Biogeochemistry

, Volume 109, Issue 1–3, pp 85–100 | Cite as

Effects of multiple global change treatments on soil N2O fluxes

  • Jamie R. Brown
  • Joseph C. Blankinship
  • Audrey Niboyet
  • Kees Jan van Groenigen
  • Paul Dijkstra
  • Xavier Le Roux
  • Paul W. Leadley
  • Bruce A. Hungate
Article

Abstract

Global environmental changes are expected to alter ecosystem carbon and nitrogen cycling, but the interactive effects of multiple simultaneous environmental changes are poorly understood. Effects of these changes on the production of nitrous oxide (N2O), an important greenhouse gas, could accelerate climate change. We assessed the responses of soil N2O fluxes to elevated CO2, heat, altered precipitation, and enhanced nitrogen deposition, as well as their interactions, in an annual grassland at the Jasper Ridge Global Change Experiment (CA, USA). Measurements were conducted after 6, 7 and 8 years of treatments. Elevated precipitation increased N2O efflux, especially in combination with added nitrogen and heat. Path analysis supported the idea that increased denitrification due to increased soil water content and higher labile carbon availability best explained increased N2O efflux, with a smaller, indirect contribution from nitrification. In our data and across the literature, single-factor responses tended to overestimate interactive responses, except when global change was combined with disturbance by fire, in which case interactive effects were large. Thus, for chronic global environmental changes, higher order interactions dampened responses of N2O efflux to multiple global environmental changes, but interactions were strongly positive when global change was combined with disturbance. Testing whether these responses are general should be a high priority for future research.

Keywords

Interactions Global environmental change Elevated CO2 Warming Precipitation Nitrogen deposition Soil Grassland FACE Nitrification Denitrification Meta-analysis 

References

  1. Ambus P, Robertson GP (1999) Fluxes of CH4 and N2O in aspen stands grown under ambient and twice-ambient CO2. Plant Soil 209:1–8. doi:10.1023/A:1004518730970 Google Scholar
  2. Arnone JA, Bohlen PJ (1998) Stimulated N2sO flux from intact grassland monoliths after two growing seasons under elevated atmospheric CO2. Oecologia 116:331–335. doi:10.1007/s004420050594 CrossRefGoogle Scholar
  3. Attard E, Poly F, Laurent F, Commeaux C, Terada A, Smets B, Recous S, Le Roux X (2010) Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underly the response of soil nitrite oxidizing enzyme activity to changes in tillage practices. Environ Microbiol 12:315–326. doi:10.1111/j.1462-2920.2009.02070.x CrossRefGoogle Scholar
  4. Attard E, Recous S, Chabbi A, De Berranger C, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Le Roux X (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land-uses. Glob Change Biol 17:1975–1989. doi:10.1111/j.1365-2486.2010.02340.x CrossRefGoogle Scholar
  5. Avrahami S, Bohannan BJM (2007) Response of Nitrosospira sp. strain AF-like ammonia oxidizers to changes in temperature, soil moisture content and fertilizer concentration. Appl Environ Microbiol 73:1166–1173. doi:10.1128/AEM.00486-07 CrossRefGoogle Scholar
  6. Avrahami S, Bohannan BJM (2009) N2O emission rates in a California meadow soil are influenced by fertilizer level, soil moisture and the community structure of ammonia oxidizing bacteria. Glob Change Biol 15:643–655. doi:10.1111/j.1365-2486.2008.01727.x CrossRefGoogle Scholar
