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.
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.
Citation: Zhang L, Guo D, Niu S, Wang C, Shao C, Li L (2012) Effects of Mowing on Methane Uptake in a Semiarid Grassland in Northern China. PLoS ONE 7(4): e35952. https://doi.org/10.1371/journal.pone.0035952
Editor: Kurt O. Reinhart, USDA-ARS, United States of America
Received: August 8, 2011; Accepted: March 28, 2012; Published: April 25, 2012
Copyright: © 2012 Zhang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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.
Competing interests: The authors have declared that no competing interests exist.
Methane (CH4) is an important greenhouse gas and plays an important role in the global carbon (C) cycle . It has a potent global warming potential (i.e. 25-fold higher than carbon dioxide in mass at a 100-year time horizon ) and is increasing at an annual rate of 1% in the atmosphere due to anthropogenic activities .
Arid and semiarid grasslands have been considered to be sinks for atmospheric CH4 , . Recent studies demonstrated that human activities have greatly altered the strength of CH4 uptake in grasslands and may affect the global CH4 budget –. Mowing, an important human practice in the Eurasian steppe management, has various effects on this semiarid grassland ecosystem –, 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 . Removal of biomass by mowing may affect CH4 uptake due to concurrent changes in nutrients for soil microbial growth –. In addition, mowing can alter availability of light to plants , soil surface temperature, and moisture  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 –. It is further predicted that if the effect of grazing is taken into account, the steppe ecosystem would become a CH4 source , . 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 . 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 .
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.
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 . 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 – 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) . 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 ).
Aboveground plant biomass was measured using the harvest method according to Chen . 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  following the protocols described by Liu et al. (2007) .
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).
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).
The arrow indicated the mowing date every year.
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.
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.
Soil temperature and moisture related to methane uptake
Positive correlations between CH4 uptake and soil temperature have been reported in several studies , , –. 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 . Other previous studies also reported that soil moisture associated with soil diffusivity is the major factor controlling CH4 uptake rate in the field , , while soil temperature is just a covariate , .
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 . 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 . 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).
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 . A number of studies reported that changes in soil inorganic N availability , due to reduced amounts of C entering into the soil, were responsible for changes in soil CH4 oxidation microbial activities . In grassland ecosystems, long-term harvesting by mowing has been shown to divert plant C from soils, posing negative effects on soil microbial populations  and forage production (ANPP) . 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 .
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  and stimulation of root exudation, favoring the microbial activity . 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 . And in our study, the increase in CH4 uptake with mowing could also result from changes in methanotrophy community structure and activity . Finally, there are some other factors that can affect the CH4 uptake, such as variation of root/shoot ratios  and species composition  after mowing.
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.
We thank Dr. Wenhao Zhang and Dr. Paul L. E. Bodelier for their helpful comments on an earlier version of this manuscript.
Conceived and designed the experiments: LL LZ CW. Performed the experiments: LZ DG. Analyzed the data: LZ LL SN. Contributed reagents/materials/analysis tools: LZ LL CS. Wrote the paper: LZ CS LL. Obtained permission for use: LL LZ.
