Grazing intensity influence soil microbial communities and their implications for soil respiration

Agriculture, Ecosystems and Environment 249 (2017) 50–56

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee

Research paper

Grazing intensity influence soil microbial communities and their implications for soil respiration

MARK ⁎

Fazhu Zhaoa,b, Chengjie Renc, Shelby Sheltond, Ziting Wangc, Guowei Panga,b, Ji Chene,f,g, , ⁎⁎ Jun Wanga,b, a

Shaanxi Key Laboratory of Earth Surface System and Environmental Carrying Capacity, Northwest University, Xi’an, Shaanxi 710127, China College of Urban and Environmental Sciences, Northwest University, Xi’an, Shaanxi 710127, China c College of Agronomy, Northwest A & F University, Yangling, 712100 Shaanxi, China d Milken Institute of Public Health, The George Washington University, Washington, D.C. 20052, USA e Center for Ecological and Environmental Sciences, Key Laboratory for Space Bioscience & Biotechnology, Northwestern Polytechnical University, Xi’an 710072, China f State Key Laboratory of Loess and Quaternary Geology (SKLLQG), and Key Laboratory of Aerosol Chemistry and Physics, Institute of Earth Environment, Chinese Academy of Sciences, Xi’an 710061, China g University of Chinese Academy of Sciences, Beijing 100049, China b

A R T I C L E I N F O

A B S T R A C T

Keywords: Grazing intensity Soil respiration Soil microbial community size Grassland Meta-analysis

Soil microorganisms regulate carbon (C) transfer from terrestrial sources to the atmosphere, therefore playing a pivotal role in soil C dynamics. Worldwide, grazing is one of the most prevalent grassland management strategies, yet the effects of grazing on soil microbial community size and soil respiration (SR) are still active areas of debate. We conducted a meta-analysis of 71 publications to synthesize the responses of soil microbial community size and SR to grazing. Our results showed that grazing significantly decreased soil total microbial, bacterial and fungal community size by 11.74, 8.85 and 11.45%, respectively. However, this effect were differed when the studies were grouped by the grazing intensity. Briefly, light and moderate grazing intensity had no effect on soil microbial, bacterial and fungal community size, but heavy grazing intensity significantly reduced soil’s total microbial, bacterial and fungal community size by 14.79, 16.48 and 28.12%, respectively. The responses of microbial community size to grazing were positively correlated with those of SR both under moderate and heavy grazing intensity. Our findings indicate that soil microbial community size could be an important underlying mechanism involved in determining soil C dynamics under grazing. Hence better understanding of the responses of soil microbial community size would greatly contribute to our understanding of soil C dynamics. Lastly, our results underscore the importance of factoring grazing intensity into consideration to further improve the model’s projection of soil C dynamics.

1. Introduction Grasslands occupy about 40% of the world’s land surface and store approximately 10% of the global soil organic carbon (SOC) (Raiesi and Asadi, 2006; Dlamini et al., 2016). Because of their area and vast amounts of C stored, grasslands can provide important ecosystem services for human beings, such as water retention, carbon (C) sequestration, and climate mitigation (Jones and Donnelly, 2005; Chen et al., 2015b), thereby facilitating important ecosystem services for human beings. A growing number of studies show that the health of grassland ecosystems strongly depends on the grassland management strategies, such as grazing and grazing exclusion (Jones and Donnelly, 2005; Hu

et al., 2016). Globally, it is estimated that more than 23% of the world’s grassland is degraded, and this can be principally attributed to overgrazing (Chen et al., 2016; Dlamini et al., 2016). The degraded grasslands not only fail to provide subsistence for the herdsman’s survival, but can also potentially affect the C-climate feedback via changes in soil microbial activity (Stark et al., 2015; Qu et al., 2016; Ren et al., 2017). However, changes in specific microbial community were not reported in previous study, since the results would be infer that grazing-induced changes in soil microbial community size were linked with the soil C dynamics (Chen et al., 2016). Uncertainties still remain regarding the responses of specific soil microbial community size to grazing as well as the underlying mechanisms (Nunan et al., 2005; Dlamini et al., 2016).

⁎ Corresponding author at: Center for Ecological and Environmental Sciences, Key Laboratory for Space Bioscience & Biotechnology, Northwestern Polytechnical University, Xi’an 710072, China. ⁎⁎ Corresponding author at: Shaanxi Key Laboratory of Earth Surface System and Environmental Carrying Capacity, Northwest University, Xi’an, Shaanxi 710127, China. E-mail addresses: [email protected] (J. Chen), [email protected] (J. Wang).

http://dx.doi.org/10.1016/j.agee.2017.08.007 Received 20 May 2017; Received in revised form 27 July 2017; Accepted 4 August 2017 0167-8809/ © 2017 Elsevier B.V. All rights reserved.

Agriculture, Ecosystems and Environment 249 (2017) 50–56

F. Zhao et al.

Fig. 1. Global distribution of grazing experiments selected in this meta-analysis.

