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Effects of Precipitation Increase on Soil Respiration: A Three-Year Field Experiment in Subtropical Forests in China

  • Qi Deng,

    Affiliations South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

  • Dafeng Hui ,

    dhui@tnstate.edu

    Affiliation Department of Biological Sciences, Tennessee State University, Nashville, Tennessee, United States of America

  • Deqiang Zhang,

    Affiliation South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

  • Guoyi Zhou,

    Affiliation South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

  • Juxiu Liu,

    Affiliation South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

  • Shizhong Liu,

    Affiliation South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

  • Guowei Chu,

    Affiliation South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

  • Jiong Li

    Affiliation South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

Effects of Precipitation Increase on Soil Respiration: A Three-Year Field Experiment in Subtropical Forests in China

  • Qi Deng, 
  • Dafeng Hui, 
  • Deqiang Zhang, 
  • Guoyi Zhou, 
  • Juxiu Liu, 
  • Shizhong Liu, 
  • Guowei Chu, 
  • Jiong Li
PLOS
x

Correction

15 Oct 2012: Deng Q, Hui D, Zhang D, Zhou G, Liu J, et al. (2012) Correction: Effects of Precipitation Increase on Soil Respiration: A Three-Year Field Experiment in Subtropical Forests in China. PLOS ONE 7(10): 10.1371/annotation/1f49fc5e-e3f9-4b90-b555-97a54990ac3f. https://doi.org/10.1371/annotation/1f49fc5e-e3f9-4b90-b555-97a54990ac3f View correction

Abstract

Background

The aim of this study was to determine response patterns and mechanisms of soil respiration to precipitation increases in subtropical regions.

Methodology/Principal Findings

Field plots in three typical forests [i.e. pine forest (PF), broadleaf forest (BF), and pine and broadleaf mixed forest (MF)] in subtropical China were exposed under either Double Precipitation (DP) treatment or Ambient Precipitation (AP). Soil respiration, soil temperature, soil moisture, soil microbial biomass and fine root biomass were measured over three years. We tested whether precipitation treatments influenced the relationship of soil respiration rate (R) with soil temperature (T) and soil moisture (M) using R = (a+cM)exp(bT), where a is a parameter related to basal soil respiration; b and c are parameters related to the soil temperature and moisture sensitivities of soil respiration, respectively. We found that the DP treatment only slightly increased mean annual soil respiration in the PF (15.4%) and did not significantly change soil respiration in the MF and the BF. In the BF, the increase in soil respiration was related to the enhancements of both soil fine root biomass and microbial biomass. The DP treatment did not change model parameters, but increased soil moisture, resulting in a slight increase in soil respiration. In the MF and the BF, the DP treatment decreased soil temperature sensitivity b but increased basal soil respiration a, resulting in no significant change in soil respiration.

Conclusion/Significance

Our results indicate that precipitation increasing in subtropical regions in China may have limited effects on soil respiration.

Introduction

Soil respiration in terrestrial ecosystems plays an important role in global carbon cycling and climate change [1][4]. However, our understanding of precipitation impacts on soil respiration is still very limited, particularly in tropical and subtropical forests [5]. As greater intensity of precipitation and more severe droughts and floods are predicted in the future [6][7], such changes in precipitation may have significant influences on soil moisture and soil respiration in terrestrial ecosystems. Compared to drought, few studies have been done on the influence of heavy precipitation on soil respiration [8][14]. Considering that tropical and subtropical forests contain more than 25% of the carbon in the terrestrial biosphere, it is imperative to improve our mechanistic understanding of soil respiration responses to precipitation and soil moisture changes [15], [16].

Soil respiration includes both respiration of living roots and microbial respiration resulted from microbial decomposition of litter and soil organic matter [3], [5], [10], [12]. Root activity and microbial decomposition are often subject to both environmental factors and substrate changes related to phenological processes [17][20]. Any changes in root biomass, soil organic matter, root and microbial activities due to precipitation change could influence soil respiration. Like many biological processes, soil respiration is also influenced by soil temperature and moisture in many different ecosystems [3], [21][23]. While it is generally accepted that global warming could influence the relationship of soil respiration and temperature, how precipitation treatments would influence soil respiration and its relationship to soil moisture has not been well investigated. When treatments such as warming, precipitation, or CO2 concentration changes are applied, response variables may respond directly to changes in environmental factors as well as alter their relationships with environmental factors. Thus, soil respiration responses to precipitation treatments could be caused by either changes in environmental factors such as soil temperature and moisture, or functional changes – which are defined as changes in model parameters of soil respiration with soil temperature and moisture, or both [23]. For example, functional change due to a change in soil temperature sensitivity may increase or decrease soil respiration even when soil temperature is not influenced by precipitation treatments. Functional change could be attributed to the changes in phenological process, substrate or microbial activity in an ecosystem [2], [5], [16], [23].

Changes in soil moisture under different precipitation treatments could influence the responses of soil respiration to precipitation. There is no doubt that precipitation is usually the driving factor of the dynamics in soil moisture. However, soil water storage after precipitation events depends on vegetation types and covers, soil characteristics (e.g., infiltration rates, slopes, textures, depths, impermeable layers), and losses to deep drainage, lateral flow, and evaporation [24]. Thus, the response of soil moisture to precipitation treatments often varies in different ecosystems. For example, drought treatments using automated retractable curtains reduced soil moisture by 32–48%, 15–61%, and 19–25% at three heathlands [25], and double precipitation increased soil moisture by only 10% in Oklahoma grassland [10]. How precipitation changes influence soil moisture in subtropical forests may have significant impacts on soil respiration.

Functional changes (i.e. changes in model parameters of soil respiration with soil temperature and moisture) reflect underlying biological changes in the response of soil respiration to precipitation changes. Many empirical models of soil respiration and soil moisture have been developed [26][29]. Response of soil respiration to soil moisture is usually nonlinear, with soil respiration increases with soil moisture increases, levels off at high soil moisture, and even decreases when soil moisture is too high [3], [28], [29]. However, linear regression seems to work well in many different ecosystems, including boreal forests, sub-Antarctic island ecosystems, temperate grasslands, temperate forests, Mediterranean ecosystems, and particularly, tropical and subtropical forests [22], [30][34]. The slope of the linear regression model can be considered as soil moisture sensitivity, as it reflects an average change in soil respiration due to one unit change of soil moisture. While many precipitation manipulation experiments have been performed [9][15], [21], [22], only a few studies have attempted to study the soil moisture sensitivity change under climate change, particularly precipitation [3], [35][37].

