al. 2011). Given the importance of soil water availabilityin this semiarid region (Liu et al. 2009), we hypothesized thatexperimental warming and increased precipitation would ex-ert different effects on soil C mineralization. The objectives ofthis study were to (1) examine the individual and combinedeffects of experimental warming and increased precipitationon soil C mineralization and soil 13C and 15N natural abun-dances and (2) quantify soil potentially mineralizable organicC to compare their effects on soil labile organic C at twodepths (0–10 and 10–20 cm). In situ soil respiration consistsof root respiration and microbial respiration. Here, laboratoryincubation method was used to only study soil C mineraliza-tion, i.e., microbial respiration, under climate change. Al-though this method has the disadvantage of using disturbed

soils, it allows controlling the environmental variables andmakes it easy to compare C mineralization from different soilsunder the same standardized conditions.

Materials and methods

Experimental site

This study site was established in late April 2005 in a semiaridtemperate steppe in Duolun County (42°02′ N, 116°17′ E,1,324 m a.s.l.), Inner Mongolia, China, which belongs tomonsoon climate of moderate temperature zone. Long-termmean annual precipitation and mean annual temperature areapproximately 383 mm and 2.1 °C, respectively. About 90 %of the total precipitation falls during the period from May toOctober, andmonthly mean temperature ranges from −17.5 °Cin January to 18.9 °C in July. The soil in this area is classifiedas chestnut according to Chinese classification or Haplic Cal-cisols according to the FAO classification with 62.75±0.04 %sand, 20.30±0.01% silt, and 16.95±0.01 % clay, respectively.Soil bulk density is 1.31±0.02 g cm−3 at the 0–10-cm depth.Soil organic C and total N contents are 20.86±3.53 and 1.87±0.31 g kg−1, respectively. The plant community at our exper-imental site is dominated by Stipa krylovii, Artemisia frigida,Potentilla acaulis, Cleistogenes squarrosa, Allium bidenta-tum, and Agropyron cristatum (Yang et al. 2011).

Experimental design

This experiment used a paired and nested design with fourtreatments (Yang et al. 2011). There were three blocks with anarea 44×28 m for each block. There was a pair of 10×15-mplots in each block, in which one plot was assigned as theincreased precipitation treatment and the other one as theambient precipitation treatment. Four 3×4-m plots were estab-lished in each 10×15-m plot with 1 m distance between theplots. The four plots were randomly assigned to warming andunwarmed control treatments with two replicates. Thus, therewere totally 24 plots with six replicates for each treatment[control (C), warming (W), increased precipitation (P), andwarming plus increased precipitation (WP)]. There were sixsprinklers arranged in two rows in each of the precipitationtreatment plot, with each sprinkler covering a circular areawith a diameter of 3 m. A total amount of 120 mm precipita-tion was applied under the increased precipitation treatment inJuly and August with approximately 15 mm week−1. Eachwarmed subplot was heated continuously by a 165×15-cmSR-2420 infrared radiators (Kalglo Electronics, Bethlehem,PA, USA) suspended 2.5 m aboveground since April 28, 2005[the heaters were turned off over the winter (November16–March 15) since 2007]. One “dummy” heater with thesame shape and size as the infrared radiator was used to

Biol Fertil Soils

simulate the shading effect of the infrared radiator in theunwarmed control subplot.

Soil sampling

Soil samples were collected from all subplots in early August,2010. In each subplot, two soil cores of 0–10- and 10–20-cmdepths were sampled using soil auger (8 cm in diameter). Afterpassing through 2-mm sieve, the soil samples were stored at4 °C and soil properties were measured within 1 week.