2010), tropical grassland (Northup et al., 2000), a meadow steppe (Yan et al., 2011), and the Tibetan alpine meadow (Li et al., 2015); though the underlying mechanisms still remain largely unclear. Therefore, it is necessary to synthesize results from a variety of studies to accurately characterize the principle effects of grazing intensity on soil microbial community size and SR. To advance the projection ability in regard to soil microbial community size and SR under grazing, we conducted a meta-analysis on the responses of soil microbial community size and SR to grazing. Specifically, our objectives were to: (1) examine global patterns of soil microbial community size responses to grazing; (2) assess effects of grazing intensities on the soil microbial community size; and (3) illustrate the responses of soil microbial community size would be tightly coupled with the changes in SR.

These gaps in knowledge have substantially hindered our evaluation and projection of grassland ecosystem services. SR is one of the largest C fluxes from terrestrial ecosystems to the atmosphere, but the effects of grazing on SR are largely unclear (Cao et al., 2004; Hou et al., 2014; Chen et al., 2016; Moinet et al., 2016). The primary reason for these large uncertainties can be ascribed to the poor understanding of the effects of grazing on soil microbial communities (Ford et al., 2012; Yang et al., 2013; Stark et al., 2015). Recent data from several meta-analysis studies supports the hypothesis that variability in the microbial community size due to ecosystem disturbances (Dooley and Treseder, 2012; Holden and Treseder, 2013) as well as other global change drivers (Treseder, 2008; Chen et al., 2015a, 2017). Combining the aforementioned observations with evidences from several multiple recent field studies (Shi et al., 2015; Chen et al., 2016), we hypothesize that grazing-induced shifts in soil microbial community is an important underlying mechanism for the responses of SR to grazing. For example, it has been reported that SR is positively correlated with actinomycetes (gram-positive bacteria) abundance during conversion from primary forest to secondary forest in northeast China (Shi et al., 2015). Therefore, a broad understanding of the responses of specific microbial community size to grazing and their links with SR would likely provide novel ways to accurately predict soil C dynamics. Furthermore, it would also significantly contribute to our knowledge of grassland soil C flux and improving existing grassland management techniques to combat climate change. Grazing intensity is regarded as a potential critical mechanism that affects soil microbial community size and SR since it alters the substrate concentration of dung and urine (Saggar et al., 2004; Zhou et al., 2017), changes soil water content and energy balance (Leriche et al., 2001; Zhang et al., 2014), and increases soil compaction by animals trampling in the soil (Houlbrooke et al., 2008). For example, a study conducted on the Tibetan Plateau have showed that grazing significantly reduced total microbial community size, which was accompanied by corresponding reduction in soil respiration (SR) (Chen et al., 2016). A previous study indicated that moderate grazing intensity could enhance plant biomass as a result of the increase in soil microbial community size, whereas heavy grazing intensity would reduce both above- and below- ground biomass and consequently decrease soil microbial community size (Northup et al., 2000). However, recent studies also indicate that grazing intensity has differential effects on soil microbial communities, highlighting the impacts of grazing intensity on microbial diversity, composition and structure (Delgado-Baquerizo et al., 2016; Olivera et al., 2016). Although, the effects of grazing intensity on soil microbes has been also widely reported in different grassland ecosystems, such as a semiarid steppe (Raiesi and Asadi, 2006; Qi et al.,

2. Methods 2.1. Source data We searched journal articles published between 1991 and 2016 using the Web of Science in both English and Chinese (http://apps. webofknowledge.com/) and China Knowledge Resource Integrated Database (http://www.cnki.net/) (Fig. 1). Briefly, the following keywords and combinations were used for the searching: (1) “grazing” or “microbe” or “microbial” or “fungi” or “bacterial” and (2) “grazing” or “soil microbial carbon”. Based on the methods for meta-analysis (Chen et al., 2017), studies were selected according to the following criteria: (1) All results were from field experiments; (2) Grazing and grazing exclusion treatments had to be made at the same experimental sites; (3) Data collection was limited to results in which means, standard deviations (SDs), and replicate numbers were reported. If standard errors (SEs) were reported, the following equation was used to calculate SD:

SD = SE ×

n

where n was the replicate number; (4) Grazing protocols (grazing intensity, grazing exclusion year) had to be clearly described or accessible from the cited articles; (5) If more than one grazing experiment was reported in the same article but with different environmental variables (e.g. grazing conducted under various geographical location or microclimate), each was regarded as an independent study. 2.2. Data acquisition In total, 71 published papers were selected from 71 study sites (Supplementary Text S1). For each selected paper, we recorded 51

Agriculture, Ecosystems and Environment 249 (2017) 50–56

F. Zhao et al.

where Xt and Xc were means of grazing exclusion and grazing treatments, respectively. The distribution of the RRs calculated in this way was nearly normal and the biases were minor. The variance within each study was calculated using the means, replicate numbers, and SDs of both grazing exclusion and grazing. We used the MetaWin software (Sinauer AsSOMiates Inc., Sunderland, MA, USA) to calculate overall weighted response ration (RR++) and 95% bootstrap confidence intervals (CIs) for the whole dataset and the grouped dataset. Significant responses (p < 0.05) were determined if CIs of RR++ did not overlap with 0. Warming-induced changes for a certain categorical group were calculated by:

Percentage(%) = exp(RR++) − 1 × 100% Random effects models in the meta-analysis were used to compare differences among groups in the ways similar to the analysis of variance framework. We sequentially compared RR++ among measurements, grazing intensity, grazing and exclusion year. A linear regression analysis was used to examine the relationships between the RRs of microbial, fungal, and bacterial community size and MAT, MAP, latitude, elevation, and RRs of SR. Due to the preference for publishing larger effects than smaller ones, we used Kendall’s tau rank and Spearman’s rank correlation to infer publication biasness (Hanka, 1994; Chen et al., 2017). All the methods in the present meta-analysis have been successfully used in numerous previous studies (Luo et al., 2006; Chen et al., 2017).

Fig. 2. Effect of grazing intensity on soil microbial community size. Error bars represent bootstrap 95% confidence intervals CIs). The effect of grazing was considered significant if the CI of the effect size did not overlap with zero. (Soil microbial community size: QW = 282.12, QB = 101.36, p = 0.001; Fungi: QW = 392.45, QB = 257.69, p = 0.001; Bacteria: QW = 281.81, QB = 371.61, p = 0.001); L: Light grazing intensity; M: Moderate grazing intensity; H: heavy grazing intensity.

3. Results 3.1. Effect of grazing intensity on microbial community size Across all studies, soil microbial community size significantly decreased following grazing by an average of 11.74% (Fig. 2 and Tables S1–S5). Light and moderate grazing intensity increased soil microbial community size by 5.05 and 1.87%, respectively, whereas, heavy grazing intensity significantly decreased microbial community size by 18.12%. Next we found light and moderate grazing intensity increased soil microbes by 2.09 and 3.14% respectively, while heavily grazing intensity decreased by the same by 14.79%. Furthermore, while light and moderate grazing intensity increased fungal community size by 17.01 and 0.80%, respectively, heavy grazing intensity decreased fungal community size by 16.48%. However, bacterial community size under moderate and heavy grazing intensity decreased by 0.28 and 28.12%, respectively.

microbial, fungal, and bacterial community size or biomass. Meanwhile, we also recorded study site, latitude, longitude, elevation, mean annual precipitation (MAP), mean annual temperature (MAT), measurements methods, grazing exclusion year, and grazing intensity from the selected papers. Where possible, soil organic carbon (SOC), total nitrogen (TN), pH, soil bulk density (BD), and SR were also recorded. We defined SR as the amount of soil CO2 release measured by soil chambers in the field studies or during laboratory incubations. This method has been successfully used in three previous meta-analyses to evaluate the responses of microbial community size and SR to other global climate change factors (Schuur et al., 2008; Treseder, 2008). If data were presented graphically, we used Getdata graph digitizer version 2.26 (http://getdata-graph-digitizer.com/) to digitize the data.

3.2. Effect of grazing on microbes 2.3. Microbial measurements

When grouped by soil depth, grazing significantly increased soil microbial community size by 3.12 and 4.00% at 0–10 and > 30 cm soil depth. In contrast, grazing significantly decreased soil microbial community size by 8.61 and 15.92% in 10–20 and 20–30 cm soil depth (Fig. 3). When grouped by grazing duration, grazing significantly decreased soil microbial community size by 10.43 (< 10 years) and 33.1% (> 20 years), while increased by 22.67% in 10–20 yr under light, moderate and heavy grazing. Specifically, the heavy grazing intensity significantly decreased by 15.74 and 37.38% in > 10 yr and > 20 yr, respectively, but no significant decrease was found in light, moderate grazing intensity in < 10 yr, 10–20 yr and > 20 yr.

Multiple types of microbial measurements were considered. Total microbial biomass or community size determined by chloroform fumigation (CF) (Vance et al., 1987) or phospholipid fatty acids (PLFA) (Frostegård et al., 1996). Fungal community size measured by fungi PLFA or quantitative polymerase chain reaction analysis (qPCR). For bacteria, bacteria PLFA and qPCR based measurement were considered for inclusion in the analysis. 2.4. Data analysis A meta-analysis approach was used to determine the significance of microbial responses to a variety of experimental grazing intensity (Hedges et al., 1999; Treseder and Kathleen, 2013; Chen et al., 2017). For each study, the response ratio (RR) was calculated as described below:

3.3. Effect of grazing on fungi When grouped by soil depth, grazing significantly decreased fungal community size by 16.64, 12.96 and 56.66% at the 10–20, 20–30 and > 30 cm soil depth; while it significantly increased fungal community about 22.45% in 10–20 cm soil depth (Fig. 4). Similarly, when grouped by grazing duration, grazing significantly diminished fungal community size by 9.12, 17.55 and 3.13% in < 10, 10–20 and > 20 yr,