Another important functional relationship is the response of soil respiration to soil temperature [2], [38], [39]. Soil temperature is the major control of soil respiration due to its influences on the kinetics of microbial decomposition, root respiration and diffusion of enzymes and substrates [32], [40]. Numerous studies have focused on the responses of soil respiration to soil temperature. The most widely used model is an exponential equation (R = R0exp(bT)) where R is soil respiration, T is soil temperature, and parameter R0 is basal soil respiration, and b is related to soil temperature sensitivity (Q10 = exp(10b) [41], [42]. Many studies reported that soil temperature sensitivity may decrease under high temperature treatments [2], [30], [38], [39] and increase under low temperature [38], [40][43]. Several studies also indicated that soil water stress or excess may decrease soil temperature sensitivity of soil respiration [27], [42], [44]. Since soil temperature and soil moisture may interactively regulate soil respiration in field conditions, relationships of soil respiration with both soil temperature and moisture have also been proposed [20], [36], [45]. Whether and how soil moisture and temperature sensitivities vary with precipitation increase have not been well investigated [5], [14].

We conducted a precipitation manipulation field experiment in subtropical forests in Southern China with an overall aim to understand the responses of soil respiration to precipitation increase. We selected three common forests at the study site, established two precipitation treatments in each forest, and measured soil respiration over three years. Double precipitation was realized through automatic interception-redistribution systems that delivering intercepted precipitation from nearby plots of the same size [10]. Adjacent control plots received ambient precipitation (AP). We addressed the following three questions in this study: 1) what are the response patterns of soil respiration to precipitation increase in the subtropical forests? 2) Do different forest sites respond differently to precipitation increase? 3) Does precipitation increase influence soil temperature and moisture sensitivities? The conclusions obtained in this study will enrich our knowledge of soil respiration responses to precipitation changes in subtropical forests in China and may have potentially significant implications for terrestrial ecosystem carbon cycling.

Materials and Methods

Ethics Statement

The study site is maintained by the South China Botanical Garden, Chinese Academy of Sciences. The location is within the Dinghushan Forest Ecosystem Research Station, Chinese Ecosystem Research Network (CERN). All necessary permits were obtained for the described field study. The field study did not involve endangered or protected species. Data will be made available upon request.

Site Description

The study site is located in the center of Guangdong Province in southern China (112°13′39′′–112°33′41′′ E, 23°09′21′′–23°11′30′′ N). Climate in the region is typical south subtropical monsoon climate, with mean annual temperature of 21.4°C, and mean annual precipitation of 1956 mm [33], of which nearly 80% falls in the hot-humid wet/rainy season (April-September) and 20% in the dry season (October-March). The bedrock is sandstone and shale. Three common subtropical forests (at elevations ranging from 200 to 300 m, less than 500 m from one another and facing the same slope direction) were selected including a coniferous Masson pine forest (PF), a conifer and broadleaf mixed forest (MF), and an evergreen broadleaf forest (BF). The three forests also represent forests in early-, middle-, and advanced-successional stages in the region [46], [47]. Soil properties and major stand information are listed in Table 1. The PF (approximately 22 ha), originally planted by local people in the 1950 s, was dominated by Pinus massoniana in the tree layer and Baeckea frutescens, Rhodomyrtus tomenosa, and Dicranopteris linearis in the shrub and herb layers. The MF (approximately 557 ha) was developed from artificial pine forest with a gradual invasion of some pioneer broadleaf species through natural succession. The upper canopy of the community is dominated by Schima superba, Castanopsis chinensis, and Craibiodendron scleranthum var. kwangtungense. Artificial disturbances have not occurred in the MF for about 100 years. The BF (approximately 218 ha) located in the central area of the reserve was dominated by Castanopsis chinensis, Cryptocarya concinna, Schima superba, Machilus chinensis without any Pinus massoniana. No disturbance was recorded for the past 400 years in the BF [37][38].

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Table 1. Stand characteristics of the pine forest (PF), the mixed forest (MF) and the broadleaf forest (BF) at the Dinghushan Forest Ecosystem Research Station.

https://doi.org/10.1371/journal.pone.0041493.t001

Experimental Design

We used a two-factor experimental design considering forest ecosystem type and precipitation treatment. At each forest site, a randomized block design was used with three blocks. In each block, one double precipitation (DP) treatment plot and one control plot were arranged. For the DP plot, precipitation was intercepted in a nearby plot with same size as the treatment plot using transparent polyvinyl chloride (PVC) sheer roof and was redistributed to the DP plot using pipes similar to those used in [10]. The control plot that received ambient precipitation (AP) was built next to the treatment plot. Each plot was 3×3 m2 and the distance between the DP and AP plots was more than one meter.

Soil Respiration Measurements

Five PVC soil collars (80 cm2 in area and 5 cm in height) were permanently installed 3 cm into the soil in each plot in November 2006. The distance between adjacent collars was more than 50 cm. Soil respiration was measured three times a month from January 2007 to December 2008 and two times a month in 2009 using a Li-6400 infrared gas analyzer (Li-COR, Inc., Lincoln, Nebraska, USA) connected to a Li-6400-09 soil respiration chamber (9.55 cm diameter) (Li-COR, Inc., Lincoln, Nebraska, USA). The measurements were made between 9∶00 am and 12∶00 pm local time. Previous work at this study site has demonstrated that soil respiration in forests measured during this period was close to daily mean [30], [48]. Soil respiration was measured three cycles for each soil collar and the CO2 concentration change in the chamber to complete one cycle was set as 10 ppm above the set point. Soil respiration in a treatment plot was calculated as the mean of five collar measurements (the measurement at five collars in a plot mostly differed by less than 5% at any measurement period). Soil temperature at 5 cm below the soil surface was also monitored with a thermocouple sensor attached to the respiration chamber during the soil respiration measurement. Volumetric soil moisture of the top 5 cm soil layer was measured on five random locations within a treatment plot using a PMKit [34] at the same time when the soil respiration measurements were being taken.