  7. Baggs EM, Blum H (2004) CH4 oxidation and emission of CH4 and N2O from Lolium perenne swards under elevated atmospheric CO2. Soil Biol Biochem 36:713–723. doi:10.1016/j.soilbio.2004.01.008 Google Scholar
  8. Baggs EM, Richter M, Hartwig UA, Cadisch G (2003) Nitrous oxide emissions from grass swards during the eighth year of elevated atmospheric pCO2 (Swiss FACE) Glob Change Biol 9:1214–1222 doi:10.1046/j.1365-2486.2003.00654.x Google Scholar
  9. Barnard R, Leadley PW, Hungate BA (2005) Global change, nitrification, and denitrification: a review. Glob Biogeochem Cycles 19:GB1007. doi:10.1029/2004GB002282 CrossRefGoogle Scholar
  10. Barnard R, Le Roux X, Hungate BA, Cleland EE, Blankinship JC, Barthes L, Leadley PW (2006) Several components of global change alter nitrifying and denitrifying activities in an annual grassland. Funct Ecol 20:557–564. doi:10.1111/j.1365-2435.2006.01146.x CrossRefGoogle Scholar
  11. Billings SA, Schaeffer SM, Evans RD (2002) Trace N gas losses and N mineralization in Mojave desert soils exposed to elevated CO2. Soil Biol Biochem 34:1777–1784. doi:10.1016/S0038-0717(02)00166-9 CrossRefGoogle Scholar
  12. Blankinship JC, Brown JR, Dijkstra P, Hungate BA (2010) Effects of interactive global change on methane uptake in an annual grassland. J Geophys Res 115:G02008. doi:10.1029/2009JG001097 CrossRefGoogle Scholar
  13. Bouwman AF, Boumans LJM, Batjes NH (2002) Emissions of N2O and NO from fertilized fields: summary of available measurement data. Glob Environ Cycle 16:1058. doi:10.1029/2001GB001811 CrossRefGoogle Scholar
  14. Braker G, Schwarz J, Conrad R (2010) Influence of temperature on the composition and activity of denitrifying soil communities. FEMS Microbiol Ecol 73:134–148. doi:10.1111/j.1574-6941.2010.00884.x Google Scholar
  15. Chèneby D, Brauman A, Rabary B, Philippot L (2009) Differential responses of nitrate reducer community size, structure, and activity to tillage systems. Appl Environ Microbiol 75:3180–3186. doi:10.1128/AEM.02338-08 CrossRefGoogle Scholar
  16. Cicerone RJ (1987) Changes in stratospheric ozone. Science 237:35–42. doi:10.1126/science.237.4810.35 CrossRefGoogle Scholar
  17. Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640Google Scholar
  18. Davidson EA (1992) Sources of nitric oxide and nitrous oxide following wetting of dry soil. Soil Sci Soc Am 56:95–102CrossRefGoogle Scholar
  19. Davidson EA, Keller M, Erickson HE, Verchot LV, Veldkamp E (2000) Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50:667–680CrossRefGoogle Scholar
  20. Davidson EA, Ishida FY, Nepstad DC (2004) Effects of an experimental drought on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob Change Biol 10:718–730. doi:10.1111/j.1365-2486.2004.00762.x CrossRefGoogle Scholar
  21. De Graaff MA, Van Groenigen KJ, Six J, Hungate BA, Van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12:2077–2091. doi:10.1111/j.1365-2486.2006.01240.x CrossRefGoogle Scholar
  22. Deiglmayr K, Philippot L, Hartwig UA, Kandeler E (2004) Structure and activity of the nitrate-reducing community in the rhizosphere of Lolium perenne and Trifolium repens under long-term elevated atmospheric pCO2. FEMS Microbiol Ecol 49:445–454. doi:10.1016/j.femsec.2004.04.017 CrossRefGoogle Scholar
  23. Del Grosso SJ, Mosier AR, Parton WJ, Ojima DS (2005) DAYCENT model analysis of past and contemporary soil N2O and net greenhouse gas flux for major crops in the USA. Soil Tillage Res 83:9–24. doi:10.1016/j.still.2005.02.007 CrossRefGoogle Scholar
  24. Dijkstra FA, Blumenthal D, Morgan JA, Pendall E, Carrillo Y, Follett RF (2010) Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland. New Phytol 187:426–437. doi:10.1111/j.1469-8137.2010.03293.x CrossRefGoogle Scholar
