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. 2012 Apr 25;7(4):e35952. doi: 10.1371/journal.pone.0035952

Effects of Mowing on Methane Uptake in a Semiarid Grassland in Northern China

Lihua Zhang 1, Dufa Guo 2, Shuli Niu 1, Changhui Wang 1, Changliang Shao 1, Linghao Li 1,*
Editor: Kurt O Reinhart3
PMCID: PMC3338480  PMID: 22558280

Abstract

Background

Mowing is a widely adopted management practice for the semiarid steppe in China and affects CH4 exchange. However, the magnitude and the underlying mechanisms for CH4 uptake in response to mowing remain uncertain.

Methodology/Principal Findings

In two consecutive growing seasons, we measured the effect of mowing on CH4 uptake in a steppe community. Vegetation was mowed to 2 cm (M2), 5 cm (M5), 10 cm (M10), 15 cm (M15) above soil surface, respectively, and control was set as non-mowing (NM). Compared with control, CH4 uptake was substantially enhanced at almost all the mowing treatments except for M15 plots of 2009. CH4 uptake was significantly correlated with soil microbial biomass carbon, microbial biomass nitrogen, and soil moisture. Mowing affects CH4 uptake primarily through its effect on some biotic factors, such as net primary productivity, soil microbial C\N supply and soil microbial activities, while soil temperature and moisture were less important.

Conclusions/Significance

This study found that mowing affects the fluxes of CH4 in the semiarid temperate steppe of north China.

Introduction

Methane (CH4) is an important greenhouse gas and plays an important role in the global carbon (C) cycle [1]. It has a potent global warming potential (i.e. 25-fold higher than carbon dioxide in mass at a 100-year time horizon [2]) and is increasing at an annual rate of 1% in the atmosphere due to anthropogenic activities [3].

Arid and semiarid grasslands have been considered to be sinks for atmospheric CH4 [4], [5]. Recent studies demonstrated that human activities have greatly altered the strength of CH4 uptake in grasslands and may affect the global CH4 budget [6]–[9]. Mowing, an important human practice in the Eurasian steppe management, has various effects on this semiarid grassland ecosystem [10]–[13], including changes to CH4 uptake. Discerning the effect of mowing on CH4 fluxes is especially important because mowing is increasingly being used as a method to collect forage and feed livestock relative to traditional grazing practices [14]. Removal of biomass by mowing may affect CH4 uptake due to concurrent changes in nutrients for soil microbial growth [15]–[17]. In addition, mowing can alter availability of light to plants [18], soil surface temperature, and moisture [19] that affect CH4 production and consumption. However, the magnitude and underlying mechanisms of CH4 uptake in response to mowing remain uncertain.

In semiarid grasslands of Inner Mongolia, grazing is another important management practice. Previous studies report that grazing tended to reduce CH4 uptake in some grassland ecosystems [20]–[27]. It is further predicted that if the effect of grazing is taken into account, the steppe ecosystem would become a CH4 source [28], [29]. In contrast to grazing, mowing has the potential to increase the capacity of the system to function as a CH4 sink. We hypothesize that mowing tends to facilitate CH4 uptake in grassland ecosystems, because diminished soil inorganic N caused by mowing would result in CH4 oxidation [10]. However, there is no direct experimental evidence to support this hypothesis. In addition, it is not clear whether soil feedbacks, especially those in combination with aboveground or abiotic mechanisms, contribute to the changes in CH4 uptake in mowed grasslands. Therefore, a better understanding of the magnitude and the underlying mechanisms for CH4 exchanges in response to mowing is essential to accurately assess the CH4 sink-source functions of Eurasian grasslands in the global carbon budget [1].

The objectives of this study were: (1) to examine the effects of mowing on CH4 fluxes in a steppe habitat; (2) to study the effects of mowing on soil chemical and microbial properties; and (3) to determine the optimal mowing height (a surrogate for mowing intensity) that maximizes CH4 sink function of the grassland ecosystem.