Soil Microbial Biomass and Fine Root Biomass Measurements

Soil samples were collected in February 2008 to determine soil microbial biomass C content, and three more times in May 2008, August 2008 and November 2008. Two samples of six cores (2.5 cm diameter) were randomly collected from each plot in the three forests. After removing roots and plant residues, the composited samples were immediately sieved through a 2-mm mesh sieve. The soil microbial biomass carbon was determined by the fumigation-extraction technique. The soil microbial biomass carbon was extracted with potassium sulfate on both fumigated and unfumigated soil [49], [50]. The carbon content of the extract was tested and the biomass was calculated based on the difference between the carbon content of fumigated vs. the unfumigated soil [49], [50].

To measure fine root biomass (diameter≤3 mm), we collected soil cores (0–20 cm depth) in February 2008 using a 10 cm diameter stainless-steel corer, and three more times in April 2008, August 2008 and October 2008. Each sample was randomly collected from each plot in each forest. Fine roots were separated by washing and sieving, dried at 60°C for 48 h and weighed.

Statistical Analysis

Soil respiration rate and soil temperature in a plot were calculated as the means of five collar measurements. Soil moisture was calculated as the mean of five measurements at random locations in a plot. We used repeated measure Analysis of Variance (ANOVA) to test the differences in soil respiration rate, soil temperature and soil moisture among forests, precipitation treatments, and years. Each treatment was replicated three times (three blocks). Multiple comparisons (Least Significant Difference, LSD method) were conducted if significant effects of forest ecosystem types, precipitation treatments or years were found. Previous work at study sites demonstrated that soil respiration increases exponentially with soil temperature and linearly with soil moisture [30], [33], [34]. Thus, we first developed the relationship between soil respiration and soil temperature with an exponential function and the relationship between soil respiration and soil moisture with a linear regression mode. Considering that soil temperature and moisture may interactively regulate soil respiration, we also fit soil respiration (R) with soil temperature (T) and soil moisture (M) together using R = (a+cM)exp(bT), where a is parameter related to basal soil respiration when both T = 0 and M = 0; b and c are parameters related to the soil temperature and moisture sensitivities of soil respiration, respectively. Like most studies, we used measurements of soil respiration, soil temperature and moisture of whole years here. One caveat of this approach was that seasonal variations of tree roots growth, carbon substrate in the soils, and soil microbial community would influence soil respiration, but were difficult to quantify. Non-linear least square method was used to derive the model parameters using SAS NLIN procedure [51]. Soil temperature and moisture sensitivities were derived for different precipitation treatments in the three forests. All data analyses were carried out using SAS software Version 9.1 [51] (SAS Institute Inc., Cary, NC, USA).

Results

Effects of Precipitation Treatments on Soil Temperature and Moisture

There were strong seasonal variations of precipitation in all three years, with intensive precipitation occurring from April through September (i.e., wet season) (Figure 1). The annual precipitation amount was 1341.6, 2925.8, and 1864.4 mm in 2007, 2008, and 2009, respectively. The very high precipitation in 2008 was mostly attributed to two heavy precipitation months (May and June) which had 50% of the total annual precipitation (Figure 1). The high precipitation intensity and large interannual variability in precipitation throughout the three years were typical in subtropical China. Mean annual air temperature did not vary much and was 22.77, 22.08, 22.71°C in 2007, 2008, and 2009, respectively. The monthly mean air temperature ranged from 11.35°C (February 2008) to 30.11°C (July 2007).

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Figure 1. Monthly rainfall and mean air temperature at the Dinghushan Forest Ecosystem Research Station in Southern China during the experimental period from 2007 to 2009.

https://doi.org/10.1371/journal.pone.0041493.g001

The seasonal patterns of soil temperature in three forests were similar to the pattern of air temperature (Figure 2a). Among the three forests, soil in the PF was significantly warmer (22.42°C) than that in the MF (20.20°C) and the BF (20.32°C) (Tables 2 and 3). No significant difference in annual mean soil temperature was found between the MF and the BF. Precipitation treatments did not change soil temperature in all three forests.

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Figure 2. Seasonal dynamics of soil temperature at 5 cm depth, soil moisture of the top 5 cm soil layer, and soil respiration under ambient precipitation (AP) and double precipitation (DP) treatments in the broadleaf forest (BF), the mixed forest (MF) and pine forest (BF).

https://doi.org/10.1371/journal.pone.0041493.g002

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Table 3. Mean value and significance of soil temperature, moisture and soil respiration from 2007 to 2009 between precipitation treatments in the pine forest (PF), the mixed forest (MF) and the broadleaf forest (BF), respectively.

https://doi.org/10.1371/journal.pone.0041493.t003

Soil moisture was significantly influenced by precipitation treatments and varied among forest ecosystem types and years (Table 2). Soil moisture in both the DP and AP treatments showed strong variations in all three forests (Figure 2b). Soil moisture was maintained at about 29% vol. in the BF and the MF, but only 20% vol. in the PF over the observation period (Table 2; Figure 2b). The DP treatment slightly increased annual mean soil moisture by approximately 11.4% compared to the AP treatment.

Effects of Precipitation Treatments on Soil Respiration, Soil Microbial Biomass and Fine Root Biomass

The soil respiration rate was significantly influenced by forest ecosystems and precipitation treatments, and the effects of precipitation treatments varied among the three forest ecosystems (Table 2). Soil respiration was significantly lower in the PF (2.37 µmol CO2 m−2 s−1), compared to that in the BF (3.07 µmol CO2 m−2 s−1) and MF (3.15 µmol CO2 m−2 s−1), averaged over three years of the experiment. The DP treatment increased mean annual soil respiration in the PF (15.4%), and did not show significant change in the BF or the MF.

The responses of soil microbial biomass and fine root biomass to precipitation treatment also varied among forest ecosystems (Figure 3). Soil microbial biomass in the DP treatment increased by 19.0% and 24.0% in the MF and the PF, respectively, compared to the AP treatment (Figure 3), but did not change in the BF. The DP treatment enhanced soil microbial biomass in both the wet and dry seasons in the PF, but only in the wet season in the MF. The DP treatment increased fine root biomass by 31.2% in the PF, but not in the MF and the BF (Figure 3). Fine root biomass in the PF was enhanced in the dry season by the DP treatment.