  25. Dobbie KE, McTaggart IP, Smith KA (1999) Nitrous oxide emissions from intensive agricultural systems: variations between crops and seasons, key driving variables, and mean emission factors. J Geophys Res 104:26891–26899.doi:10.1029/1999JD900378 CrossRefGoogle Scholar
  26. Docherty KM, Balser TC, Bohannan BJM, Gutknecht JLM (2011) Soil microbial responses to fire and interacting global change factors in a California annual grassland. Biogeochemistry. doi:10.1007/s10533-011-9654-3
  27. Dukes JS, Chiariello NR, Cleland EE, Moore LA, Shaw MR, Thayer S, Tobeck T, Mooney HA, Field CB (2005) Responses of grassland production to single and multiple global environmental changes. PLoS Biol 3:1829–1837. doi:10.1371/journal.pbio.0030319 CrossRefGoogle Scholar
  28. Garcia-Montiel DC, Melillo JM, Steudler PA, Neill C, Feigl BJ, Cerri CC (2002) Relationship between N2O and CO2 emissions from the Amazon Basin. Geophys Res Lett 29:1090. doi:10.1029/2002GL013830 CrossRefGoogle Scholar
  29. Gutknecht JL, Henry HA, Balser TC (2010) Inter-annual variation in soil extra-cellular enzyme activity in response to simulated global change and fire disturbance. Pedobiologia 53:283–293CrossRefGoogle Scholar
  30. Hagedorn F, Bucher JB, Tarjan D, Rusert P, Bucher-Wallin I (2000) Responses of N fluxes and pools to elevated atmospheric CO2 in model forest ecosystems with acidic and calcareous soils. Plant Soil 224:273–286. doi:10.1023/A:1004831401190 Google Scholar
  31. Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45. doi:10.1111/j.1747-0765.2007.00195.x CrossRefGoogle Scholar
  32. Henry HAL, Chiariello NR, Vitousek PM, Mooney HA, Field CB (2006) Interactive effects of fire, elevated carbon dioxide, nitrogen deposition, and precipitation on a California annual grassland. Ecosystems 9:1066–1075. doi:10.1007/s10021-005-0077-7 CrossRefGoogle Scholar
  33. Horz H, Barbrook A, Field CB, Bohannan BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci USA 101:15136–15141. doi:10.1073/pnas.0406616101 CrossRefGoogle Scholar
  34. Huang B, Chen G, Huang G, Hauro T (2003) Nitrous oxide emission from temperate meadow grassland and emission estimation for temperate grassland of China. Nutr Cycl Agroecosyst 67:31–36. doi:10.1023/A:1025131229285 CrossRefGoogle Scholar
  35. Hungate BA, Lund CP, Pearson HL, Chapin FS III (1997) Elevated CO2 and nutrient addition alter soil N cycling and N trace gas fluxes with early season wet-up in a California annual grassland. Biogeochemistry 37:89–109. doi:10.1023/A:1005747123463 CrossRefGoogle Scholar
  36. Hutchinson GL, Mosier AR (1981) Improved soil cover method for field measurement of nitrous-oxide fluxes. Soil Sci Soc Am J 45:311–316CrossRefGoogle Scholar
  37. Jamieson N, Monaghan R, Barraclough D (1999) Seasonal trends of gross N mineralization in a natural calcareous grassland. Glob Change Biol 5:423–431. doi:10.1046/j.1365-2486.1999.00232.x CrossRefGoogle Scholar
  38. Kaiser EA, Kohrs K, Kucke M, Schnug E, Heinemeyer O, Munch JC (1998) Nitrous oxide release from arable soil: Importance of N-fertilization, crops and temporal variation. Soil Biol Biochem 30:1553–1563. doi:10.1016/S0038-0717(98)00036-4 CrossRefGoogle Scholar
  39. Kammann C, Mueller C, Ludger G, Jaeger HJ (2008) Elevated CO2 stimulates N2O emissions in permanent grassland. Soil Biol Biochem 40:2194–2205. doi:10.1016/j.soilbio.2008.04.012 Google Scholar
  40. Kanerva T, Regina K, Ramo K, Ojanpera K, Manninen S (2007) Fluxes of N2O, CH4 and CO2 in a meadow ecosystem exposed to elevated ozone and carbon dioxide for three years. Environ Pollut 145:818–828. doi:10.1016/j.envpol.2006.03.055 Google Scholar
