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Grazing-induced reduction of natural nitrous oxide release from continental steppe


Atmospheric concentrations of the greenhouse gas nitrous oxide (N2O) have increased significantly since pre-industrial times owing to anthropogenic perturbation of the global nitrogen cycle1,2, with animal production being one of the main contributors3. Grasslands cover about 20 per cent of the temperate land surface of the Earth and are widely used as pasture. It has been suggested that high animal stocking rates and the resulting elevated nitrogen input increase N2O emissions4,5,6,7. Internationally agreed methods to upscale the effect of increased livestock numbers on N2O emissions are based directly on per capita nitrogen inputs8. However, measurements of grassland N2O fluxes are often performed over short time periods9, with low time resolution and mostly during the growing season. In consequence, our understanding of the daily and seasonal dynamics of grassland N2O fluxes remains limited. Here we report year-round N2O flux measurements with high and low temporal resolution at ten steppe grassland sites in Inner Mongolia, China. We show that short-lived pulses of N2O emission during spring thaw dominate the annual N2O budget at our study sites. The N2O emission pulses are highest in ungrazed steppe and decrease with increasing stocking rate, suggesting that grazing decreases rather than increases N2O emissions. Our results show that the stimulatory effect of higher stocking rates on nitrogen cycling4,7 and, hence, on N2O emission is more than offset by the effects of a parallel reduction in microbial biomass, inorganic nitrogen production and wintertime water retention. By neglecting these freeze–thaw interactions, existing approaches may have systematically overestimated N2O emissions over the last century for semi-arid, cool temperate grasslands by up to 72 per cent.

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Figure 1: Dynamics of N 2 O fluxes, soil air concentrations and environmental parameters.
Figure 2: Effect of stocking rate on cumulative N 2 O fluxes, as recorded using the manual-chamber approach.
Figure 3: Annual N 2 O emissions and livestock numbers between 1890 and 2000 for situation S1.

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  1. Solomon, S. et al. (eds) Climate Change 2007: The Physical Science Basis 143–145 (Cambridge Univ. Press, 2007)

    Google Scholar 

  2. Mosier, A. et al. Closing the global N2O budget: nitrous oxide emissions through the agricultural nitrogen cycle - OECD/IPCC/IEA phase II development of IPCC guidelines for national greenhouse gas inventory methodology. Nutr. Cycl. Agroecosyst. 52, 225–248 (1998)

    Article  CAS  Google Scholar 

  3. Davidson, E. A. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nature Geosci. 2, 659–662 (2009)

    Article  ADS  CAS  Google Scholar 

  4. Ma, X. Z. et al. Short-term effects of sheep excrement on carbon dioxide, nitrous oxide and methane fluxes in typical grassland of Inner Mongolia. N. Zeal. J. Agric. Res. 49, 285–297 (2006)

    Article  CAS  Google Scholar 

  5. Oenema, O., Velthof, G. L., Yamulki, S. & Jarvis, S. C. Nitrous oxide emissions from grazed grassland. Soil Use Manage. 13, 288–295 (1997)

    Article  Google Scholar 

  6. Saggar, S., Hedley, C. B., Giltrap, D. L. & Lambie, S. M. Measured and modelled estimates of nitrous oxide emission and methane consumption from a sheep-grazed pasture. Agric. Ecosyst. Environ. 122, 357–365 (2007)

    Article  CAS  Google Scholar 

  7. Yamulki, S., Jarvis, S. C. & Owen, P. Nitrous oxide emissions from excreta applied in a simulated grazing pattern. Soil Biol. Biochem. 30, 491–500 (1998)

    Article  CAS  Google Scholar 

  8. Eggleston, S., Buendia, L., Miwa, K., Ngara, T. & Tanabe, K. (eds) 2006 IPCC Guidelines for National Greenhouse Gas Inventories 10.53–11.54 (Institute for Global Environmental Strategies, 2006)

    Google Scholar 

  9. Matzner, E. & Borken, W. Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review. Eur. J. Soil Sci. 59, 274–284 (2008)

    Article  Google Scholar 

  10. Groffman, P. M., Hardy, J. P., Driscoll, C. T. & Fahey, T. J. Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Glob. Change Biol. 12, 1748–1760 (2006)

    Article  ADS  Google Scholar 

  11. Papen, H. & Butterbach-Bahl, K. A 3-year continuous record of nitrogen trace gas fluxes from untreated and limed soil of a N-saturated spruce and beech forest ecosystem in Germany - 1. N2O emissions. J. Geophys. Res. 104, 18487–18503 (1999)

    Article  ADS  CAS  Google Scholar 

  12. Rover, M., Heinemeyer, O. & Kaiser, E. A. Microbial induced nitrous oxide emissions from an arable soil during winter. Soil Biol. Biochem. 30, 1859–1865 (1998)