Methods

Site description

The field experiment was conducted in a typical temperate steppe in Duolun County (116°17′E, 42°02′N, 1324 m asl), Inner Mongolia, North China. This area has a continental monsoon climate, being semiarid and temperate in summer. Mean annual temperature is about 2.1°C with monthly mean extreme temperatures of 18.9°C in July and −17.5°C in January. Mean annual precipitation is approximately 385 mm with about 80% occurring from mid-June to late September. The study site's soil is chestnut soil (Chinese classification) or Haplic Calcisols according to the FAO classification, with sand, silt and clay being 62.8%, 20.3% and 16.9% respectively. Mean soil bulk density is 1.31 g cm−3 and pH is 7.12 [30]. The dominant plant species are Artemisia frigida Willda, Stipa krylovii Roshev., Potentilla acaulis L., Cleistogenes squarrosa (Trin.) Keng., Allium bidentatum Fisch. Ex Prokh., and Agropyron cristatum (L.) Gaertn.

Field experimental design

The study site has been fenced to exclude grazing since 2001. From 2003, a 10-ha area in the Stipa krylovii community was enclosed, in which mowing (including collection of the hay) plots were established. We used a Latin square design with control and four levels of mowing treatments. Each treatment had five replicates. Twenty-five 10×20 m plots were arranged in a 5×5 matrix. The buffer distance between plots was 4 m. We used mowing height as a surrogate for mowing intensity. Vegetation was mowed at heights of 2 cm (M2), 5 cm (M5), 10 cm (M10),15 cm (M15) above soil surface and the control had non-mowing (NM, about 30 cm). A machine was used to mow the plots once annually in late August since 2003.

Measurements of CH4 flux and above ground plant biomass

The static opaque chamber method [31]–[33] was used to measure CH4 flux. One stainless steel base (50×50 cm) was installed into the soil of each plot. The steel base had a groove on top to ensure airtight connection with the chamber (50×50×50 cm) [34]. Two electric fans were installed inside the top of the chamber to mix the air during measurement. Gas samples of 60 mL were collected into syringes with airtight stopcocks at a 10-min interval during the 30 minutes of chamber closure. Simultaneously, air temperature and air pressure in the chamber were measured. Analysis of CH4 was conducted using a gas chromatograph (HP 5860, Agilent Technologies), which was equipped with flame ionization detector (FID) using 60–80 mesh 13 XMS column (2 mm inner diameter and 2 m long), with an oven temperature of 55°C. Nitrogen was used as the carrier gas with a flow rate of 30 mL min−1, and the CH4 flux was determined from changes in the slope of the mixing ratio of four samples taken at 0, 10, 20 and 30 min after chamber closure. Corrections were made for air temperature and pressure. The correlation coefficient of the regression was validated (r2≥0.95, n = 4). CH4 flux was measured weekly in 2008 from June to September and every two weeks in 2009 from May to September. Meanwhile soil (5 cm) temperature and moisture were measured by the Long-Stem Thermometer 6310 (Made in US) and portable soil moisture measuring kit ML2x (ThetaKit, Delta-T Devices, Cambridge, UK [35]).

Aboveground plant biomass was measured using the harvest method according to Chen [36]. We randomly selected 1 m2 square areas from every plot and clipped plant material 1 cm above the ground level.

Soil sampling and analysis

Soil samples (0–10 cm layer) were collected using soil corers (5 cm diameter) every month during the growing season in 2009. Three soil samples were taken randomly in each plot and mixed evenly. The mixed sample was then divided into two sub-samples, one stored at 4°C for microbial analysis and the other air-dried for soil total C, N and phosphorus (P) analyses. We collected a total of 250 soil samples (5 treatments×5 replicates×2 sub-samples×5 months). Soil microbial biomass carbon (MBC) and nitrogen (MBN) were determined using the chloroform fumigation–extraction method [37] following the protocols described by Liu et al. (2007) [38].

Statistical analysis

Seasonal mean CH4 uptake was calculated from the monthly mean values which were averaged by month. Seasonal cumulative CH4 uptake was calculated using a simple linear interpolation, by which the arithmetical mean of the two temporally closest observations was extrapolated to represent the flux of each duration. Differences in seasonal cumulative CH4 uptake, average ST, SM, soil MBC, and MBN among treatments were determined by analysis of variance (ANOVA) followed by multiple comparisons (Duncan test). Because the effect of mowing was different between 2008 and 2009, repeated-measures ANOVAs were applied to determine the main and interactive effects of measurement time and mowing treatment on CH4 uptake rate, ST, SM, soil MBC and MBN in the two growing seasons, respectively. The linear regression was used to determine the seasonal variation of CH4 uptake responses to ST, SM, soil MBC and MBN. Stepwise multiple linear analyses were used to examine post-mowing ecosystem CH4 uptake as a function of ST, SM, soil MBC, and MBN. All statistical analyses were conducted with SAS software (SAS Institute Inc., Cary, NC, USA).