  41. Kettunen R, Saarnio S, Martikainen P, Silvola J (2005) Elevated CO2 concentration and nitrogen fertilisation effects on N2O and CH4 fluxes and biomass production of Phleum pratense on farmed peat soil. Soil Biol Biochem 37:739–750. doi:10.1016/j.soilbio.2004.09.010 Google Scholar
  42. Kettunen R, Saarnio S, Martikainen PJ, Silvola J (2007a) Can a mixed stand of N2-fixing and non-fixing plants restrict N2O emissions with increasing CO2 concentration? Soil Biol Biochem 39:2538–2546. doi:10.1016/j.soilbio.2007.04.023 Google Scholar
  43. Kettunen R, Saarnio S, Silvola J (2007b) N2O fluxes and CO2 exchange at different N doses under elevated CO2 concentration in boreal agricultural mineral soil under Phleum pratense. Nutr Cyc Agroecosyst 78:197–209. doi:10.1007/s10705-006-9085-z
  44. Larsen KS, Andresen LC, Beier C, Jonasson S, Albert KR, Ambus P, Arndal MF, Carter MS, Christensen S, Holmstrup M, Ibrom A, Kongstad J, Van Der Linden L, Maraldo K, Michelsen A, Mikkelsen TN, Pilegaard K, Priemé A, Ro-Poulsen H, Schmidt IK, Selsted MB, Stevnbak K (2011) Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Glob Change Biol 17:1884–1899. doi:10.1111/j.1365-2486.2010.02351.x CrossRefGoogle Scholar
  45. Laville P, Lehuger S, Loubet B, Chaumartin F, Cellier P (2011) Effect of management, climate and soil conditions of N2O and NO emissions from an arable crop rotation using high temporal resolution measurements. Agric For Meteorol 151:228–240. doi:10.1016/j.agrformet.2010.10.008 CrossRefGoogle Scholar
  46. Li CS, Frolking S, Frolking TA (1992) A model of nitrous-oxide evolution from soil driven by rainfall evens. 1. Model structure and sensitivity. J Geophys Res 97:9759–9776CrossRefGoogle Scholar
  47. Li CS, Narayanan V, Harriss RC (1996) Model estimates of nitrous oxide emissions from agricultural lands in the United States. Glob Biogeochem Cycles 10:297–306. doi:10.1029/96GB00470 CrossRefGoogle Scholar
  48. Liikanen A, Ratilainen E, Saarnio S, Alm J, Martikainen PJ, Silvola J (2003) Greenhouse gas dynamics in boreal, littoral sediments under raised CO2 and nitrogen supply. Freshw Biol 48:500–511. doi:10.1046/j.1365-2427.2003.01023.x Google Scholar
  49. Luo YQ, Gerten D, Le Maire G, Parton WJ, Weng ES, Zhou XH, Keough C, Beier C, Ciais P, Cramer W, Dukes JS, Emmett B, Hanson PJ, Knapp A, Linder S, Nepstad D, Rustad L (2008) Modeled interactive effects of precipitation, temperature and [CO2] on ecosystem carbon and water dynamics in different climatic zones. Glob Change Biol 14:1986–1999. doi:10.1111/j.1365-2486.2008.01629.x
  50. Malchair S, De Boeck HJ, Lemmens CM, Merckx R, Nijs I, Ceulemans R, Carnol M (2010) Do climate warming and plant species richness affect potential nitrification, basal respiration and ammonia-oxidizing bacteria in experimental grasslands? Soil Biol Biochem 42:1944–1951. doi:10.1016/j.soilbio.2010.07.006 CrossRefGoogle Scholar
  51. Marhan S, Philippot L, Bru D, Rudolph S, Franzaring J, Hogy P, Fangmeier A, Kandeler E (2011) Abundance and activity of nitrate reducers in an arable soil are more affected by temporal variation and soil depth than by elevated atmospheric CO2. FEMS Microbiol Ecol 76:209–219. doi:10.1111/j.1574-6941.2011.01048.x CrossRefGoogle Scholar
  52. Martin-Olmedo P, Rees RM, Grace J (2002) The influence of plants grown under elevated CO2 and N fertilization on soil nitrogen dynamics. Glob Change Biol 8:643–657. doi:10.1046/j.1365-2486.2002.00499.x