- 1. Li L, H X, Liu H, Chen ZZ (1998) Study on the carbon cycling of a Leymus chinensis steppe in the Xilin River Basin, Acta Bot Sin 40: 955–961.L. LiX. HH. LiuZZ Chen1998Study on the carbon cycling of a Leymus chinensis steppe in the Xilin River Basin,Acta Bot Sin40955961
- 2. IPCC (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK. IPCC2007Climate Change 2007: The Physical Science Basis.Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK
- 3. Dlugokencky EJ, Houweling S, Bruhwiler L, Masarie KA, Lang PM, et al. (2003) Atmospheric methane levels off: temporary pause or a new steady-state? Geophysical Research Letters 30: 1–48.EJ DlugokenckyS. HouwelingL. BruhwilerKA MasariePM Lang2003Atmospheric methane levels off: temporary pause or a new steady-state?Geophysical Research Letters30148
- 4. Potter CS, Davidson EA, Verchot LV (1996) Estimation of global biogeochemical controls and seasonality in soil methane consumption. Chemosphere 32: 2219–2246.CS PotterEA DavidsonLV Verchot1996Estimation of global biogeochemical controls and seasonality in soil methane consumption.Chemosphere3222192246
- 5. Dalal R, Allen D, Livesley S, Richards G (2008) Magnitude and biophysical regulators of methane emission and consumption in the Australian agricultural, forest, and submerged land scapes: a review. Plant and Soil 309: 89–103.R. DalalD. AllenS. LivesleyG. Richards2008Magnitude and biophysical regulators of methane emission and consumption in the Australian agricultural, forest, and submerged land scapes: a review.Plant and Soil30989103
- 6. Mosier AR, Schimel D, Valentine D, Bronson K, Parton W (1991) Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands. Nature 360: 330–332.AR MosierD. SchimelD. ValentineK. BronsonW. Parton1991Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands.Nature360330332
- 7. Mosier AR, Parton WJ, Valentine DW, Ojima DS, Schimel DS, et al. (1997) CH4 and N2O fluxes in Colorado short-grass steppe. 2. Long-term impact of land use change. Global Biogeochem Cycles 11: 29–42.AR MosierWJ PartonDW ValentineDS OjimaDS Schimel1997CH4 and N2O fluxes in Colorado short-grass steppe. 2. Long-term impact of land use change.Global Biogeochem Cycles112942
- 8. Smith KA, Dobbie KE, Ball BC, Bakken LR, Sitaula BK, et al. (2000) Oxidation of atmospheric methane in Northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink. Global Change Biolo 6: 791–803.KA SmithKE DobbieBC BallLR BakkenBK Sitaula2000Oxidation of atmospheric methane in Northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink.Global Change Biolo6791803
- 9. Merino A, Perez-Batallon P, Macıas F (2004) 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 36: 917–925.A. MerinoP. Perez-BatallonF. Macıas2004Responses 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 Biogeoch36917925
- 10. Robson TM, Lavorel S, Clement JC, Rouxc XL (2007) Neglect of mowing and manuring leads to slower nitrogen cycling in subalpine grasslands. Soil Biol & Biochem 39: 930–941.TM RobsonS. LavorelJC ClementXL Rouxc2007Neglect of mowing and manuring leads to slower nitrogen cycling in subalpine grasslands.Soil Biol & Biochem39930941
- 11. Ilmarinen K, Mikola J (2009) Soil feedback does not explain mowing effects on vegetation structure in a semi-natural grassland. Acta Oecolog 35: 838–848.K. IlmarinenJ. Mikola2009Soil feedback does not explain mowing effects on vegetation structure in a semi-natural grassland.Acta Oecolog35838848
- 12. Ilmarinen K, Mikola J, Nissinen K, Vestberg M (2009) Role of Soil Organisms in the Maintenance of Species-Rich Seminatural Grasslands through Mowing. Restoration Ecology 17: 78–88.K. IlmarinenJ. MikolaK. NissinenM. Vestberg2009Role of Soil Organisms in the Maintenance of Species-Rich Seminatural Grasslands through Mowing.Restoration Ecology177888
- 13. Luo Y, Sherry R, Zhou X, Wan S (2009) Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest. Global Change Biolo 1: 62–74.Y. LuoR. SherryX. ZhouS. Wan2009Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest.Global Change Biolo16274
- 14. Foster BL, Kindscher K, Houseman GR, Murphy CA (2009) Effects of hay management and native species sowing on grassland community structure, biomass, and restoration. Ecolog Applications 19: 1884–1896.BL FosterK. KindscherGR HousemanCA Murphy2009Effects of hay management and native species sowing on grassland community structure, biomass, and restoration.Ecolog Applications1918841896