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Figure 3. Soil microbial biomass carbon content and fine root biomass (diameter≤3 mm) under ambient precipitation (AP) and double precipitation (DP) treatments in the broadleaf forest (BF), the mixed forest (MF) and the pine forest (PF).

Error bars are standard errors, sample size n = 6 for soil microbial biomass carbon content, sample size n = 3 for fine root biomass. Different letters in each forest denote significant difference (p<0.05) among precipitation treatments. *indicates significant difference between wet and dry seasons.

https://doi.org/10.1371/journal.pone.0041493.g003

Effects of Precipitation Treatments on the Functional Relationships of Soil Respiration with Soil Temperature and Moisture

Under both precipitation treatments and in all three forests, soil respiration responded exponentially to soil temperature and linearly to soil moisture (Figure 4). The DP treatment reduced soil temperature sensitivity in the BF and the MF, but not in the PF. Soil moisture sensitivity was not influenced by the DP treatment. Since soil temperature and soil moisture interactively regulate soil respiration, we considered both soil temperature and soil moisture and fit a combination model [30]. The best regression models explained 75–93% of soil respiration variations under two precipitation treatments in three forests (Table 4). The DP treatment decreased soil temperature sensitivities in the BF and the MF, but did not change soil moisture sensitivity. Basal soil respiration was enhanced under the DP treatment in both the BF and the MF. Under high temperature and heavy precipitation conditions, soil respiration under the DP treatment was lower than that under the AP treatment (Table 4), but in the PF, the DP treatment did not change the functional relationship of soil respiration with soil temperature and moisture developed under the AP control.

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Figure 4. Relationship of soil respiration with soil temperature or soil moisture under ambient precipitation (AP) and double precipitation (DP) treatments in the broadleaf forest (BF), the mixed forest (MF) and the pine forest (PF).

If fitted models aren’t significantly different between in the AP and DP treatments, one single model is fitted for all data. **indicates significant relationship at α = 0.01 levels.

https://doi.org/10.1371/journal.pone.0041493.g004

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Table 4. Functional relationship and significant test of model parameters.

https://doi.org/10.1371/journal.pone.0041493.t004

Discussion

The findings from our three-year precipitation manipulation experiment provide insights into the effects of precipitation increase on forest ecosystem soil respiration in subtropical monsoon areas and may have significant implications in modeling soil respiration. First, we found that unlike in arid and semi-arid ecosystems, soil respiration in the subtropical forests showed little response to precipitation increase, even when the precipitation was doubled. Second, we proposed to differentiate two reasons of soil respiration changes in response to precipitation increase (i.e., changes due to climate factor change and/or functional change) and demonstrated that different mechanisms may lead to different responses of soil respiration to precipitation treatments in different forest sites. The DP treatment increased soil moisture, enhanced basal soil respiration, but decreased soil temperature sensitivity in the BF and MF, resulting in no change in soil respiration. The increase in soil respiration in the PF under the DP treatment was solely caused by an increase in soil moisture, as no functional change was detected. Third, the slight increase in soil respiration under the DP treatment in the PF was supported by increases in soil microbial biomass and fine root biomass. As no changes in soil microbial biomass and fine root biomass were observed in the BF treatment and only slight change in soil microbial biomass in the MF, little change in soil respiration was observed in the MF and the BF. Our findings indicate that total soil respiration might not change much in the subtropical forests if precipitation increases in the future.

Responses of Soil Respiration to Precipitation Treatments

Previous studies have indicated that the water status of an ecosystem may influence the direction of soil respiration to either reduction or increase in precipitation treatments [25]. In this study, we found 15.4% annual increase in soil respiration in the PF and no change of soil respiration in the BF and the MF (Table 3). Different responses might be attributed to differences in soil condition and vegetation at these study sites. Soil in the PF contains more sand, less clay, and more gravel, and had lower ambient soil moisture content than those in the BF and the MF (Table 1). Trees in the PF were younger and smaller in biomass and LAI [29]. As a result, we found that soil respiration in the PF was low, but showed a significant influence by precipitation increase. Responses of soil respiration to precipitation increase also varied among different studies. For example, the DP treatment resulted in an increase of 9.0% in soil respiration in a tallgrass prairie [10]. But a large increase of 31% in soil respiration was reported in arid and semiarid grassland with 30% increase in annual precipitation [36]. Results from a recent study indicated that soil respiration may be decreased under precipitation increase in a humid tropical forest [13].

Functional Changes of Soil Respiration to Precipitation Treatments

Functional change of soil respiration to soil temperature/moisture under climate change is common and contributes to the responses of soil respiration in different ecosystems. A study in grasslands found that soil respiration was more sensitive to soil moisture than to soil temperature during prolonged drying cycles [52]. Ecosystems in xeric regions often possess lower soil respiration and higher soil moisture sensitivity than those in mesic regions [30], [53]. But the response of soil respiration to soil moisture change may be different in wet subtropical forests. We found that the DP treatment did not change soil moisture sensitivity, but decreased soil temperature sensitivity significantly in the BF and the MF ecosystems (Table 4). Many other studies have also found that soil respiration is insensitive to soil moisture unless that soil moisture is below levels at which metabolic activity decreases [20], [26], [54].

The lower temperature sensitivities under the DP treatment here may be due to the following two reasons. 1) Enhanced soil moisture under the DP treatment might decrease soil aeration and soil oxygen concentration [14], thus, more activation energy was needed to stimulate enzymatic rates [20]. Due to the subtropical monsoon climate, forests in the study site receive abundant heat, light, and water [55], [56]. Therefore, soils in these wet forests are often limited by soil oxygen concentration and nutrients, especially during the hot-humid season (April-September) [47]. 2) Greater leaching of dissolved organic carbon and nutrients under the DP treatment may reduce substrate availability [15], [57], and result in a decline in the Q10 values of soil respiration [8]. Previous work in this experiment has also shown that the active organic carbon, in particular particulate and light fraction organic carbon, often infiltrated to deeper soil layers with precipitation increase in the MF and BF [58], [59]. In the PF where soil was relative drier, the DP treatment stimulated fine root biomass and microbial activity (Figure 3). The greater soil microbial activity could release more nutrients from soil organic matter for fine root uptake, and increase soil respiration. The DP treatment in the BF and the MF did not stimulate soil microbe or fine root biomass, and caused little change in soil respiration in these forests.