X RR = ln ⎧ t ⎫ = ln(Xt ) − ln(Xc ) ⎨ X ⎭ ⎩ c⎬ 52

Agriculture, Ecosystems and Environment 249 (2017) 50–56

F. Zhao et al.

Fig. 3. Effect of grazing on soil microbial community size (Depth: QW = 526.57, QB = 35.39, p = 0.001; QB = 61.77, Duration: < 10: QW = 158.06, p = 0.001; 10–20: QW = 126.73, QB = 180.21, QB = 629.40, p = 0.003; > 20: QW = 24.64, p = 0.001); L: Light grazing intensity; M: Moderate grazing intensity; H: heavy grazing intensity.

respectively. In detail, heavy grazing intensity significantly reduced fungal community size by 11.86% in < 10 yr, however, no significant decrease or increase was found in the other grazing duration.

3.4. Effect of grazing on bacteria When grouped by soil depth, grazing significantly decreased bacterial community size by 8.17, 21.20, 18.12 and 69.52% at 0–10, 10–20, 20–30 and > 30 cm soil depth (Fig. 5). Again, when grouped by grazing duration, grazing significantly decreased bacterial community Fig. 4. Effect of grazing on fungi. (Depth: QB = 101.30, p = 0.01; QW = 522.79, QB = 51.56, Duration: < 10: QW = 78.86, p = 0.001; 10–20: QW = 14.36, QB = 9.48, QB = 51.07, p = 0.035; > 20: QW = 37.44, p = 0.044); L: Light grazing intensity; M: Moderate grazing intensity; H: heavy grazing intensity.

53

Agriculture, Ecosystems and Environment 249 (2017) 50–56

F. Zhao et al.

Fig. 5. Effect of grazing on bacteria. (Depth: QB = 32.50, p = 0.037; QW = 212.52, QB = 73.19, Duration: < 10: QW = 76.27, p = 0.001; 10–20: QW = 13.66, QB = 3.10, QB = 12.10, p = 0.101; > 20: QW = 9.12, p = 0.211); L: Light grazing intensity; M: Moderate grazing intensity; H: heavy grazing intensity.

4. Discussion

size by 19.78, 28.30 and 9.82% in < 10, 10–20 and > 20 yr, respectively. In detail, heavy grazing intensity significantly decrease 25.76, 47.36, and 10.48% in < 10 yr, 10–20 yr, and > 20 yr, and significant increase was found only in moderate grazing intensity in 10–20 yr.

Livestock grazing has substantial impacts on the belowground C cycles (Zou et al., 2007), but there is a lack of consistency in the existing reports on the actual effects of grazing on SR (Chen et al., 2016; Zhou et al., 2017). This may be due to the poor understanding of the associated underlying mechanisms. In the current study, we founded that the effects of grazing on microbial community size are largely dependent on the grazing intensity. More important, the responses of microbial community size to grazing are well correlated with the corresponding responses of SR, even when evaluated by irrespective of grazing intensity. These results would provide us novel insights from the microbial community size to reconcile the wide spectrum of alteration in the SR observed in responses to grazing. Furthermore, these our results also highlight underscores the importance of that grazing intensity could be an important factor affecting in determining key the responses of soil C dynamics to grazing and therefore should be fully considered incorporated into any future the biogeochemical models when designed attempting to better for understanding the responses of soil C dynamics to grazing.

3.5. Soil respiration A number of studies reported the effects of grazing on SR in addition to the effects of grazing intensity on microbial, fungal and bacterial community size. We found significant linear relationship between RR of total soil microbial community size and SR (Fig. 6). However, RR of total microbial community size was positively related with SR under light grazing intensity (n = 58, r = 0.51), whereas, under heavy grazing intensity, we observed a negative association with total RR and SR (n = 32, r = 0.37).

4.1. Microbial community size is modulated by grazing intensity Grazing is considered as one of the most widespread grassland management strategies, which has important consequences for soil microbial community size due to changes in substrate availability for soil microorganisms (Stark et al., 2015). Our meta-analysis indicates that low grazing intensity tended to increase the microbial community size, while heavy grazing intensity decreased soil microbial community size (Figs. 2–4). These results are in line with previous studies, on alpine grassland grazing, at lightly intensity was found to significantly enhance microbial community size (Zhou et al., 2010), but reductions in microbial community size were also reported in the same ecosystem with relatively high grazing intensity (Qi et al., 2011). Moreover, recent work also illustrated that heavy grazing intensity significantly reduced soil bacterial diversity indices (Qu et al., 2016; Zhong et al., 2016),

Fig. 6. Relationships between the response ratios (RR) of soil microbial community size and RR of soil respiration (SR); L: Light grazing intensity; M: Moderate grazing intensity; H: heavy grazing intensity.