Soil property measurements

Soil moisture was determined after being oven-dried at105 °C overnight. Soil pH was measured at a 1:2.5 drysoil/water ratio. Soil exchangeable NH4

+-N and NO3−-N

contents were determined in the KCl extracts (Zhou et al.2012b). Briefly, field moist soil samples (5 g) were extractedwith 30 ml of 2 M KCl in an end-to-end shaker for 1 h andfiltered through a Whatman no. 42 paper. The concentrationof inorganic N was measured using a Lachat Quickchemautomated analyzer (Quick Chem method 10-107-064-D forNH4

+ and 10107-04-1-H for NO3−).

Measurements of soil 13C and 15N natural abundances

The air-dried soil samples were finely ground. Soil total Cand N contents and δ13C and δ15N were determined usingan Isoprime isotope ratio mass spectrometer with a Euro-vector elemental analyzer (Isoprime-EuroEA 3000). Soil Cand N isotope ratios are expressed in a relative δ notation(Zhou et al. 2011):

d ¼ RSAMPLE � RSTDð Þ RSTD=½ � � 1;000; ð1Þ

where RSAMPLE is either 13C/12C or 15N/14N ratios of thesample and RSTD is either 13C/12C or 15N/14N ratios of thestandard. Both carbon dioxide and N2 samples were analyzedrelative to internal working gas standards. Soil C isotope ratiosare expressed relative to Pee Dee Belemnite (δ13C00.0‰); Nisotope ratios are expressed relative to air (δ15N00.0 ‰).

Measurements of soil C mineralization and potentiallymineralizable organic C (C0)

Soil C mineralization was measured by a 70-day incubationas described by Chen et al. (2005). Field soil samples (30 gdry weight equivalent) were incubated aerobically in a 1-Lsealed jar at 22 °C in the darkness. The CO2-C evolved fromsoils over the incubation period (1, 3, 7, 14, 21, 28, 35, 42,49, 56, 63, and 70 days) was trapped in 0.1 M NaOH, andthe remaining NaOH was determined by titrating using

0.05 M HCl after precipitation of carbonate with 1 ml 1 MBaCl2. The cumulative CO2-C was calculated by the cumu-lative production of CO2 from the soils during the 70-dayincubation and expressed as milligrams of CO2-C per kilo-gram dry soil. A non-linear regression approach was used toestimate C0 and the first-order rate constant (k) (Zhou et al.2012a). The equation was Cm0C0×(1−exp−kt), where Cm

was the organic C mineralized (milligrams per kilogram) ata specific time (t). The Statistical Analysis System (SAS)was used to calculate C0 and k using SAS-ProcNLINprocedure.

Statistical analyses

For each soil depth, two-way analysis of variance (ANOVA)for a blocked split-plot design was used to determine themain and interactive effects of experimental warming andincreased precipitation on soil properties, δ13C, δ15N,cumulative CO2-C, and C0. Relationships between soilproperties, δ13C, δ15N, cumulative CO2-C, and C0 werecalculated based on Pearson’s correlation coefficients. Thedifferences were considered significant at P<0.05. AllANOVA and correlation analyses were performed withSAS v.8.1 software (SAS Institute Inc., Cary, NC, USA).

Results

Soil properties

Experimental warming marginally but significantly in-creased the contents of exchangeable NH4

+-N (P00.073)(Table 1; Fig. 1). However, no significant differences in soilmoisture, pH, and NO3

−-N contents under experimentalwarming were found at the two depths (Table 1; Fig. 1). Incontrast, increased precipitation marginally but significantlyelevated soil moisture at the 0–10-cm depth (P00.071),while significantly elevated it at the 10–20-cm depth. In-creased precipitation significantly elevated pH of the surfacesoils (P<0.01), while it significantly decreased exchange-able NH4

+-N contents (P<0.05) but significantly increasedNO3

−-N contents at the two depths (P<0.05). In the warmedplots, inorganic N was dominated by exchangeable NH4

+-N,while inorganic N under increased precipitation was domi-nated by NO3

−-N. No significant interactive effects of ex-perimental warming and increased precipitation were foundon soil moisture, pH, and exchangeable NH4

+-N and NO3−-

N contents (Table 1; Fig. 1).