  53. Matson PA, Naylor R, Ortis-Monasterio I (1998) Integration of environmental, agronomic and economic aspects of fertilizer management. Science 280:112–115. doi:10.1126/science.280.5360.112 CrossRefGoogle Scholar
  54. Mosier AR (1994) Nitrous oxide emissions from agricultural soils. Fertil Res 37:191–200.doi:10.1007/BF00748937 CrossRefGoogle Scholar
  55. Mosier AR, Parton WJ, Valentine DW, Ojima DS, Schimel DS, Delgado JA (1996) CH4 and N2O fluxes in the Colorado shortgrass steppe.1. Impact of landscape and nitrogen addition. Glob Biogeochem Cycles 10:387–399. doi:10.1029/96GB01454 CrossRefGoogle Scholar
  56. Mosier AR, Morgan JA, King JY, LeCain D, Milchunas DG (2002) Soil–atmosphere exchange of CH4, CO2, NOx, and N2O in the Colorado shortgrass steppe under elevated CO2. Plant Soil 240:201–211CrossRefGoogle Scholar
  57. Mummey DL, Smith JL, Bolton H (1994) Nitrous-oxide flux from a shrub-steppe ecosystem—sources and regulation. Soil Biol Biochem 26:279–286. doi:10.1016/0038-0717(94)90168-6 CrossRefGoogle Scholar
  58. Niboyet A, Barthes L, Hungate BA, Le Roux X, Bloor JMG, Ambroise A, Fontaine S, Price PM, Leadley PW (2010) Responses of soil nitrogen cycling to the interactive effects of elevated CO2 and inorganic N supply. Plant Soil 327:35–47. doi:10.1007/s11104-009-0029-7 CrossRefGoogle Scholar
  59. Niboyet A, Le Roux X, Dijkstra P, Hungate BA, Barthes L, Blankinship JC, Brown JR, Field CB, Leadley PW (2011a) Testing interactive effects of global environmental changes on soil nitrogen cycling. Ecosphere 2:art56. doi:10.1890/ES10-00148.1
  60. Niboyet A, Brown JR, Dijkstra P, Blankinship JC, Leadley PW, LeRoux X, Barthes L, Barnard RL, Field CB, Hungate BA (2011b) Strong interactors: wildfire, global environmental change, and greenhouse gas emissions. PLoS ONE. doi:10.1371/journal.pone.0020105
  61. Reich PB, Hungate BA, Luo YQ (2006) Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Ann Rev Ecol Evol Syst 37:611–636. doi:10.1146/annurev.ecolsys.37.091305.110039 Google Scholar
  62. Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8:214–222. doi:10.1111/j.1462-2920.2005.00882.x CrossRefGoogle Scholar
  63. Smith KA, Thomson PE, Clayton H, McTaggart IP, Conen F (1998) Effects of temperature, water content and nitrogen fertilisation on emissions of nitrous oxide by soils. Atmos Environ 32:3301–3309. doi:10.1016/S1352-2310(97)00492-5 CrossRefGoogle Scholar
  64. Stehfest E, Bouwman L (2006) N2O and NO emission from agricultural fields and soils under natural vegetation: summarizing available measurement data and modeling of global annual emissions. Nutr Cycl Agroecosyst 74:207–228. doi:10.1007/s10705-006-9000-7 CrossRefGoogle Scholar
  65. Szukics U, Abell GCJ, Hödl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72:395–406. doi:10.1111/j.1574-6941.2010.00853.x CrossRefGoogle Scholar
  66. Tian H, Xu X, Liu M, Ren W, Zhang C, Chen G, Lu C (2010) Spatial and temporal patterns of CH4 and N2O fluxes in terrestrial ecosystems of North America during 1979–2008: application of a global biogeochemistry model. Biogeosciences 7:2673–2694. doi:10.5194/bg-7-2673-2010 CrossRefGoogle Scholar
  67. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Environmental microbiology of anaerobes. Wiley, New York, pp 179–244Google Scholar
  68. Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD (2011) A framework for representing microbial decomposition in coupled climate models. Biogeochemistry. doi:10.1007/s10533-011-9635-6
  69. Treseder KK, Balser TC, Bradford MA, Brodie EL, Dubinsky EA, Eviner VT, Hofmockel KS, Lennon JT, Levine UY, MacGregor BJ, Pett-Ridge J, Waldrop MP (2011) Integrating microbial ecology into ecosystem models: challenges and priorities. Biogeochemistry. doi:10.1007/s10533-011-9636-5