Results

Effects of mowing on soil temperature and moisture

Soil temperature (ST; Fig. 1 A, B) and soil moisture (SM; Fig. 1 C, D) varied substantially throughout the growing seasons. Soil temperature was relatively low in May and September, while it was higher in July (Fig. 1A, B). Soil moisture was relatively high in July (Fig. 1C, D). Soil temperature was negatively correlated with mowing height (r2 = 0.74, p<0.001). Only 15 cm and 2 cm mowing height treatments significantly affected soil temperature (Table 1), whereas no regular correlation or significant effects were found between mowing height and soil moisture. However, there was a significant interactive effect between sampling date and all mowing treatments on soil temperature (p<0.0001) and soil moisture (p<0.0001) (Table 1).

Figure 1. Seasonal variations in soil temperature (A, B) and volumetric soil moisture (C, D) at the soil depth of 0–10 cm, and in fluxes of CH4 (E, F) in control and the four mowing treatments in 2008 (left) and 2009 (right); Data are mean ±SE (n = 5).

Figure 1

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The arrow indicated the mowing date every year.

Table 1. Results (P values) of repeated measures ANOVAs on the effects of mowing (M), sampling date (D), and their interactions on soil temperature (ST), soil moisture (SM), soil microbial biomass carbon (MBC), soil microbial biomass nitrogen (MBN) and CH4 uptake rate in all the mowing treatments.

ST SM MBC MBN CH4
2008 2009
M15 D <0.0001 <0.0001 0.033 0.0015 <0.0001 <0.0001
M 0.0127 0.1185 0.1816 0.0051 0.2841 0.1031
D×M 0.0002 <0.0001 0.2609 0.1322 0.0055 0.0171
M10 D <0.0001 <0.0001 0.0543 0.5226 0.0366 0.0015
M 0.9604 0.1231 0.0852 0.2153 0.067 0.0738
D×M 0.0082 <0.0001 0.4644 0.3332 0.4018 0.0128
M5 D <0.0001 <0.0001 0.0311 0.3296 0.0306 0.0006
M 0.1366 0.1745 0.2025 0.5497 0.7462 0.2509
D×M 0.0293 <0.0001 0.3787 0.2891 0.0984 0.0145
M2 D <0.0001 <0.0001 0.0221 0.001 0.002 0.0004
M 0.0033 0.1096 0.3951 0.7815 0.9513 0.1069
D×M 0.0063 0.0002 0.3019 0.6835 0.0071 0.0142
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Changes in soil microbial carbon and nitrogen

Both soil microbial biomass carbon and nitrogen (MBC and MBN) showed strong seasonal fluctuations with peak values (for no mowing and all mowing treatments) between June and July 2009 (Fig. 2C, D). Mostly, there was no effect of mowing treatments on MBC or MBN, except a marginally significant effect of one of the mowing treatments (M10) on soil MBC (p = 0.085) and a significant effect of another (M15) on soil MBN (p = 0.005). No significant interactive effects were found between sampling date and mowing on soil MBC and MBN for all the treatments (Table 1). Soil MBC in all the mowing treatments and soil MBN in M15 and M2 were strongly affected by sampling date (p<0.05). Changes in soil MBC and MBN became more evident from May to August; after which they remained almost unchanged (Fig. 2 C, D). Except for M15, other mowing treatments increased the seasonal averaged soil MBC and MBN (Fig. 2 C, D). Compared with control, M10, M5 and M2 enhanced soil MBC by 19.1%, 20% and 12.8%, and soil MBN by 2.0%, 0.2%, 2.0%, respectively. In contrast, the lightest level of mowing (M15) reduced soil MBC by 13.3% and soil MBN by 18.3%, respectively.

Figure 2. Monthly average CH4 uptake in control and different mowing treatments in 2008 (A) and 2009 (B), and effects of mowing on microbial biomass carbon (MBC) (C), microbial biomass nitrogen (MBN) (D).

Figure 2

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Vertical bars represent the standard error of the means (n = 5). Different letters between columns mean significant difference among treatments at P<0.05.

Effects of mowing on methane uptake

There were substantial seasonal variations in CH4 uptake for control and the mowing treatments in both 2008 and 2009 (Fig. 1E, F). The greatest CH4 emissions were in late July (Fig. 1E, F) during which soil moisture (Fig. 1C, D) and soil temperature (Fig. 1A, B) was also the highest. Inter-annual variations in CH4 uptake were also observed.