Environmental Factor Changes Alone may Contribute to Soil Respiration Changes Under Precipitation Treatments

Environmental factor changes induced by climate change alone could have significant influences on ecosystem responses. In this study, we found that the functional response of soil respiration to soil temperature and moisture in the PF under the DP treatment was not changed compared to the AP treatment (Table 4). However, increases in soil moisture under the DP treatment slightly enhanced soil respiration. A similar result was reported recently in a Mediterranean evergreen forest [37]. They found that when 27% of throughfall was excluded over three years, soil moisture was reduced by 7–10%. While the three-year throughfall exclusion did not change functional properties of the response of soil respiration to soil water content and soil temperature, soil respiration decreased by 11% due to the environmental factor change.

Limitation of the Study

In this study, we selected three typical forest ecosystems in the south of China and tested the effects of precipitation increase on soil respiration. One shortcoming of the experimental design was unreplicated forest ecosystem types. While three replicated plots were employed for each precipitation treatment (i.e. DP and AP) at each forest ecosystem site, the forest types were not replicated. Thus, the inferences regarding the response differences among forest ecosystems should be read with caution. Further studies are needed to draw rigorous conclusions regarding forest ecosystem responses using replicated forest types.

Conclusions

Using a three-year field experiment in subtropical forests in China, we demonstrated that soil respiration under the DP treatment was not changed in the BF and the MF, but slightly increased in the PF. The lower response of soil respiration was consistent with small or no change of fine root biomass and microbial biomass under the DP treatment. The different responses in the three forests were associated with both functional change and environmental factor change induced by the precipitation treatments. Changes in soil temperature sensitivity and basal soil respiration together with change in soil moisture help us understand soil respiration responses at different forest sites. The shift of soil temperature sensitivity and basal soil respiration under different precipitation regimes may have potentially significant implications for terrestrial ecosystem carbon cycling, and should be considered in terrestrial ecosystem models. Whether soil moisture sensitivity of soil respiration is changed by precipitation treatments, particularly drought, may warrant further study.

Acknowledgments

The authors are grateful to Dr. Ben Bond-Lamberty for his insightful comments and valuable suggestions. We also thank Drs. Yiqi Luo, Robert B. Jackson and Phillip Ganter for their constructive comments on an early version of this manuscript. Ms. Jennifer Cartwright provided critical editing of the manuscript.

Author Contributions

Conceived and designed the experiments: DZ DH GZ. Performed the experiments: QD J. Liu SL GC J. Li. Analyzed the data: QD DH DZ GZ. Wrote the paper: DH QD DZ GZ.