  70. Tscherko D, Kandeler E, Jones TH (2001) Effect of temperature on below-ground N-dynamics in a weedy model ecosystem at ambient and elevated atmospheric CO2 levels. Soil Biol Biochem 33:491–501. doi:10.1016/S0038-0717(00)00190-5 CrossRefGoogle Scholar
  71. Van Groenigen JW, Velthof G, Oenema O, Van Groenigen KJ, Van Kessel C (2010) Towards an agronomic assessment of N2O emissions: a case study for arable crops. Eur J Soil Sci 61:903–913. doi:10.1111/j.1365-2389.2009.01217.x CrossRefGoogle Scholar
  72. Van Groenigen KJ, Osenberg CW, Hungate BA (2011) Increased soil emissions of potent greenhouse gases under elevated CO2. Nature 475:214–216. doi:10.1038/nature10176 CrossRefGoogle Scholar
  73. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152. doi:10.1890/1051-0761(2006)016[2143:ECODCA]2.0.CO;2 CrossRefGoogle Scholar
  74. Weier KL, Doran JW, Power JF, Walters DT (1993) Denitrification and the N2:N2O ratio as affected by soil water, available carbon and nitrate. Soil Sci Soc Am J 57:66–72CrossRefGoogle Scholar
  75. Welzmiller JT, Matthias AD, White S, Thompson TL (2008) Elevated carbon dioxide and irrigation effects on soil nitrogen gas exchange in irrigated sorghum. Soil Sci Soc Am J 72: 393–401. doi:10.2136/sssaj2007.0033 Google Scholar
  76. Wootton JT (1994) Putting the pieces together: testing the independence of interactions among organisms. Ecology 75:1544–1551. doi:10.2307/1939615 CrossRefGoogle Scholar
  77. Wrage N, Velthof GL (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732. doi:10.1016/S0038-0717(01)00096-7 CrossRefGoogle Scholar
  78. Wrage N, Velthol GL, Laanbroek HJ, Oenema O (2004) Nitrous oxide production in grassland soils: assessing the contribution of nitrifier denitrification. Soil Biol Biochem 36:229–236. doi:10.1016/j.soilbio.2003.09.009 CrossRefGoogle Scholar
  79. Xu X, Tian H, Hui D (2008) Convergence in the relationship of CO2 and N2O exchanges between soil and atmosphere within terrestrial ecosystems. Glob Change Biol 14:1651–1660. doi:10.1111/j.1365-2486.2008.01595.x CrossRefGoogle Scholar
  80. Zavaleta ES, Shaw MR, Chiariello NR, Thomas BD, Cleland EE, Field CB, Mooney HA (2003a) Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecol Monogr 73:585–604. doi:10.1890/02-4053 CrossRefGoogle Scholar
  81. Zavaleta ES, Shaw MR, Chiariello NR, Mooney HA, Field CB (2003b) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc Natl Acad Sci USA 100:7650–7654. doi:10.1073/pnas.0932734100 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jamie R. Brown
    • 1
  • Joseph C. Blankinship
    • 1
    • 2
  • Audrey Niboyet
    • 3
    • 4
  • Kees Jan van Groenigen
    • 1
  • Paul Dijkstra
    • 1
  • Xavier Le Roux
    • 5
  • Paul W. Leadley
    • 6
  • Bruce A. Hungate
    • 1
  1. 1.Department of Biological Sciences and Merriam-Powell Center for Environmental ResearchNorthern Arizona UniversityFlagstaffUSA
  2. 2.School of Natural Sciences and Sierra Nevada Research InstituteUniversity of CaliforniaMercedUSA
  3. 3.Laboratoire Ecologie, Systématique et EvolutionUMR 8079 Université Paris-Sud 11/CNRS/AgroParisTechOrsayFrance
  4. 4.Laboratoire Biogéochimie et Ecologie des Milieux Continentaux, AgroParisTechUMR 7618 Université Pierre et Marie Curie/CNRS/AgroParisTechThiverval GrignonFrance
  5. 5.Laboratoire d’Ecologie MicrobienneUniversité de LyonVilleurbanneFrance
  6. 6.Laboratoire Ecologie, Systématique et EvolutionUniversité Paris-Sud, UMR 8079 Université Paris-Sud/CNRS/AgroParisTechOrsayFrance

Personalised recommendations