Mowing had different effects on the CH4 uptake rate at different temporal stages and different treatments (Fig. 2A, B). For instance, during the dry and warm periods during the growing season CH4 uptake rates were highest at M10 plots in 2008 and 2009 (Fig. 2A, B). When the seasonal cumulative uptake data in 2008 and 2009 were analyzed separately and collectively using ANOVA multiple comparison analysis, only one mowing treatment (M10) increased CH4 uptake relative to the no mowing and the M15 mowing treatment in 2009 (Fig. 3 B) as well as during 2008–2009 (Fig. 3 C). Moreover, there were significant interactive effects of the sampling date and mowing on CH4 uptake rate for all treatments in 2009 (p<0.05), and for M15 and M2 in 2008 (Table 1). Generally, the grassland was acting as a CH4 sink in the two growing seasons (Fig. 2 A, B; Fig. 3 A–C), and mowing had positive effects on the CH4 uptake with intermediate mowing height having the greatest impact.

Figure 3. Cumulative methane uptake in 2008 (A), 2009 (B) and the overall of the two growing seasons (C), and net aboveground primary productivity (ANPP) in 2008 (D), 2009 (E) and average of the two seasons (F) in response to mowing intensity.

Figure 3

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Values represent the mean±SE (n = 5). Different letters between columns mean significant difference among treatments at P<0.05.

Discussion

Soil temperature and moisture related to methane uptake

Positive correlations between CH4 uptake and soil temperature have been reported in several studies [22], [32], [39]–[41]. However, our results show that no significant correlations between soil temperature and CH4 uptake were found during the growing season, but positive correlations between soil moisture and CH4 uptake were significant (Fig. 4), which is consistent with that reported by Livesley [42]. Other previous studies also reported that soil moisture associated with soil diffusivity is the major factor controlling CH4 uptake rate in the field [8], [41], while soil temperature is just a covariate [43], [44].

Figure 4. Dependence of seasonal variation in CH4 uptake on soil moisture (SM), microbial biomass carbon (MBC) and microbial biomass nitrogen (MBN).

Figure 4

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Further analyses revealed that a combination of soil temperature (ST) and soil moisture (SM) slightly improved the correlation between CH4 uptake rate and SM (Y = 61.82−1.30ST+3.21SM, r2 = 0.26, p = 0.04), suggesting that SM is the dominant environmental factor controlling CH4 uptake in the study area. Previous studies reported that the activity of methanotrophs can be greatly inhibited by small variation in soil moisture [45]. Therefore, CH4 oxidation in dry soils is likely to be limited due to low microbial activity occurring during periods of low levels of soil moisture [46]. Similiarly, we found that there were positive relationships between SM and soil MBC\MBN (Fig. 5), and between soil MBC\MBN and CH4 uptake rate (Fig. 4).

Figure 5. Correlations between soil temperature (ST) and microbial biomass carbon\nitrogen (MBC\MBN), and between soil moisture (SM) and microbial biomass carbon\nitrogen (MBC\MBN).

Figure 5

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Soil microbial carbon and nitrogen associated with methane

Stepwise multiple regression analyses showed that soil MBC and MBN were positively correlated with CH4 uptake. Variations in soil MBC and MBN explained 34.9% (p = 0.002) and 20.7% (p = 0.022) of variations in CH4 uptake, respectively (Fig. 5). Soil moisture was positively correlated with soil MBC and MBN, explaining 48.4% and 68.3% of variations in soil MBC and MBN, respectively (p<0.0001) (Fig. 5), during the 2009 growing season. When the control and mowing treatments were considered separately, the same correlations between soil MBC, MBN and CH4 uptake were observed, and the best correlation was found in M10 treatment.

Mowing-induced changes in methane uptake

Our results show that effects of mowing on CH4 uptake were greatly dependent on the mowing height (Fig. 2 A, B). Moderate mowing heights (M10) enhanced CH4 uptake while the tallest mowing height (M15) resulted in less CH4 uptake than the M10 height, whereas no significant effects were found for other treatments (Fig. 2 B). Our study helps to illustrate that the effects of mowing on CH4 are complex and possibly mediated by: (1) changes to soil moisture; 2) changes to soil C/N supply possibly as a result of altered NPP; and 3) affects on soil microbial C and N.