References

  1. 1. Valentini R, Matteucci G, Dolman AJ, Schulze E-D, Rebmann C, et al. (2000) Respiration as the main determinant of carbon balance in European forests. Nature 404: 861–865.R. ValentiniG. MatteucciAJ DolmanE-D SchulzeC. Rebmann2000Respiration as the main determinant of carbon balance in European forests.Nature404861865
  2. 2. Luo Y, Wan S, Hui D, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413: 622–625.Y. LuoS. WanD. HuiLL Wallace2001Acclimatization of soil respiration to warming in a tall grass prairie.Nature413622625
  3. 3. Hui D, Luo Y (2004) Evaluation of soil CO2 production and transport in Duke Forest using a process-based modeling approach. Global Biogeochem Cycles 18: GB4029.D. HuiY. Luo2004Evaluation of soil CO2 production and transport in Duke Forest using a process-based modeling approach.Global Biogeochem Cycles18GB4029
  4. 4. Jackson RB, Cook CW, Pippen JS, Palmer SM (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest. Ecology 90: 3352–3366.RB JacksonCW CookJS PippenSM Palmer2009Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest.Ecology9033523366
  5. 5. Wu Z, Dijkstra P, Koch GW, Penuelas J, Hungate BA (2011) Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biol 2(17): 927–942.Z. WuP. DijkstraGW KochJ. PenuelasBA Hungate2011Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation.Global Change Biol2(17)927942
  6. 6. Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: The Physical Science Basis. Solomon, S., Qin, D., Manning, M, et al. eds. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York, USA: Cambridge University Press, 996pp. Intergovernmental Panel on Climate Change (IPCC)2007Climate Change 2007: The Physical Science Basis. Solomon, S., Qin, D., Manning, M, et al. eds. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge, UK and New York, USA: Cambridge University Press, 996pp
  7. 7. Allan RP, Soden BJ (2008) Atmospheric warming and the amplification of precipitation extremes. Science 321: 1481–1484.RP AllanBJ Soden2008Atmospheric warming and the amplification of precipitation extremes.Science32114811484
  8. 8. Harper CW, Blair JM, Fay PA, Knapp AK, Carlisle JD (2005) Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem. Global Change Biol 11: 322–334.CW HarperJM BlairPA FayAK KnappJD Carlisle2005Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem.Global Change Biol11322334
  9. 9. Borken W, Savage K, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Global Change Biol 12: 177–193.W. BorkenK. SavageEA DavidsonSE Trumbore2006Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil.Global Change Biol12177193
  10. 10. Zhou XH, Sherry RA, An Y, Wallace LL, Luo Y (2006) Main and interactive effects of warming, clipping, and doubled precipitation on soil CO2 efflux in a grassland ecosystem. Global Biogeochem Cycles 20: GB1003.XH ZhouRA SherryY. AnLL WallaceY. Luo2006Main and interactive effects of warming, clipping, and doubled precipitation on soil CO2 efflux in a grassland ecosystem.Global Biogeochem Cycles20GB1003
  11. 11. Davidson EA, Nepstad DC, Ishida FY, Brando PM (2008) Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Global Change Biol 14: 582–2590.EA DavidsonDC NepstadFY IshidaPM Brando2008Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest.Global Change Biol145822590
  12. 12. Jenerette GD, Scott RL, Huxman TE (2008) Whole ecosystem metabolic pulses following precipitation events. Funct Ecol 22: 924–930.GD JeneretteRL ScottTE Huxman2008Whole ecosystem metabolic pulses following precipitation events.Funct Ecol22924930
  13. 13. Cleveland CC, Wieder WR, Reed SC, Townsend AR (2010) Experimental drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere. Ecology 91(8): 2313–2323.CC ClevelandWR WiederSC ReedAR Townsend2010Experimental drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere.Ecology91(8)23132323
  14. 14. van Straaten O, Veldkamp E, Köhler M, Anas I (2010) Spatial and temporal effects of drought on soil CO2 efflux in a cacao agroforestry system in Sulawesi, Indonesia. Biogeosciences 7: 1223–1235.O. van StraatenE. VeldkampM. KöhlerI. Anas2010Spatial and temporal effects of drought on soil CO2 efflux in a cacao agroforestry system in Sulawesi, Indonesia.Biogeosciences712231235
  15. 15. Knapp AK, Beier C, Briske DD, Classen AT, Luo Y, et al. (2008) Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58: 811–821.AK KnappC. BeierDD BriskeAT ClassenY. Luo2008Consequences of more extreme precipitation regimes for terrestrial ecosystems.Bioscience58811821
  16. 16. Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, et al. (2012) Precipitation manipulation experiments - challenges and recommendations for the future. Ecology Letters. C. BeierC. BeierkuhnleinT. WohlgemuthJ. PenuelasB. Emmett2012Precipitation manipulation experiments - challenges and recommendations for the future.Ecology Letters
  17. 17. Rustad LE, Huntington TG, Boone RD (2000) Controls on soil respiration: implications for climate change. Biogeochemistry 48: 1–6.LE RustadTG HuntingtonRD Boone2000Controls on soil respiration: implications for climate change.Biogeochemistry4816
  18. 18. Bond-Lamberty B, Thomson A (2010) Temperature-associated increases in the global soil respiration record. Nature, 464, 579–582. B. Bond-LambertyA. Thomson2010Temperature-associated increases in the global soil respiration record.Nature, 464, 579–582
  19. 19. Hartley IP, Armstrong AF, Murthy R, Barron-Gafford, Ineson P, et al. (2006) The dependence of respiration on photosynthetic substrate supply and temperature: integrating leaf, soil and ecosystem measurements. Global Change Biol 12: 1954–1968.IP HartleyAF ArmstrongR. MurthyP. Barron-Gafford, Ineson2006The dependence of respiration on photosynthetic substrate supply and temperature: integrating leaf, soil and ecosystem measurements.Global Change Biol1219541968
  20. 20. Fang C, Moncrieff JB (2001) The dependence of soil CO2 efflux on temperature. Soil Biol Biochem 33: 155–165.C. FangJB Moncrieff2001The dependence of soil CO2 efflux on temperature.Soil Biol Biochem33155165
  21. 21. Curriel Yuste J, Janssens IA, Carrara A, Meiresonne L, Ceulemans R (2003) Interactive effects of temperature and precipitation on soil respiration in a temperate maritime pine forest. Tree Physiol 23: 1263–1270.J. Curriel YusteIA JanssensA. CarraraL. MeiresonneR. Ceulemans2003Interactive effects of temperature and precipitation on soil respiration in a temperate maritime pine forest.Tree Physiol2312631270
  22. 22. Scotta ED, Veldkamp E, Schwendenmann, Guimarães BR, Paixão RK, et al. (2007) Effects of an induced drought on soil CO2 efflux and soil CO2 production in an eastern Amazonian rainforest, Brazil. Global Change Biol 13: 546–560.ED ScottaE. VeldkampBR Schwendenmann, GuimarãesRK Paixão2007Effects of an induced drought on soil CO2 efflux and soil CO2 production in an eastern Amazonian rainforest, Brazil.Global Change Biol13546560