Soil δ13C and δ15N

Experimental warming had no significant effects on soilδ13C and δ15N at the two depths (Table 1; Fig. 1). However,

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increased precipitation significantly decreased soil δ13C atthe two depths. There were no significant interactive effectsof experimental warming and increased precipitation on soilδ13C and δ15N at the two depths (Table 1).

Soil C mineralization and potentially mineralizable organicC (C0)

The CO2 evolution ranged from 28.7 to 47.8 mg CO2-C kg−1 dry soil day−1 and were generally the highest in alltreatments during the first 2 weeks of the incubation, andthis was then followed by a steady and strong decrease torates of 2.9 to 7.8 mg CO2-C kg−1 dry soil day−1 at the endof incubation. Cumulative CO2-C over the incubationdecreased in the order of warming plus increased precipita-tion > increased precipitation > control > warming in thesurface soils and in the order of increased precipitation >control > warming > warming plus increased precipitationin the subsurface soils (Fig. 2). Warming significantly de-creased cumulative CO2-C in the subsurface soils (P<0.05),while increased precipitation significantly enhanced it in thesurface soils (P<0.01; Table 1). Significantly interactiveeffects of warming and increased precipitation on cumula-tive CO2-C were detected in the surface soils (P<0.05).

The first-order exponential equation well described themineralization kinetics for all the treatments (all r200.99).After model fitting, soil C0 exerted a similar pattern ascumulative CO2-C at the two depths among the treatments(Fig. 1). Experimental warming significantly decreased C0

in the subsurface soils (P<0.05), while increased precipita-tion significantly elevated it in the surface soils (P<0.05;Table 1). There were significant interactive effects of exper-imental warming and increased precipitation on soil C0 inthe surface soils. The warmed and increased precipitationplots decreased soil C0 by 381 and 74 mg kg−1 dry soil

compared with the control plots, respectively, while theircombined plots increased it by 271 mg kg−1 dry soil com-pared with the control plots at the 0–10-cm depth.

Cumulative CO2-C during the 70-day incubation weresignificantly and positively correlated with soil C0 acrossthe treatments (r200.96, P<0.001). Both cumulative CO2-Cand soil C0 were significantly and negatively correlated withsoil δ13C (both P<0.001). In addition, cumulative CO2-Cand soil C0 exerted significant positive relationships withsoil moisture (r200.74–0.83, both P<0.001) and contents ofexchangeable NH4

+-N (r200.24–0.26, both P<0.05) andNO3

−-N (r200.70–0.82, both P<0.001) across the treatments.

Discussion

As a key component of the comprehensive project (Bai et al.2010a; Liu et al. 2009; Yang et al. 2011), we focused on howsoil C mineralization responded to climate change and foundthe contrasting effects of experimental warming and in-creased precipitation on it at the 0–10- and 10–20-cm depths.

Labile organic C pool is a fraction of SOC, but it is moresensitive to management practices compared with SOC(Belay-Tedla et al. 2009; Chen et al. 2005; Rui et al.2011). Experimental warming, in this study, decreased soilC mineralization and C0, indicator for labile organic C, atthe two depths which were in contrast with other reports thatwarming stimulates soil C mineralization (Luo et al. 2001;

Table 1 Summary of results (P value) of two-way factorial ANOVAon the effects of warming, increased precipitation, and their interac-tions on soil moisture, pH, contents of exchangeable NH4

+-N and

NO3−-N, δ13C, δ15N, cumulative CO2-C, and potentially mineralizable

organic C (C0) at two depths of 0–10 and 10–20 cm

Treatment Soilmoisture (%)

pH NH4+-N

(mg kg−1)NO3

−-N(mg kg−1)

δ13C(‰)

δ15N(‰)

Cumulative CO2-C(mg kg−1 dry soil)

C0 (mg kg−1

dry soil)