While soil moisture was positively associated with CH4 uptake, mowing treatments generally had no effect on soil moisture except for two mowing treatments (M15, M2) (Table 1). This suggests mowing is affecting CH4 by affecting factors other than soil moisture. We observed that there were no apparent differences in standing dead, ground litter and canopy height between mowed and un-mowed plots in the growing seasons. However, light levels of mowing (M15) resulted in lower soil temperature and was associated with changes in community composition such as reduced forbs. This might explain the reduced CH4 uptake in M15 (Fig. 2 and 3), since CH4 oxidation is likely to be limited due to low microbial activity with reduced soil temperature.

We found CH4 uptake was negatively correlated with net above ground primary productivity (ANPP) (Fig. 6). This correlation may be the result of a shift in the intensity of competition between plants and CH4 oxidation microbes for soil nutrients, water and other resources. Soil microorganisms are known to respond to alterations in plant-derived C supply [47]. A number of studies reported that changes in soil inorganic N availability [48], due to reduced amounts of C entering into the soil, were responsible for changes in soil CH4 oxidation microbial activities [49]. In grassland ecosystems, long-term harvesting by mowing has been shown to divert plant C from soils, posing negative effects on soil microbial populations [50] and forage production (ANPP) [14]. Here light and intermediate mowing (M15, M10) had no effect on ANPP while more intensive mowing treatments (M5, M2) reduced ANPP (Fig. 3 D, E, F). Though mowing had subtle effects on ANPP, these effects correspond with the direct effects of mowing on CH4 suggesting a link between ANPP and CH4. Similar results have been reported by Whiting and Chanton in a wetland [51].

Figure 6. Dependence of seasonal cumulative CH4 uptake on the net aboveground primary productivity (ANPP, g m−2).

Figure 6

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In our study, mowing-induced increases in CH4 uptake may be mediated by changes in MBC and MBN (Fig. 2 C, D and Fig. 7). It has been reported that reduction in inorganic N by mowing resulted in an increase of CH4 oxidation [52] and stimulation of root exudation, favoring the microbial activity [53]. Other soil physical environmental factors caused by mowing could be co-responsible. For example, some have observed greater CH4 uptake rates in soil cores in New Zealand where type I methanotrophs are dominant [54]. And in our study, the increase in CH4 uptake with mowing could also result from changes in methanotrophy community structure and activity [55]. Finally, there are some other factors that can affect the CH4 uptake, such as variation of root/shoot ratios [56] and species composition [57] after mowing.

Figure 7. Mowing-induced changes in seasonal mean CH4 uptake rate and seasonal mean microbial biomass carbon (MBC).

Figure 7

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In general, our study demonstrates that moderate mowing can substantially enhance CH4 uptake in the semiarid steppe ecosystem. Long-term mowing increased CH4 uptake mainly due to its effect on soil biotic factors. 10 cm appeared to be the optimal mowing height. The substantial inter-annual variations in CH4 uptake indicate that it is necessary to conduct long-term observations in grasslands in the future to accurately determine the optimal mowing height for enhancing CH4 uptake.

Acknowledgments

We thank Dr. Wenhao Zhang and Dr. Paul L. E. Bodelier for their helpful comments on an earlier version of this manuscript.

Footnotes

Competing Interests: The authors have declared that no competing interests exist.