- 15. Zhou Z, Wan S, Luo Y (2007) Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Globale Change Biol 13: 761–775.Z. ZhouS. WanY. Luo2007Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem.Globale Change Biol13761775
- 16. Bahn M, Knapp M, Garajova Z, Pfahringer N (2006) Root respiration in temperate mountain grasslands differing in land use. Global Change Biol 12: 995–1006.M. BahnM. KnappZ. GarajovaN. Pfahringer2006Root respiration in temperate mountain grasslands differing in land use.Global Change Biol129951006
- 17. Gavrichkova O, Moscatelli MC, Kuzyakov Y, Grego S, Valentini R (2010) Influence of defoliation on CO2 efflux from soil and microbial activity in a Mediterranean grassland. Agriculture, Ecosystems and Environ 136: 87–96.O. GavrichkovaMC MoscatelliY. KuzyakovS. GregoR. Valentini2010Influence of defoliation on CO2 efflux from soil and microbial activity in a Mediterranean grassland.Agriculture, Ecosystems and Environ1368796
- 18. Parr TW, Way JM (1988) Management of roadside vegetation: The long-term effects of cutting. J Applied Ecol 25: 1073–1087.TW ParrJM Way1988Management of roadside vegetation: The long-term effects of cutting.J Applied Ecol2510731087
- 19. Wan S, Luo Y, Wallace LL (2002) Changes in microclimate induced by experimental warming and clipping in tallgrass prairie. Global Change Biol 8: 754–768.S. WanY. LuoLL Wallace2002Changes in microclimate induced by experimental warming and clipping in tallgrass prairie.Global Change Biol8754768
- 20. Allard V, Soussana JF, Falcimagne R, Berbigier P, Bonnefond JM, et al. (2007) 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 121: 47–58.V. AllardJF SoussanaR. FalcimagneP. BerbigierJM Bonnefond2007The role of grazing management for the net biome productivity and greenhouse gas budget (CO2, N2O and CH4) of semi-natural grassland.Agriculture, Ecosystems and Environ1214758
- 21. Pinares-Patino CS, D'Hour P, Jouany JP, Martin C (2007) Effects of stocking rate on methane and carbon dioxide emissions from grazing cattle, Agriculture, Ecosystems and Environ 121: 30–46.CS Pinares-PatinoP. D'HourJP JouanyC. Martin2007Effects of stocking rate on methane and carbon dioxide emissions from grazing cattle,Agriculture, Ecosystems and Environ1213046
- 22. Liu C, Holst J, Bruggemann N, Butterbach-Bahl K, Yao Z, et al. (2007) Winter-grazing reduces methane uptake by soils of a typical semi-arid steppe in Inner Mongolia, China. Atmospheric Environ 41: 5948–5958.C. LiuJ. HolstN. BruggemannK. Butterbach-BahlZ. Yao2007Winter-grazing reduces methane uptake by soils of a typical semi-arid steppe in Inner Mongolia, China.Atmospheric Environ4159485958
- 23. Zhou XQ, Wang YF, Huang XZ, Hao YB, Tian JQ, et al. (2008) Effects of grazing by sheep on the structure of methane-oxidizing bacterial community of steppe soil, Soil Biol & Biochem 40: 258–261.XQ ZhouYF WangXZ HuangYB HaoJQ Tian2008Effects of grazing by sheep on the structure of methane-oxidizing bacterial community of steppe soil,Soil Biol & Biochem40258261
- 24. Lin X, Wang S, Ma X, Xu G, Luo C, et al. (2009) 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 41: 718–725.X. LinS. WangX. MaG. XuC. Luo2009Fluxes of CO2, CH4, and N2O in an alpine meadow affected by yak excreta on the Qinghai-Tibetan plateau during summer grazing periods,Soil Biol & Biochem41718725
- 25. Qi Y, Dong Y, Yang X, Geng Y, Liu L, et al. (2005) Effects of grazing on carbon dioxide and methane fluxes in typical temperate grassland in Inner Mongolia, China. Resources Science 27: 103–109 (in Chinese).Y. QiY. DongX. YangY. GengL. Liu2005Effects of grazing on carbon dioxide and methane fluxes in typical temperate grassland in Inner Mongolia, China.Resources Science27103109 (in Chinese)
- 26. Chen W, Wolf B, Zheng X, Yao Z, Butterbach-bahl K, et al. (2011) Annual methane uptake by temperate semiarid steppes as regulated by stocking rates, aboveground plant biomass and topsoil air permeability. Global Change Biol 2011doi: W. ChenB. WolfX. ZhengZ. YaoK. Butterbach-bahl2011Annual methane uptake by temperate semiarid steppes as regulated by stocking rates, aboveground plant biomass and topsoil air permeability.Global Change Biol2011doi10.1111/j.1365-2486.2011.02444.x. 10.1111/j.1365-2486.2011.02444.x.