    Article  CAS  Google Scholar 

  13. Hoffmann, C. et al. Effects of grazing and topography on dust flux and deposition in the Xilingele grassland, Inner Mongolia. J. Arid Environ. 72, 792–807 (2008)

    Article  ADS  Google Scholar 

  14. Essery, R. & Pomeroy, J. Vegetation and topographic control of wind-blown snow distributions in distributed and aggregated simulations for an Arctic tundra basin. J. Hydrom. 5, 735–744 (2004)

    Article  Google Scholar 

  15. Brooks, P. D., Williams, M. W. & Schmidt, S. K. Inorganic nitrogen and microbial biomass dynamics before and during spring snowmelt. Biogeochemistry 43, 1–15 (1998)

    Article  Google Scholar 

  16. Rivkina, E. M., Friedmann, E. I., McKay, C. P. & Gilichinsky, D. A. Metabolic activity of permafrost bacteria below the freezing point. Appl. Environ. Microbiol. 66, 3230–3233 (2000)

    Article  ADS  CAS  Google Scholar 

  17. Sharma, S. et al. Influence of freeze-thaw stress on the structure and function of microbial communities and denitrifying populations in soil. Appl. Environ. Microbiol. 72, 2148–2154 (2006)

    Article  ADS  CAS  Google Scholar 

  18. Koponen, H. T. & Martikainen, P. J. Soil water content and freezing temperature affect freeze-thaw related N2O production in organic soil. Nutr. Cycl. Agroecosyst. 69, 213–219 (2004)

    Article  CAS  Google Scholar 

  19. Teepe, R., Vor, A., Beese, F. & Ludwig, B. Emissions of N2O from soils during cycles of freezing and thawing and the effects of soil water, texture and duration of freezing. Eur. J. Soil Sci. 55, 357–365 (2004)

    Article  CAS  Google Scholar 

  20. Mosier, A. R. et al. CH4 and N2O fluxes in the Colorado shortgrass steppe. 2. Long-term impact of land use change. Glob. Biogeochem. Cycles 11, 29–42 (1997)

    Article  ADS  CAS  Google Scholar 

  21. Ramankutty, N., Evan, A. T., Monfreda, C. & Foley, J. A. Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Glob. Biogeochem. Cycles 22, GB1003 (2008)

    Article  ADS  Google Scholar 

  22. New, M., Lister, D., Hulme, M. & Makin, I. A high-resolution data set of surface climate over global land areas. Clim. Res. 21, 1–25 (2002)

    Article  Google Scholar 

  23. FertiStat Fertilizer use by crop statistics. Food Agric. Org. UN〉 (2007)

  24. FAOSTAT. Food Agric. Org. UN〉 (2008)

  25. Mitchell, B. R. International Historical Statistics: Europe 1750–1988 3rd edn, 325–370 (Stockton, 1992)

    Book  Google Scholar 

  26. Mitchell, B. R. International Historical Statistics: The Americas 1750–1988 2nd edn, Ch. C (Stockton, 1993)

    Book  Google Scholar 

  27. Mitchell, B. R. International Historical Statistics: Africa, Asia and Oceania 1750–1988 2nd rev. edn, Ch. C (Stockton, 1995)

    Book  Google Scholar 

  28. Crutzen, P. J., Mosier, A. R., Smith, K. A. & Winiwarter, W. N2O release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos. Chem. Phys. 8, 389–395 (2008)

    Article  ADS  CAS  Google Scholar 

  29. Dannenmann, M., Gasche, R., Ledebuhr, A. & Papen, H. Effects of forest management on soil N cycling in beech forests stocking on calcareous soils. Plant Soil 287, 279–300 (2006)

    Article  CAS  Google Scholar 

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This work has been supported by the German Research Foundation (DFG research group 536, ‘Matter fluxes in grasslands of Inner Mongolia as influenced by stocking rate’) and the National Natural Science Foundation of China (grant number 40805061), with co-funding from the NitroEurope Integrated Project of the European Commission. We thank K. K. Goldewijk for providing livestock data for the years before 1961, and Z. Yu, K. Müller, L. Lin, P. Schoenbach, G. Willibald, R. Kiese, C. Werner and C. Liu for support with field measurements.

Author Contributions K.B.-B., N.B., X.Z. and M.D. designed the experiment. B.W., W.C. and Z.Y. carried out the flux measurements. H.W. conducted the microbiological measurements. B.W., W.C., H.W. and M.D. performed data analysis. B.W. carried out the upscaling for temperate grasslands. M.A.S., K.B.-B., N.B., M.D. and B.W. drafted the manuscript.

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Correspondence to Klaus Butterbach-Bahl.

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Wolf, B., Zheng, X., Brüggemann, N. et al. Grazing-induced reduction of natural nitrous oxide release from continental steppe. Nature 464, 881–884 (2010).

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