Funding: This work was funded by the National Natural Science Foundation of China (40801037), the State Key Research Development Program of China (2010CB951301-2) and State Key Laboratory of Vegetation and Environmental Change Youth Funds, and an open funding of the State Key Laboratory of Vegetation and Environmental Change, Institute of Botany. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  • 1.Li L, H X, Liu H, Chen ZZ. Study on the carbon cycling of a Leymus chinensis steppe in the Xilin River Basin, Acta Bot Sin. 1998;40:955–961. [Google Scholar]
  • 2.IPCC. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK; 2007. Climate Change 2007: The Physical Science Basis. [Google Scholar]
  • 3.Dlugokencky EJ, Houweling S, Bruhwiler L, Masarie KA, Lang PM, et al. Atmospheric methane levels off: temporary pause or a new steady-state? Geophysical Research Letters. 2003;30:1–48. [Google Scholar]
  • 4.Potter CS, Davidson EA, Verchot LV. Estimation of global biogeochemical controls and seasonality in soil methane consumption. Chemosphere. 1996;32:2219–2246. [Google Scholar]
  • 5.Dalal R, Allen D, Livesley S, Richards G. Magnitude and biophysical regulators of methane emission and consumption in the Australian agricultural, forest, and submerged land scapes: a review. Plant and Soil. 2008;309:89–103. [Google Scholar]
  • 6.Mosier AR, Schimel D, Valentine D, Bronson K, Parton W. Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands. Nature. 1991;360:330–332. [Google Scholar]
  • 7.Mosier AR, Parton WJ, Valentine DW, Ojima DS, Schimel DS, et al. CH4 and N2O fluxes in Colorado short-grass steppe. 2. Long-term impact of land use change. Global Biogeochem Cycles. 1997;11:29–42. [Google Scholar]
  • 8.Smith KA, Dobbie KE, Ball BC, Bakken LR, Sitaula BK, et al. Oxidation of atmospheric methane in Northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink. Global Change Biolo. 2000;6:791–803. [Google Scholar]
  • 9.Merino A, Perez-Batallon P, Macıas F. Responses of soil organic matter and greenhouse gas fluxes to soil management and landuse changes in a humid temperature region of southern Europe. Soil Biology and Biogeoch. 2004;36:917–925. [Google Scholar]
  • 10.Robson TM, Lavorel S, Clement JC, Rouxc XL. Neglect of mowing and manuring leads to slower nitrogen cycling in subalpine grasslands. Soil Biol & Biochem. 2007;39:930–941. [Google Scholar]
  • 11.Ilmarinen K, Mikola J. Soil feedback does not explain mowing effects on vegetation structure in a semi-natural grassland. Acta Oecolog. 2009;35:838–848. [Google Scholar]
  • 12.Ilmarinen K, Mikola J, Nissinen K, Vestberg M. Role of Soil Organisms in the Maintenance of Species-Rich Seminatural Grasslands through Mowing. Restoration Ecology. 2009;17:78–88. [Google Scholar]
  • 13.Luo Y, Sherry R, Zhou X, Wan S. Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest. Global Change Biolo. 2009;1:62–74. [Google Scholar]
  • 14.Foster BL, Kindscher K, Houseman GR, Murphy CA. Effects of hay management and native species sowing on grassland community structure, biomass, and restoration. Ecolog Applications. 2009;19:1884–1896. doi: 10.1890/08-0849.1. [DOI] [PubMed] [Google Scholar]
  • 15.Zhou Z, Wan S, Luo Y. Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Globale Change Biol. 2007;13:761–775. [Google Scholar]
  • 16.Bahn M, Knapp M, Garajova Z, Pfahringer N. Root respiration in temperate mountain grasslands differing in land use. Global Change Biol. 2006;12:995–1006. [Google Scholar]
  • 17.Gavrichkova O, Moscatelli MC, Kuzyakov Y, Grego S, Valentini R. Influence of defoliation on CO2 efflux from soil and microbial activity in a Mediterranean grassland. Agriculture, Ecosystems and Environ. 2010;136:87–96. [Google Scholar]
  • 18.Parr TW, Way JM. Management of roadside vegetation: The long-term effects of cutting. J Applied Ecol. 1988;25:1073–1087. [Google Scholar]
  • 19.Wan S, Luo Y, Wallace LL. Changes in microclimate induced by experimental warming and clipping in tallgrass prairie. Global Change Biol. 2002;8:754–768. [Google Scholar]