- 27. Hirotaa M, Tanga Y, Hub Q, Katoc T, Hiratad S, et al. (2005) The potential importance of grazing to the fluxes of carbon dioxide and methane in an alpine wetland on the Qinghai-Tibetan Plateau. Atmospheric Environ 39: 5255–5259.M. HirotaaY. TangaQ. HubT. KatocS. Hiratad2005The potential importance of grazing to the fluxes of carbon dioxide and methane in an alpine wetland on the Qinghai-Tibetan Plateau.Atmospheric Environ3952555259
- 28. Liu C, Holst J, Yao Z, Bruggemann N, Butterbach-Bahl K, et al. (2009) Growing season methane budget of an Inner Mongolian steppe. Atmospheric Environ 43: 3086–3095.C. LiuJ. HolstZ. YaoN. BruggemannK. Butterbach-Bahl2009Growing season methane budget of an Inner Mongolian steppe.Atmospheric Environ4330863095
- 29. Wang Z, Song Y, Gulledge J, Yu Q, Liu H, et al. (2009) China's grazed temperate grasslands are a net source of atmospheric methane. Atmospheric Environ 43: 2148–2153.Z. WangY. SongJ. GulledgeQ. YuH. Liu2009China's grazed temperate grasslands are a net source of atmospheric methane.Atmospheric Environ4321482153
- 30. Xia J, Niu S, Wan S (2009) Response of ecosystem carbon exchange to warming and nitrogen addition during two hydrologically contrasting growing seasons in a temperate steppe. Global Change Biol 15: 1544–1556.J. XiaS. NiuS. Wan2009Response of ecosystem carbon exchange to warming and nitrogen addition during two hydrologically contrasting growing seasons in a temperate steppe.Global Change Biol1515441556
- 31. Bubier J, Moore T, Savage K, Crill P (2005) A comparison of methane flux in a boreal land scape between a dry and a wet year. Global Biogeochem Cycles 19: 1–11.J. BubierT. MooreK. SavageP. Crill2005A comparison of methane flux in a boreal land scape between a dry and a wet year.Global Biogeochem Cycles19111
- 32. Menyailo O, Hungate BA, Abraham W, Conrad R (2008) Changing landuse reduces soil CH4 uptake by altering biomass and activity but not composition of high-affinity methanotrophs. Global Change Biol 14: 2405–2419.O. MenyailoBA HungateW. AbrahamR. Conrad2008Changing landuse reduces soil CH4 uptake by altering biomass and activity but not composition of high-affinity methanotrophs.Global Change Biol1424052419
- 33. Huang Y, Sun W, Zhang W, Yu Y, Su Y, et al. (2010) Marshland conversion to cropland in northeast China from 1950 to 2000 reduced the greenhouse effect. Global Change Biol 16: 680–695.Y. HuangW. SunW. ZhangY. YuY. Su2010Marshland conversion to cropland in northeast China from 1950 to 2000 reduced the greenhouse effect.Global Change Biol16680695
- 34. Wang YS, Wang YH (2003) Quick measurement of CH4, CO2 and N2O emissions from short-plant ecosystems. Advances in Atmospheric Sciences 20: 842–844.YS WangYH Wang2003Quick measurement of CH4, CO2 and N2O emissions from short-plant ecosystems.Advances in Atmospheric Sciences20842844
- 35. Kaleita A, Heitman J, Logsdon S (2005) Field calibration of the theta probe for des moines lobe soils. Applied Engineering in Agricul 21: 865–870.A. KaleitaJ. HeitmanS. Logsdon2005Field calibration of the theta probe for des moines lobe soils.Applied Engineering in Agricul21865870
- 36. Chen Q, Wang Q, Han X, Wan S, Li L (2010) Temporal and spatial variability and controls of soil respiration in a temperate steppe in northern China. Global Biogeochem Cycles 24: GB2010.Q. ChenQ. WangX. HanS. WanL. Li2010Temporal and spatial variability and controls of soil respiration in a temperate steppe in northern China.Global Biogeochem Cycles24GB2010