  23. 23. Hui D, Luo Y, Katul G (2003) Partitioning interannual variability in net ecosystem exchange into climatic variability and functional change. Tree Physiol 23: 433–442.D. HuiY. LuoG. Katul2003Partitioning interannual variability in net ecosystem exchange into climatic variability and functional change.Tree Physiol23433442
  24. 24. Brady NC, Weil RR (2002) The Nature and Properties of Soils. NC BradyRR Weil2002The Nature and Properties of Soils.13th ed.Upper Saddle River (NJ): Prentice Hall. Upper Saddle River (NJ): Prentice Hall.
  25. 25. Sowerby A, Emmett BA, Tietema A, Beier C (2008) Contrasting effects of repeated summer drought on soil efflux in hydric and mesic heathland soils. Global Change Biol 14: 2388–2404.A. SowerbyBA EmmettA. TietemaC. Beier2008Contrasting effects of repeated summer drought on soil efflux in hydric and mesic heathland soils.Global Change Biol1423882404
  26. 26. Davidson EA, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biol 4: 217–227.EA DavidsonE. BelkRD Boone1998Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest.Global Change Biol4217227
  27. 27. Reichstein M, Rey A, Freibauer A, Tenhunen J, Valentini R, et al. (2003) Modeling temporal and large-scale spatial variability of soil respiration from soil water availability, temperature and vegetation productivity indices. Global Biogeochem Cycles 17: 1–15.M. ReichsteinA. ReyA. FreibauerJ. TenhunenR. Valentini2003Modeling temporal and large-scale spatial variability of soil respiration from soil water availability, temperature and vegetation productivity indices.Global Biogeochem Cycles17115
  28. 28. Ilstedt U, Nordgren A, Malmer A (2000) Optimum soil water for soil respiration before and after amendment with glucose in humid tropical acrisols and a boreal mor layer. Soil Biol Biochem 32: 1591–1599.U. IlstedtA. NordgrenA. Malmer2000Optimum soil water for soil respiration before and after amendment with glucose in humid tropical acrisols and a boreal mor layer.Soil Biol Biochem3215911599
  29. 29. Deng Q, Zhou GY, Liu SZ, Chu GW, Zhang DQ (2011) Responses of soil CO2 efflux to precipitation pulses in two subtropical forests in southern China, Environ manage 48: 1182–1188.Q. DengGY ZhouSZ LiuGW ChuDQ Zhang2011Responses of soil CO2 efflux to precipitation pulses in two subtropical forests in southern China, Environ manage4811821188
  30. 30. Tang XL, Liu SG, Zhou GY, Zhang DQ, Zhou CY (2006) Soil-atmospheric exchange of CO2, CH4, and N2O in three subtropical forest ecosystems in southern China. Global Change Biol 12: 546–560.XL TangSG LiuGY ZhouDQ ZhangCY Zhou2006Soil-atmospheric exchange of CO2, CH4, and N2O in three subtropical forest ecosystems in southern China.Global Change Biol12546560
  31. 31. Schwendenmann L, Veldkamp E (2005) The role of dissolved organic carbon, dissolved organic nitrogen, and dissolved inorganic nitrogen in a tropical wet forest ecosystem. Ecosystems 8: 339–351.L. SchwendenmannE. Veldkamp2005The role of dissolved organic carbon, dissolved organic nitrogen, and dissolved inorganic nitrogen in a tropical wet forest ecosystem.Ecosystems8339351
  32. 32. Luo Y, Zhou X (2006) Soil and Respiration Environment. Academic Press, San Diego. Y. LuoX. Zhou2006Soil and Respiration Environment.Academic Press, San Diego
  33. 33. Zhang DQ, Sun XM, Zhou GY, Yan JH, Wang YS, et al. (2006) Seasonal dynamics of soil CO2 effluxes with responses to environmental factors in lower subtropical forest of China. Science in China Ser, D-Earth Sciences 49 (S1): 139–149.DQ ZhangXM SunGY ZhouJH YanYS Wang2006Seasonal dynamics of soil CO2 effluxes with responses to environmental factors in lower subtropical forest of China.Science in China Ser, D-Earth Sciences 49(S1)139149
  34. 34. Deng Q, Zhou GY, Liu JX, Liu S, Duan H, et al. (2010) Responses of soil respiration to elevated carbon dioxide and nitrogen addition in young subtropical forest ecosystems in China. Biogeosciences 7: 315–328.Q. DengGY ZhouJX LiuS. LiuH. Duan2010Responses of soil respiration to elevated carbon dioxide and nitrogen addition in young subtropical forest ecosystems in China.Biogeosciences7315328
  35. 35. Noormets A, Desai A, Cook BD, Ricciuto DM, Euskirchen ES, et al. (2008) Moisture sensitivity of ecosystem respiration: comparison of 14 forest ecosystems in the Upper Great Lakes Region, USA. Agric For Meteorol 148: 216–230.A. NoormetsA. DesaiBD CookDM RicciutoES Euskirchen2008Moisture sensitivity of ecosystem respiration: comparison of 14 forest ecosystems in the Upper Great Lakes Region, USA.Agric For Meteorol148216230
  36. 36. Liu W, Zhang Z, Wan S (2009) Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biol 15: 184–195.W. LiuZ. ZhangS. Wan2009Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland.Global Change Biol15184195
  37. 37. Misson L, Rocheteau A, Rambal S, Ourcival JM, Limousin JM, et al. (2010) Functional changes in the control of carbon fluxes after 3 years of increased drought in a Mediterranean evergreen forest? Global Change Ecol 16: 2461–2475.L. MissonA. RocheteauS. RambalJM OurcivalJM Limousin2010Functional changes in the control of carbon fluxes after 3 years of increased drought in a Mediterranean evergreen forest?Global Change Ecol1624612475
  38. 38. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165–173.EA DavidsonIA Janssens2006Temperature sensitivity of soil carbon decomposition and feedbacks to climate change.Nature440165173
  39. 39. Davidson EA, Janssens I, Luo YQ (2006) On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Global Change Biol 12: 154–164.EA DavidsonI. JanssensYQ Luo2006On the variability of respiration in terrestrial ecosystems: moving beyond Q10.Global Change Biol12154164
  40. 40. Kirschbaum MUF (2010) The temperature dependence of organic matter decomposition: seasonal temperature variations turn a sharp short-term temperature response into a more moderate annually averaged response. Global Change Biol 16: 2117–2129.MUF Kirschbaum2010The temperature dependence of organic matter decomposition: seasonal temperature variations turn a sharp short-term temperature response into a more moderate annually averaged response.Global Change Biol1621172129
  41. 41. Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408: 184–187.PM CoxRA BettsCD JonesSA SpallIJ Totterdell2000Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model.Nature408184187
  42. 42. Xu M, Qi Y (2001) Spatial and seasonal variations of Q10 determined by soil respiration measurements at a Sierra Nevadan forest. Global Biogeochem Cycles 15: 687–697.M. XuY. Qi2001Spatial and seasonal variations of Q10 determined by soil respiration measurements at a Sierra Nevadan forest.Global Biogeochem Cycles15687697