  • 20.Allard V, Soussana JF, Falcimagne R, Berbigier P, Bonnefond JM, et al. The role of grazing management for the net biome productivity and greenhouse gas budget (CO2, N2O and CH4) of semi-natural grassland. Agriculture, Ecosystems and Environ. 2007;121:47–58. [Google Scholar]
  • 21.Pinares-Patino CS, D'Hour P, Jouany JP, Martin C. Effects of stocking rate on methane and carbon dioxide emissions from grazing cattle, Agriculture, Ecosystems and Environ. 2007;121:30–46. [Google Scholar]
  • 22.Liu C, Holst J, Bruggemann N, Butterbach-Bahl K, Yao Z, et al. Winter-grazing reduces methane uptake by soils of a typical semi-arid steppe in Inner Mongolia, China. Atmospheric Environ. 2007;41:5948–5958. [Google Scholar]
  • 23.Zhou XQ, Wang YF, Huang XZ, Hao YB, Tian JQ, et al. Effects of grazing by sheep on the structure of methane-oxidizing bacterial community of steppe soil, Soil Biol & Biochem. 2008;40:258–261. [Google Scholar]
  • 24.Lin X, Wang S, Ma X, Xu G, Luo C, et al. Fluxes of CO2, CH4, and N2O in an alpine meadow affected by yak excreta on the Qinghai-Tibetan plateau during summer grazing periods, Soil Biol & Biochem. 2009;41:718–725. [Google Scholar]
  • 25.Qi Y, Dong Y, Yang X, Geng Y, Liu L, et al. Effects of grazing on carbon dioxide and methane fluxes in typical temperate grassland in Inner Mongolia, China. Resources Science. 2005;27:103–109 (in Chinese). [Google Scholar]
  • 26.Chen W, Wolf B, Zheng X, Yao Z, Butterbach-bahl K, et al. Annual methane uptake by temperate semiarid steppes as regulated by stocking rates, aboveground plant biomass and topsoil air permeability. Global Change Biol. 2011;2011doi 10.1111/j.1365-2486.2011.02444.x. [Google Scholar]
  • 27.Hirotaa M, Tanga Y, Hub Q, Katoc T, Hiratad S, et al. The potential importance of grazing to the fluxes of carbon dioxide and methane in an alpine wetland on the Qinghai-Tibetan Plateau. Atmospheric Environ. 2005;39:5255–5259. [Google Scholar]
  • 28.Liu C, Holst J, Yao Z, Bruggemann N, Butterbach-Bahl K, et al. Growing season methane budget of an Inner Mongolian steppe. Atmospheric Environ. 2009;43:3086–3095. [Google Scholar]
  • 29.Wang Z, Song Y, Gulledge J, Yu Q, Liu H, et al. China's grazed temperate grasslands are a net source of atmospheric methane. Atmospheric Environ. 2009;43:2148–2153. [Google Scholar]
  • 30.Xia J, Niu S, Wan S. Response of ecosystem carbon exchange to warming and nitrogen addition during two hydrologically contrasting growing seasons in a temperate steppe. Global Change Biol. 2009;15:1544–1556. [Google Scholar]
  • 31.Bubier J, Moore T, Savage K, Crill P. A comparison of methane flux in a boreal land scape between a dry and a wet year. Global Biogeochem Cycles. 2005;19:1–11. [Google Scholar]
  • 32.Menyailo O, Hungate BA, Abraham W, Conrad R. Changing landuse reduces soil CH4 uptake by altering biomass and activity but not composition of high-affinity methanotrophs. Global Change Biol. 2008;14:2405–2419. [Google Scholar]
  • 33.Huang Y, Sun W, Zhang W, Yu Y, Su Y, et al. Marshland conversion to cropland in northeast China from 1950 to 2000 reduced the greenhouse effect. Global Change Biol. 2010;16:680–695. [Google Scholar]
  • 34.Wang YS, Wang YH. Quick measurement of CH4, CO2 and N2O emissions from short-plant ecosystems. Advances in Atmospheric Sciences. 2003;20:842–844. [Google Scholar]
  • 35.Kaleita A, Heitman J, Logsdon S. Field calibration of the theta probe for des moines lobe soils. Applied Engineering in Agricul. 2005;21:865–870. [Google Scholar]
  • 36.Chen Q, Wang Q, Han X, Wan S, Li L. Temporal and spatial variability and controls of soil respiration in a temperate steppe in northern China. Global Biogeochem Cycles. 2010;24:GB2010. doi: 10.1029/2009GB003538. [Google Scholar]
  • 37.Vance ED, Brookes PC, Jenkinson DS. An extraction method for measuring soil microbial biomass C. Soil Biol and Biochem. 1987;19:703–707. [Google Scholar]
  • 38.Liu W, Xu W, Han Y, Wang C, Wan S. Response of microbial biomass and respiration of soil to topography, burning, and nitrogen fertilization in a temperate steppe. Biol and Fertil Soils. 2007;44:259–268. [Google Scholar]