54

Agriculture, Ecosystems and Environment 249 (2017) 50–56

F. Zhao et al.

intensity would have differential effects on the autotrophic and heterotrophic components of SR, yet direct evidence is still lacking.

whereas moderate grazing intensity has the potential to affect the soil microbial diversity and stabilize ecosystem functions (Li et al., 2016). Thus, the effects of grazing on soil microbial community size would be largely depended on the grazing intensity. In addition to grazing intensity, a number of other factors were reportedly to influence the soil microbial community composition and its diversity by, namely the plant species populating the ecosystem (Liu et al., 2015), SOC (Wang et al., 2016), and soil C:N ratio (Ingram et al., 2008). Changes in microbial community size were are primarily associated with the above- and below- ground biomass (Zhou et al., 2017). A possible explanation for enhanced plant productivity in light grazing intensity would stimulate photosynthetically-fixed C inputs to belowground, leading to increased root exudates and root biomass (Zhou et al., 2017), which would consequently translate into a larger number of microorganisms. However, heavy grazing intensity could decrease defoliation cause losses of photosynthetic tissue and reduce belowground C inputs through lower root production and aboveground biomass (Aldezabal et al., 2015). Thus, it was not surprising that heavy grazing intensity would lead to reductions in microbial community size (Odriozola et al., 2014). Alternatively, light grazing intensity stimulated the cumulative net N mineralization (Xu et al., 2007; Brůček et al., 2009), supporting greater diversity in soil microbial. Thus, light grazing intensity will benefit grassland ecosystems in terms of dry matter production, nutrient cycling, and C and N storage, and thereby improve the soil microbial community and facilitate soil functions.

4.3. Uncertainties and implications Weak correlations between the response ratios of total microbial community size and SOC, TN, bacterial: fungal community size, MAT and MAP were observed in this study, whereas strong correlations between duration of grazing and the response ratios of total microbial community size (Figs. S1–S4). This indicates that MAT and MAP were not major factors that influence the responses of microbial community size to grazing. However, a recent case study indicated direct effects of temperatures on microbial activities in response to long-term grazing intensity (Stark et al., 2015), while another case study reported that semi-arid steppes are more sensitive to precipitation fluctuation than to temperature changes (Sharkhuu et al., 2016). These discrepancies may stem from the paucity of data for the various types of climatic regions, such as in arid and semiarid regions, cold areas and humid areas. Thus, future experiments should be conducted across a wide range of ecosystems to clarify the underlying principles. Grazing is worldwide grassland management strategy, and the effects of grazing on ecosystem C dynamics have been frequently investigated, yet there still remains a large uncertainty. Our study would probably provide novel insights from the grazing intensity to reconcile the differential impacts of grazing on ecosystem functions and service. Therefore, grazing intensity should be fully considered in the biogeochemical models to improve the model performance of ecosystem functions. The current study only constitutes an early attempt at linking soil microbial community size to SR under various grazing intensity, and future studies on the other ecosystem processes and ecosystem functions are clearly needed under grassland management strategies.

4.2. Concurrent response of microbial community size and SR to grazing intensity Grazing can directly or indirectly affect SR via changes in plant productivity, plant community succession, microbial community size, and nutrient availability (Kölbl et al., 2011). Some studies indicate that grazing could increase SR (Frank et al., 2002; Klumpp et al., 2007), while other studies illustrated that grazing reduced SR (Zou et al., 2007). Mechanisms of grazing on SR widely reported, include changes in soil temperature (Flanagan and Johnson, 2005; Odriozola et al., 2014), the daily maximum net photosynthetic rate (Liu et al., 2016), and precipitation fluctuation (Sharkhuu et al., 2016), the result is still highly under debate. In this meta-analysis, our results indicate that grazing intensity would affect soil microbial community sizes, which were significantly correlated with SR (Fig. 5). These results likely provide insights that grazing-induced changes in soil microbial community size are critical underlying mechanisms for the responses of SR, but further studies on the responses of specific microbial communities are needed. Soil moisture induced larger reductions under heavy grazing intensity, and might be another important factor contributing the differential responses of soil microbial community size and SR to grazing, since SR are is inextricably linked with soil moisture (Chen et al., 2016; Sharkhuu et al., 2016). This was probably due to the lower canopy cover and higher solar radiation in heavy grazing intensity site than in lower grazing intensity site (Ronga et al., 2015). On the other hand, heavy grazing intensity has been shown to increase soil bulk density but to decrease soil aeration these things are not contradictory, which leads to suppressed SR. This is likely due to the inhibition of SR diffusion from the soil and reduced soil microbial activity (Yan et al., 2011; Pan et al., 2016). The more pronounced reductions in aboveground biomass under heavy grazing intensity would repress SR through its influence on substrate availability (Ronga et al., 2015), particularly the root metabolic activity (Xu et al., 2016). This suggests that heavy grazing intensity induced reductions in SR could mainly be caused by reduction in soil autotrophic respiration. Moreover, reduced substrate supply from photosynthesis may also stimulate root death and decomposition in the heavy grazing intensity plots (Xu et al., 2016), possibly leading to enhanced heterotrophic respiration. These results imply that grazing