0–10 cm

W 0.663 0.931 0.158 0.444 0.675 0.381 0.302 0.881

P 0.071 0.008** 0.036* 0.021* 0.045* 0.427 0.006** 0.039*

W × P 0.904 0.794 0.263 0.773 0.604 0.378 0.027* 0.014*

10–20 cm

W 0.672 0.894 0.073 0.721 0.812 0.461 0.048* 0.027*

P <0.001** 0.510 0.042* 0.036* 0.041* 0.515 0.688 0.707

W × P 0.726 0.596 0.192 0.909 0.573 0.277 0.359 0.622

W warming, P increased precipitation, WP warming plus increased precipitation, C control

*P<0.05; **P<0.01 (represent significant differences)

Fig. 1 Soil moisture (a), pH (b), contents of exchangeable NH4+-N (c)

and NO3−-N (d), 13C (e), and 15N (f) natural abundances (‰), poten-

tially mineralizable organic C (C0; g) (mean±SE) at two depths underwarming, increased precipitation, and their interactions. W warming,P increased precipitation, WP warming plus increased precipitation,C control

b

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(a) (b)

(c) (d)

(e) (f)

(g)

W P WP C0

-2

-22

-23

-24

-25

-26

13C

nat

ural

abu

ndan

ce (‰

)

0-10 cm 10-20 cm

Treatment

W P WP C0

5

10

15

Soi

l moi

stur

e (%

)

0-10 cm 10-20 cm

TreatmentW P WP C

0

1

6.6

6.7

6.8

6.9

7.0

pH

0-10 cm 10-20 cm

Treatment

W P WP C0

5

10

15

0-10 cm 10-20 cm

NH

4+-N

(m

g kg

-1 d

ry s

oil)

TreatmentW P WP C

0

5

10

15

0-10 cm 10-20 cm

NO

3- -N (

mg

kg-1 d

ry s

oil)

Treatment

W P WP C0

2

4

6

8

15N

nat

ural

abu

ndan

ce (

‰)

0-10 cm 10-20 cm

Treatment

W P WP C0

400

800

1200

1600

C0

(mg

kg-1 d

ry s

oil)

0-10 cm 10-20 cm

Treatment

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Melillo et al. 2002) and increases soil labile organic C(Belay-Tedla et al. 2009). However, our results were consis-tent with lower labile organic C under warming in arid orsemi-arid regions (Liu et al. 2009; Zhang et al. 2005). Incontrast, increased precipitation stimulated labile organic Cin the surface soils. Given that soil water availability plays apredominant role in regulating ecosystem functioning in aridand semiarid ecosystems (Liu et al. 2009; Niu et al. 2008;Yang et al. 2011), improved water availability under in-creased precipitation can stimulate soil microbial activity,which may contribute to higher soil C mineralization(Davidson and Janssens 2006). This is supported by thesignificantly positive relationship between soil moistureand C mineralization (P<0.001). Increased precipitationcan also stimulate plant growth and consequent below-ground C allocation and C substrate (Zak et al. 2000), whichwas supported by higher total plant coverage across 5 years

(Yang et al. 2011) and higher labile organic C under increasedprecipitation (Fig. 1g). Moreover, increased water availabilityunder increased precipitation can facilitate diffusion of solubleorganic C substrate, thereby increasing substrate availabilityfor soil microorganisms (Hungate et al. 2007; Schimel et al.2007). In addition, soil C mineralization was found to bestrongly affected by soil exchangeable NH4

+-N and NO3−-N

levels across the treatments (both P<0.001), which implied Nlimitation in Inner Mongolian grasslands (Bai et al. 2010b;Zhou et al. 2010).