  • 39.Wang Y, Xue M, Zheng X, Ji B, Du R, et al. Effects of environmental factors on N2O emission from and CH4 uptake by the typical grasslands in the Inner Mongolia. Chemosphere. 2005;58:205–215. doi: 10.1016/j.chemosphere.2004.04.043. [DOI] [PubMed] [Google Scholar]
  • 40.Peichl M, Altafarain M, Lah S, Moore T. Carbon dioxide, methane, and nitrous oxide exchanges in an age-sequence of temperate pine forests. Global Change Biol. 2010;16:2198–2212. [Google Scholar]
  • 41.Chen W, Wolf B, Yao Z, Brüggemann N, Butterbach-Bahl K, et al. Annual methane uptake by typical semiarid steppe in Inner Mongolia. Journal of Geophy Research. 2010 doi: 10.1029/2009JD013783. [Google Scholar]
  • 42.Livesley SJ, Kiese R, Miehle P, Weston CJ, Butterbach-bahl K, et al. Soil–atmosphere exchange of greenhouse gases in a Eucalyptus marginata woodland, a clover-grass pasture, and Pinus radiata and Eucalyptus globulus plantations. Global Change Biol. 2009;15:425–440. [Google Scholar]
  • 43.Burke IC, Mosier AR, Guerschman JP. Methane and nitrous oxide fluxes from urban soils to the atmosphere. Ecolog Applications. 2004;14:975–981. [Google Scholar]
  • 44.Li LH, Han XG, Wang QB, Chen QS. Correlations between plant biomass and soil respiration in a Leymus chinensis steppe community in the Xilin River Basin of Inner Mongolia. Acta Bot Sin. 2002b;44:593–597. [Google Scholar]
  • 45.Borken W, Davidson EA, Savage K, Sundquist ET, Steudler P. Effect of summer throughfall exclusion, summer drought, and winter snow cover on methane fluxes in a temperate forest soil. Soil Biol and Biochem. 2006;38:1388–1395. [Google Scholar]
  • 46.Christensen TR. Methane emission from arctic tundra. Biogeochem. 1993;21:117–139. [Google Scholar]
  • 47.Jin H, Sun OJ, Liu J. Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem. J Plant Ecology. 2010 doi: 10.1093/jpe/rtq001. [Google Scholar]
  • 48.Gulledge J, HrywnaY, Cavanaugh C, Steudler PA. Effects of long-term nitrogen fertilization on the uptake kinetics of atmospheric methane in temperate forest soils. FEMS Microbiology Ecol. 2004;49:389–400. doi: 10.1016/j.femsec.2004.04.013. [DOI] [PubMed] [Google Scholar]
  • 49.Tate KR, Ross DJ, Saggar S, Hedleya CB, Dandoa J, et al. Methane uptake in soils from Pinusradiata plantations, areverting shrub land and adjacent pastures: Effects of land-use change, and soil texture, water and mineral nitrogen. Soil Biol & Biochem. 2007;39:1437–1449. [Google Scholar]
  • 50.Garcia FO, Rice CW. Microbial biomass dynamics in tall grass prairie. Soil Science Society of America J. 1994;58:816–823. [Google Scholar]
  • 51.Whiting GJ, Chanton JP. Primary production control of methane emission from wetlands. Nature. 1993;364:794–795. [Google Scholar]
  • 52.Reay DS, Nedwell DB. Methane oxidation in temperate soils: effects of inorganic N. Soil Biol & Biochem. 2004;36:2059–2065. [Google Scholar]
  • 53.Lipson DA, Schmidt SK. Seasonal changes in an alpine bacterial community in the Colorado Rocky Mountains. Applied and Environm Microbiol. 2004;70:2867–2879. doi: 10.1128/AEM.70.5.2867-2879.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Sihgh BK, Tate K. Biochemical and molecular characterization of methanotrophs in soil from a paristine New Zealand beech forest. FEMS Microbio Letters. 2007;275:89–97. doi: 10.1111/j.1574-6968.2007.00885.x. [DOI] [PubMed] [Google Scholar]
  • 55.Priemé A, Christensen S, Dobbie KE, Smith KA. Slow increase in rate of methane oxidation in soils with time following land use change from arable agriculture to woodland. Soil Biol and Biochem. 1997;29:1269–1273. [Google Scholar]
  • 56.Nitschke N, Ebeling A, Rottstock T, Scherber C, Middelhoff C, et al. Time course of plant diversity effects on Certaurea jacea establishment and the role of competition and herbivory. J Plant Ecol. 2010 doi: 10.1093/jpe/rtp036. [Google Scholar]
  • 57.Zhao N, Li YH, Wang ZW, Liu RT. Seeding dynamics in response to mowing and grazing in a typical steppe community in Inner Mongolia, China. J Plant Ecology. 2008;32:591–600. [Google Scholar]

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