  43. 43. Zhou T, Shi PJ, Hui D, Luo Y (2009) Global pattern of temperature sensitivity of soil heterogeneous respiration (Q10) and its implications for carbon-climate feedback. J Geophy Res - Biogeosciences 114: G02016.T. ZhouPJ ShiD. HuiY. Luo2009Global pattern of temperature sensitivity of soil heterogeneous respiration (Q10) and its implications for carbon-climate feedback.J Geophy Res - Biogeosciences114G02016
  44. 44. Jassal RS, Black TA, Novak MD, Gaumont-Guay Nesic Z (2008) Effect of soil water stress on soil respiration and its temperature sensitivity in an 18-year-old temperate Douglas-fir stand. Global Change Biol 14: 1–14.RS JassalTA BlackMD NovakZ. Gaumont-Guay Nesic2008Effect of soil water stress on soil respiration and its temperature sensitivity in an 18-year-old temperate Douglas-fir stand.Global Change Biol14114
  45. 45. Schaefer K, Denning AS, Suits N, Kaduk J, Baker I, et al. (2002) Effect of climate on interannual variability of terrestrial CO2 fluxes. Global Biogeochem Cycles 16: GB1102.K. SchaeferAS DenningN. SuitsJ. KadukI. Baker2002Effect of climate on interannual variability of terrestrial CO2 fluxes.Global Biogeochem Cycles16GB1102
  46. 46. Peng SL, Wang BS (1995) Forest succession at Dinghushan, Guangdong, China. Chinese Journal of Botany 7: 75–80.SL PengBS Wang1995Forest succession at Dinghushan, Guangdong, China.Chinese Journal of Botany77580
  47. 47. Wang BS, Ma MJ (1982) The successions of the forest community in Dinghushan. Tropical and Subtropical Forest Ecosystem Research 1: 142–156.BS WangMJ Ma1982The successions of the forest community in Dinghushan.Tropical and Subtropical Forest Ecosystem Research1142156(in Chinese with English abstract). (in Chinese with English abstract).
  48. 48. Shen CD, Yi WX, Sun YM, Xing CP, Yang Y, et al. (2001) Distribution of 14C and 13C in forest soils of the Dinghushan Biosphere Reserve. Radiocarbon 43(2B): 671–678.CD ShenWX YiYM SunCP XingY. Yang2001Distribution of 14C and 13C in forest soils of the Dinghushan Biosphere Reserve.Radiocarbon43(2B)671678
  49. 49. Jenkinson DS (1987) Determination of microbial biomass carbon and nitrogen in soil. In: Wilson JR, editor. DS Jenkinson1987Determination of microbial biomass carbon and nitrogen in soil.JR Wilsoneds.Advances in N Cycling in Agricultural Ecosystem.Wallingford, UK: Commonwealth Agricultural Bureau International press, 368–386. Wallingford, UK: Commonwealth Agricultural Bureau International press, 368–386.
  50. 50. Vance ED, Brookes SA, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19: 703–707.ED VanceSA BrookesDS Jenkinson1987An extraction method for measuring soil microbial biomass C. Soil Biol Biochem19703707
  51. 51. Hui D, Jiang C (1996) Practical SAS Usage, Beijing University of Aeronautics & Astronautics Press, Beijing, China. D. HuiC. Jiang1996Practical SAS Usage, Beijing University of Aeronautics & Astronautics Press, Beijing, China.
  52. 52. Fay PA, Kaufman DM, Nippert JB, Carlisle JD, Harper CW (2008) Changes in grassland ecosystem function due to extreme rainfall events: implications for responses to climate change. Global Change Biol 14: 1600–1608.PA FayDM KaufmanJB NippertJD CarlisleCW Harper2008Changes in grassland ecosystem function due to extreme rainfall events: implications for responses to climate change.Global Change Biol1416001608
  53. 53. Shen W, Jenerette GD, Hui D, Phillips RP, Ren H (2008) Effects of changing precipitation regimes on dryland soil respiration and C pool dynamics at rainfall event, seasonal and interannual scales. J Geophys Res – Biogeosciences 113: G03024.W. ShenGD JeneretteD. HuiRP PhillipsH. Ren2008Effects of changing precipitation regimes on dryland soil respiration and C pool dynamics at rainfall event, seasonal and interannual scales.J Geophys Res – Biogeosciences113G03024
  54. 54. Palmroth S, Maier CA, McCarthy HR, Oishi AC, Kim HS, et al. (2005) Contrasting responses to drought of forest floor CO2 efflux in a Loblolly pine plantation and a nearby Oak–Hickory forest. Global Change Biol 11: 421–434.S. PalmrothCA MaierHR McCarthyAC OishiHS Kim2005Contrasting responses to drought of forest floor CO2 efflux in a Loblolly pine plantation and a nearby Oak–Hickory forest.Global Change Biol11421434
  55. 55. Ding MM, Brown S, Lugo AE (2001) A continental subtropical forest in China compared with an insular subtropical forest in the Caribbean. General Technical Report IITF-17, USDA (United States Department of Agriculture) Forest Service, International Institute of Tropical Forestry, Rio Piedras, Puerto Rico. MM DingS. BrownAE Lugo2001A continental subtropical forest in China compared with an insular subtropical forest in the Caribbean.General Technical Report IITF-17, USDA (United States Department of Agriculture) Forest Service, International Institute of Tropical Forestry, Rio Piedras, Puerto Rico
  56. 56. Yan JH, Zhang DQ, Zhou GY, Liu JX (2009) Soil respiration associated with forest succession in subtropical forests in Dinghushan Biosphere Reserve. Soil Biol Biochem 9: 1–9.JH YanDQ ZhangGY ZhouJX Liu2009Soil respiration associated with forest succession in subtropical forests in Dinghushan Biosphere Reserve.Soil Biol Biochem919
  57. 57. Liu JX, Zhang DQ, Zhou GY, Faivre-Vuillin B, Deng Q, et al. (2008) CO2 enrichment increases cation and anion loss in leaching water of model forest ecosystems in southern China. Biogeosciences 5: 1783–1795.JX LiuDQ ZhangGY ZhouB. Faivre-VuillinQ. Deng2008CO2 enrichment increases cation and anion loss in leaching water of model forest ecosystems in southern China.Biogeosciences517831795
  58. 58. Chen XM, Liu JX, Deng Q, Chu GW, Zhou GY, et al. (2010) Effects of precipitation intensity on soil organic carbon fractions and their distribution under subtropical forests of South China. Chinese Journal of Applied Ecology 21: 1210–1216.XM ChenJX LiuQ. DengGW ChuGY Zhou2010Effects of precipitation intensity on soil organic carbon fractions and their distribution under subtropical forests of South China.Chinese Journal of Applied Ecology2112101216(in Chinese with English abstract). (in Chinese with English abstract).
  59. 59. Liu S, Luo Y, Huang YH, Zhou GY (2007) Studies on the community biomass and its allocations of five forest types in Dinghushan Nature Reserve. Ecol Science 26(5), 387–393. S. LiuY. LuoYH HuangGY Zhou2007Studies on the community biomass and its allocations of five forest types in Dinghushan Nature Reserve.Ecol Science 26(5), 387–393
  60. 60. Fang YT, Mo JM, Peng SL, Li DJ (2003) Role of forest succession on carbon sequestration of forest ecosystems in lower subtropical China. Acta Ecologica Sinica, 23, 1685–1694. YT FangJM MoSL PengDJ Li2003Role of forest succession on carbon sequestration of forest ecosystems in lower subtropical China.Acta Ecologica Sinica, 23, 1685–1694
  61. 61. He C, Chen S, Liang Y (1982) The soils of Dinghushan Biosphere Reserve. Tropical and Subtropical Forest Ecosystem, 1, 25–38. C. HeS. ChenY. Liang1982The soils of Dinghushan Biosphere Reserve.Tropical and Subtropical Forest Ecosystem, 1, 25–38