- 37. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol and Biochem 19: 703–707.ED VancePC BrookesDS Jenkinson1987An extraction method for measuring soil microbial biomass C.Soil Biol and Biochem19703707
- 38. Liu W, Xu W, Han Y, Wang C, Wan S (2007) Response of microbial biomass and respiration of soil to topography, burning, and nitrogen fertilization in a temperate steppe. Biol and Fertil Soils 44: 259–268.W. LiuW. XuY. HanC. WangS. Wan2007Response of microbial biomass and respiration of soil to topography, burning, and nitrogen fertilization in a temperate steppe.Biol and Fertil Soils44259268
- 39. Wang Y, Xue M, Zheng X, Ji B, Du R, et al. (2005) Effects of environmental factors on N2O emission from and CH4 uptake by the typical grasslands in the Inner Mongolia. Chemosphere 58: 205–215.Y. WangM. XueX. ZhengB. JiR. Du2005Effects of environmental factors on N2O emission from and CH4 uptake by the typical grasslands in the Inner Mongolia.Chemosphere58205215
- 40. Peichl M, Altafarain M, Lah S, Moore T (2010) Carbon dioxide, methane, and nitrous oxide exchanges in an age-sequence of temperate pine forests. Global Change Biol 16: 2198–2212.M. PeichlM. AltafarainS. LahT. Moore2010Carbon dioxide, methane, and nitrous oxide exchanges in an age-sequence of temperate pine forests.Global Change Biol1621982212
- 41. Chen W, Wolf B, Yao Z, Brüggemann N, Butterbach-Bahl K, et al. (2010) Annual methane uptake by typical semiarid steppe in Inner Mongolia. Journal of Geophy Research. W. ChenB. WolfZ. YaoN. BrüggemannK. Butterbach-Bahl2010Annual methane uptake by typical semiarid steppe in Inner Mongolia.Journal of Geophy Research
- 42. Livesley SJ, Kiese R, Miehle P, Weston CJ, Butterbach-bahl K, et al. (2009) 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 15: 425–440.SJ LivesleyR. KieseP. MiehleCJ WestonK. Butterbach-bahl2009Soil–atmosphere exchange of greenhouse gases in a Eucalyptus marginata woodland, a clover-grass pasture, and Pinus radiata and Eucalyptus globulus plantations.Global Change Biol15425440
- 43. Burke IC, Mosier AR, Guerschman JP (2004) Methane and nitrous oxide fluxes from urban soils to the atmosphere. Ecolog Applications 14: 975–981.IC BurkeAR MosierJP Guerschman2004Methane and nitrous oxide fluxes from urban soils to the atmosphere.Ecolog Applications14975981
- 44. Li LH, Han XG, Wang QB, Chen QS (2002b) Correlations between plant biomass and soil respiration in a Leymus chinensis steppe community in the Xilin River Basin of Inner Mongolia. Acta Bot Sin 44: 593–597.LH LiXG HanQB WangQS Chen2002bCorrelations between plant biomass and soil respiration in a Leymus chinensis steppe community in the Xilin River Basin of Inner Mongolia.Acta Bot Sin44593597
- 45. Borken W, Davidson EA, Savage K, Sundquist ET, Steudler P (2006) Effect of summer throughfall exclusion, summer drought, and winter snow cover on methane fluxes in a temperate forest soil. Soil Biol and Biochem 38: 1388–1395.W. BorkenEA DavidsonK. SavageET SundquistP. Steudler2006Effect of summer throughfall exclusion, summer drought, and winter snow cover on methane fluxes in a temperate forest soil.Soil Biol and Biochem3813881395
- 46. Christensen TR (1993) Methane emission from arctic tundra. Biogeochem 21: 117–139.TR Christensen1993Methane emission from arctic tundra.Biogeochem21117139