Changes in soil δ13C and δ15N offer an approach tounderstand soil organic matter dynamics. For instance, thesechanges over time following changes in vegetation can beused to quantify SOC decomposition rates (e.g., Liao et al.2006). Higher aboveground biomass (Niu et al. 2008; Yanget al. 2011), root productivity, and mortality (Bai et al.2010a) have been reported in the increased precipitationplots in the same experiment. In this way, more freshplant-derived C via litter decomposition and root exudationinputs into the soils under increased precipitation, whichmay contribute to significantly lower soil δ13C (Table 1).Furthermore, soil δ15N reflects net effects of N-cyclingprocesses as influenced by climate change (Bijoor et al.2008; Robinson 2001). Warming has been reported to stim-ulate N-cycling rates, resulting in soil δ15N enrichments(Bijoor et al. 2008). However, we found that neither warmingnor increased precipitation affected soil δ15N (Table 1). Thiscould be due to similar legume communities between theincreased precipitation and control plots (Yang et al. 2011).

Previous studies in the same experiment have revealedthat there are no interactions of warming and increasedprecipitation on ecosystem respiration (Niu et al. 2008),net ecosystem productivity (Yang et al. 2011), and in situsoil respiration (Liu et al. 2009). Moreover, warming sup-pressed the above parameters under both ambient andincreased precipitation (Liu et al. 2009; Niu et al. 2008).As a result, we would expect additive effects of warmingand increased precipitation on soil C mineralization, but thisonly occurred for soil C mineralization at the 0–10-cm depth(Fig. 2). Warming inhibited soil C mineralization by 25 %under ambient precipitation but stimulated soil C minerali-zation by 17 % under increased precipitation at this depth.Given close relationships between soil C mineralization androot growth, the interactive effects of warming andincreased precipitation on soil C mineralization might beattributed to non-additive effects on cumulative root produc-tivity, mortality, and standing crop in the same experiment(Bai et al. 2010a). However, the previous study reported thatwarming stimulated root productivity, mortality, and stand-ing crop under ambient precipitation but suppressed themunder increased precipitation (Bai et al. 2010a), implyingcomplexity of C cycling in response to climate change.Different from the previous studies without significant

(a)

(b)

0 10 20 30 40 50 60 700

200

400

600

800

1000

1200 W P WP C

Cum

ulat

ive

CO

2-C

evo

lved

(mg

kg-1 d

ry s

oil)

Cum

ulat

ive

CO

2-C

evo

lved

(mg

kg-1 d

ry s

oil)

Incubation time (days)

0 10 20 30 40 50 60 700

100

200

300

400

500

600 W P WP C

Incubation time (days)

Fig. 2 Cumulative CO2-C (milligrams per kilogram dry soil, mean±SE)evolved from the 70-day incubations at 0–10- (a) and 10–20-cm (b) soildepths under warming, increased precipitation, and their interactions. Wwarming, P increased precipitation, WP warming plus increased precip-itation, C control

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interactive effects of multifactor climate change on soil Ccycling (Garten et al. 2009; Wan et al. 2007), our resultshighlight importance of factor interactions in response toclimate change.

Conclusions

Different from in situ soil respiration, that of soil underlaboratory conditions only determines soil organic C miner-alization, and this method makes it easy to study soil Cmineralization in response to climate change under the samestandardized conditions. Experimental warming andincreased precipitation exert different influences on soil Cmineralization, labile organic C, and 13C natural abundancesat two depths. Additionally, there were significant interac-tive effects of warming × increased precipitation on Cmineralization in surface soils. Our results may have signif-icant implications for soil C cycling in response to climatechange in semiarid and arid regions. Soil C mineralization inresponse to experimental warming and increased precipita-tion needs further study in this region for periods longerthan 10 years.

Acknowledgments This study was conducted as part of a compre-hensive research project (Global Change Multi-factor Experiment—Duolun) sponsored by the Institute of Botany, Chinese Academy ofSciences. This research was supported by the National Science Foun-dation of China (no. 30925009). The authors thank Prof. Shiqiang Wanfor accessing the experimental site and Prof. P. Nannipieri, Editor-in-Chief, and two reviewers for helpful comments on the early version ofthe manuscript.

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