5. Conclusion Results indicates that the effects of grazing on soil microbial community sizes are largely dependent on grazing intensity via both biotic and abiotic factors. Moreover, the responses of microbial community size to grazing are closely correlated with the responses of SR, even when assessed at moderate and heavy grazing intensity. Soil microbial community size is an important underlying mechanism involved in determining soil C dynamics under various grazing intensity. Finally, our results highlight the need for incorporating the grazing intensity in the biogeochemical models to improve the model performance of soil C dynamics. Acknowledgments This study was supported by the National Natural Science Foundation of China (No 41601578; 41601290; 31270484; 31570440), Natural Science Foundation of Northwest University (15NW03), and Young Talent fund of University Association for Science and Technology in Shaanxi, China (20170302). This research was also supported by China Postdoctoral Science Foundation (2017M610647), the Natural Science Basic Research Plan in Shaanxi Province (2017JQ3041), fundamental research funds for the central universities (3102016QD078), and State Key Laboratory of Loess and Quaternary Geology (SKLLQG1303, SKLLQG1602), Key Laboratory of Aerosol Chemistry and Physics (KLACP-17-02) Institute of Earth Environment, Chinese Academy of Sciences. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.agee.2017.08.007. 55

Agriculture, Ecosystems and Environment 249 (2017) 50–56

F. Zhao et al.

Northup, B.K., Brown, J.R., Holt, J.A., 2000. Grazing impacts on the spatial distribution of soil microbial biomass around tussock grasses in a tropical grassland. Appl. Soil Ecol. 13, 259–270. Nunan, N., Daniell, T.J., Singh, B.K., Papert, A., Mcnicol, J.W., Prosser, J.I., 2005. Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. Appl. Environ. Microbiol. 71, 6784–6792. Odriozola, I., García-Baquero, G., Laskurain, N.A., Aldezabal, A., 2014. Livestock grazing modifies the effect of environmental factors on soil temperature and water content in a temperate grassland. Geoderma 235–236, 347–354. Olivera, N.L., Prieto, L., Bertiller, M.B., Ferrero, M.A., 2016. Sheep grazing and soil bacterial diversity in shrublands of the Patagonian Monte, Argentina. J. Arid Environ. 125, 16–20. Pan, Z., Johnson, D.A., Wei, Z., Ma, L., Rong, Y., 2016. Non-growing season soil CO2 efflux patterns in five land-use types in northern China. Atmos. Environ. 144, 160–167. Qi, S., Zheng, H., Lin, Q., Li, G., Xi, Z., Zhao, X., 2010. Effects of livestock grazing intensity on soil biota in a semiarid steppe of Inner Mongolia. Plant Soil 340, 117–126. Qu, T.B., Du, W.C., Yuan, X., Yang, Z.M., Liu, D.B., Wang, D.L., Yu, L.J., 2016. Impacts of grazing intensity and plant community composition on soil bacterial community diversity in a steppe grassland. PLoS One 11, e0159680. Raiesi, F., Asadi, E., 2006. Soil microbial activity and litter turnover in native grazed and ungrazed rangelands in a semiarid ecosystem. Biol. Fertil. Soils 43, 76–82. Ren, C., Chen, J., Deng, J., Zhao, F., Han, X., Yang, G., Tong, X., Feng, Y., Shelton, S., Ren, G., 2017. Response of microbial diversity to C:N:P stoichiometry in fine root and microbial biomass following afforestation. Biol. Fertil. Soils 1–12. Ronga, Y.P., Douglas, A.J., Fei, Y., 2015. Soil respiration patterns for four major land-use types of the agro-pastoral region of northern China. Agric. Ecosyst. Environ. 