- 47. Jin H, Sun OJ, Liu J (2010) Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem. J Plant Ecology. H. JinOJ SunJ. Liu2010Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem.J Plant Ecology
- 48. Gulledge J, HrywnaY , Cavanaugh C, Steudler PA (2004) Effects of long-term nitrogen fertilization on the uptake kinetics of atmospheric methane in temperate forest soils. FEMS Microbiology Ecol 49: 389–400.J. GulledgeHrywnaYC. CavanaughPA Steudler2004Effects of long-term nitrogen fertilization on the uptake kinetics of atmospheric methane in temperate forest soils.FEMS Microbiology Ecol49389400
- 49. Tate KR, Ross DJ, Saggar S, Hedleya CB, Dandoa J, et al. (2007) 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 39: 1437–1449.KR TateDJ RossS. SaggarCB HedleyaJ. Dandoa2007Methane 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 & Biochem3914371449
- 50. Garcia FO, Rice CW (1994) Microbial biomass dynamics in tall grass prairie. Soil Science Society of America J 58: 816–823.FO GarciaCW Rice1994Microbial biomass dynamics in tall grass prairie.Soil Science Society of America J58816823
- 51. Whiting GJ, Chanton JP (1993) Primary production control of methane emission from wetlands. Nature 364: 794–795.GJ WhitingJP Chanton1993Primary production control of methane emission from wetlands.Nature364794795
- 52. Reay DS, Nedwell DB (2004) Methane oxidation in temperate soils: effects of inorganic N. Soil Biol & Biochem 36: 2059–2065.DS ReayDB Nedwell2004Methane oxidation in temperate soils: effects of inorganic N.Soil Biol & Biochem3620592065
- 53. Lipson DA, Schmidt SK (2004) Seasonal changes in an alpine bacterial community in the Colorado Rocky Mountains. Applied and Environm Microbiol 70: 2867–2879.DA LipsonSK Schmidt2004Seasonal changes in an alpine bacterial community in the Colorado Rocky Mountains.Applied and Environm Microbiol7028672879
- 54. Sihgh BK, Tate K (2007) Biochemical and molecular characterization of methanotrophs in soil from a paristine New Zealand beech forest. FEMS Microbio Letters 275: 89–97.BK SihghK. Tate2007Biochemical and molecular characterization of methanotrophs in soil from a paristine New Zealand beech forest.FEMS Microbio Letters2758997
- 55. Priemé A, Christensen S, Dobbie KE, Smith KA (1997) Slow increase in rate of methane oxidation in soils with time following land use change from arable agriculture to woodland. Soil Biol and Biochem 29: 1269–1273.A. PrieméS. ChristensenKE DobbieKA Smith1997Slow increase in rate of methane oxidation in soils with time following land use change from arable agriculture to woodland.Soil Biol and Biochem2912691273
- 56. Nitschke N, Ebeling A, Rottstock T, Scherber C, Middelhoff C, et al. (2010) Time course of plant diversity effects on Certaurea jacea establishment and the role of competition and herbivory. J Plant Ecol. N. NitschkeA. EbelingT. RottstockC. ScherberC. Middelhoff2010Time course of plant diversity effects on Certaurea jacea establishment and the role of competition and herbivory.J Plant Ecol
- 57. Zhao N, Li YH, Wang ZW, Liu RT (2008) Seeding dynamics in response to mowing and grazing in a typical steppe community in Inner Mongolia, China. J Plant Ecology 32: 591–600.N. ZhaoYH LiZW WangRT Liu2008Seeding dynamics in response to mowing and grazing in a typical steppe community in Inner Mongolia, China.J Plant Ecology32591600