213, 142–150. Saggar, S., Bolan, N.S., Bhandral, R., Hedley, C.B., Luo, J., 2004. A review of emissions of methane, ammonia, and nitrous oxide from animal excreta deposition and farm effluent application in grazed pastures. N. Z. J. Agric. Res. 47, 513–544. Schuur, E.A.G., Bockheim, J., Canadell, J.G., Euskirchen, E., Field, C.B., Goryachkin, S.V., Hagemann, S., Kuhry, P., Lafleur, P.M., Lee, H., 2008. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. Bioscience 58, 701–714. Sharkhuu, A., Plante, A.F., Enkhmandal, O., Gonneau, C., Casper, B.B., Boldgiv, B., Petraitis, P.S., 2016. Soil and ecosystem respiration responses to grazing, watering and experimental warming chamber treatments across topographical gradients in northern Mongolia. Geoderma 269, 91–98. Shi, B., Gao, W., Jin, G., 2015. Effects on rhizospheric and heterotrophic respiration of conversion from primary forest to secondary forest and plantations in northeast China. Eur. J. Soil Biol. 66, 11–18. Stark, S., Männistö, M.K., Ganzert, L., Tiirola, M., Häggblom, M.M., 2015. Grazing intensity in subarctic tundra affects the temperature adaptation of soil microbial communities. Soil Biol. Biochem. 84, 147–157. Treseder, S.R.H., Kathleen, K., 2013. A meta-analysis of soil microbial biomass responses to forest disturbances. Front. Microbiol. 4, 163. Treseder, K.K., 2008. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol. Lett. 11, 1111–1120. Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707. Wang, X., McConkey, B.G., VandenBygaart, A.J., Fan, J., Iwaasa, A., Schellenberg, M., 2016. Grazing improves C and N cycling in the Northern Great Plains: a meta-analysis. Sci. Rep. 6. Xu, Y., Li, L., Wang, Q., Chen, Q., Cheng, W., 2007. The pattern between nitrogen mineralization and grazing intensities in an Inner Mongolian typical steppe. Plant Soil 300, 289–300. Xu, W., Li, X., Liu, W., Li, L., Hou, L., Shi, H., Xia, J., Liu, D., Zhang, H., Chen, Y., Cai, W., Fu, Y., Yuan, W., 2016. Spatial patterns of soil and ecosystem respiration regulated by biological and environmental variables along a precipitation gradient in semi-arid grasslands in China. Ecol. Res. 31, 505–513. Yan, R., Yan, Y., Xin, X., Yang, G., Xu, W., 2011. Changes in microorganisms and enzyme activities in soil under different grazing intensities in meadow steppe, Inner Mongolia. Ecol. Environ. Sci. 43 (9), 1918–1930. Yang, Y., Wu, L., Lin, Q., Yuan, M., Xu, D., Yu, H., Hu, Y., Duan, J., Li, X., He, Z., Xue, K., van Nostrand, J., Wang, S., Zhou, J., 2013. Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob. Change Biol. 19, 637–648. Zhang, S.Y., Li, X.Y., Ma, Y.J., Zhao, G.Q., Li, L., Chen, J., Jiang, Z.Y., Huang, Y.M., 2014. Interannual and seasonal variability in evapotranspiration and energy partitioning over the alpine riparian shrub Myricaria squamosa Desv. on Qinghai-Tibet Plateau. Cold Reg. Sci. Technol. 102, 8–20. Zhong, L., Hoogendoorn, C.J., Bowatte, S., Li, F.Y., Wang, Y., Luo, D., 2016. Slope class and grazing intensity effects on microorganisms and nitrogen transformation processes responsible for nitrous oxide emissions from hill pastures. Agric. Ecosyst. Environ. 217, 70–78. Zhou, X., Wang, J., Hao, Y., Wang, Y., 2010. Intermediate grazing intensities by sheep increase soil bacterial diversities in an Inner Mongolian steppe. Biol. Fertil. Soils 46, 817–824. Zhou, G., Zhou, X., He, Y., Shao, J., Hu, Z., Liu, R., Zhou, H., Hosseinibai, S., 2017. Grazing intensity significantly affects belowground carbon and nitrogen cycling in grassland ecosystems: a meta-analysis. Glob. Change Biol. 23, 1167–1179. Zou, C., Wang, K., Wang, T., Xu, W., 2007. Overgrazing and soil carbon dynamics in eastern Inner Mongolia of China. Ecol. Res. 22, 135–142.

References Aldezabal, A., Moragues, L., Odriozola, I., Mijangos, I., 2015. Impact of grazing abandonment on plant and soil microbial communities in an Atlantic mountain grassland. Appl. Soil Ecol. 96, 251–260. Brůček, P., Šimek, M., Hynšt, J., 2009. Long-term animal impact modifies potential production of N2O from pasture soil. Biol. Fertil. Soils 46, 27–36. Cao, G., Tang, Y., Mo, W., Wang, Y., Li, Y., Zhao, X., 2004. Grazing intensity alters soil respiration in an alpine meadow on the Tibetan plateau. Soil Biol. Biochem. 36, 237–243. Chen, J., Luo, Y., Xia, J., Jiang, L., Zhou, X., Lu, M., Liang, J., Shi, Z., Shelton, S., Cao, J., 2015a. Stronger warming effects on microbial abundances in colder regions. Sci. Rep. 5, 18032. Chen, J., Shi, W., Cao, J., 2015b. Effects of grazing on ecosystem CO2 exchange in a Meadow Grassland on the Tibetan Plateau during the growing season. Environ. Manage. 55, 347–359. Chen, J., Zhou, X., Wang, J., Hruska, T., Shi, W., Cao, J., Zhang, B., Xu, G., Chen, Y., Luo, Y., 2016. Grazing exclusion reduced soil respiration but increased its temperature sensitivity in a Meadow Grassland on the Tibetan Plateau. Ecol. Evol. 6, 675–687. Chen, J., Luo, Y., Li, J., Zhou, X., Cao, J., Wang, R.W., Wang, Y., Shelton, S., Jin, Z., Walker, L.M., 2017. Costimulation of soil glycosidase activity and soil respiration by nitrogen addition. Glob. Change Biol. 23, 1328–1337. Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitan, J.J., Encinar, D., Berdugo, M., Campbell, C.D., Singh, B.K., 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541. Dlamini, P., Chivenge, P., Chaplot, V., 2016. Overgrazing decreases soil organic carbon stocks the most under dry climates and low soil pH: a meta-analysis shows. Agric. Ecosyst. Environ. 221, 258–269. Dooley, S.R., Treseder, K.K., 2012. The effect of fire on microbial biomass: a meta-analysis of field studies. Biogeochemistry 109, 49–61. Flanagan, L.B., Johnson, B.G., 2005. Interacting effects of temperature, soil moisture and plant biomass production on ecosystem respiration in a northern temperate grassland. Agric. For. Meteorol. 130, 237–253. Ford, H., Rousk, J., Garbutt, A., Jones, L., Jones, D.L., 2012. Grazing effects on microbial community composition, growth and nutrient cycling in salt marsh and sand dune grasslands. Biol. Fertil. Soils 49, 89–98. Frank, A.B., Liebig, M.A., Hanson, J.D., 2002. Soil carbon dioxide fluxes in northern semiarid grasslands. Soil Biol. Biochem. 34, 1235–1241. Hanka, R., 1994. The handbook of research synthesis. Biometrics 22, 458. Hedges, L.V., Gurevitch, J., Curtis, P.S., 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156. Holden, S.R., Treseder, K.K., 2013. A meta-analysis of soil microbial biomass responses to forest disturbances. Front. Microbiol. 4. Hou, X.Y., Wang, Z., Michael, S.P., Ji, L., Yun, X.J., 2014. The response of grassland productivity, soil carbon content and soil respiration rates to different grazing regimes in a desert steppe in northern China. Rangel. J. 36, 573–582. Houlbrooke, D.J., Littlejohn, R.P., Morton, J.D., Paton, R.J., 2008. Effect of irrigation and grazing animals on soil quality measurements in the North Otago Rolling Downlands of New Zealand. Soil Use Manage. 24, 416–423. Hu, Z., Li, S., Guo, Q., Niu, S., He, N., Li, L., Yu, G., 2016. A synthesis of the effect of grazing exclusion on carbon dynamics in grasslands in China. Glob. Change Biol. 22, 1385–1393. Ingram, L.J., Stahl, P.D., Schuman, G.E., Buyer, J.S., Vance, G.F., Ganjegunte, G.K., Welker, J.M., Derner, J.D., 2008. Grazing impacts on soil carbon and microbial communities in a mixed-grass ecosystem. Soil Sci. Soc. Am. J. 72, 939. Jones, M.B., Donnelly, A., 2005. Carbon sequestration in temperate grassland ecosystems and the influence of management, climate and elevated CO2. N. Phytol. 164, 423–439. Kölbl, A., Steffens, M., Wiesmeier, M., Hoffmann, C., Funk, R., Krümmelbein, J., Reszkowska, A., Zhao, Y., Peth, S., Horn, R., 2011. Grazing changes topographycontrolled topsoil properties and their interaction on different spatial scales in a semiarid grassland of Inner Mongolia, P.R. China. Plant Soil 340, 35–58. Klumpp, K., Soussana, J.F., Falcimagne, R., 2007. Effects of past and current disturbance on carbon cycling in grassland mesocosms. Agric. Ecosyst. Environ. 121, 59–73. Leriche, H., Leroux, X., Gignoux, J., Tuzet, A., Fritz, H., Abbadie, L., Loreau, M., 2001. Which functional processes control the short-term effect of grazing on net primary production in grasslands? Oecologia 129, 114–124. Li, Y.M., Wang, S.P., Li, X.Z., Liu, W.S., Luo, C.C., Zhang, Z.H., Zhu, X.X., Jiang, L.L., Li, X., 2015. Soil bacterial community responses to warming and grazing in a Tibetan alpine meadow. FEMS Microbiol. Ecol. 92 (1) (fiv152). Li, Y., Lin, Q., Wang, S., Li, X., Liu, W., Luo, C., Zhang, Z., Zhu, X., Jiang, L., Li, X., 2016. Soil bacterial community responses to warming and grazing in a Tibetan alpine meadow. FEMS Microbiol. Ecol. 92 (1) (fiv152). Liu, N., Kan, H.M., Yang, G.W., Zhang, Y.J., 2015. Changes in plant, soil, and microbes in a typical steppe from simulated grazing: explaining potential change in soil C. Ecol. Monogr. 85, 260–286. Liu, H., Zang, R., Chen, H.Y., 2016. Effects of grazing on photosynthetic features and soil respiration of rangelands in the Tianshan Mountains of Northwest China. Sci. Rep. 6, 30087. Luo, Y., Hui, D., Zhang, D., 2006. Elevated CO₂ stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87, 53–63. Moinet, G.Y.K., Cieraad, E., Hunt, J.E., Fraser, A., Turnbull, M.H., Whitehead, D., 2016. Soil heterotrophic respiration is insensitive to changes in soil water content but related to microbial access to organic matter. Geoderma 274, 68–78.

56