Nitrous oxide emissions decrease with plant diversity but increase with grassland primary productivity

  • 327 Accesses


Nitrous oxide (N2O), a main greenhouse gas that contributes to ozone layer depletion, is released from soils. Even when it has been argued that agriculture is the main cause of its increase in the atmosphere, natural ecosystems are also an important source of N2O. However, the impacts of human activities on N2O emissions through biodiversity loss or primary productivity changes in natural ecosystems have rarely been assessed. Here, we analyzed the effects of vegetation attributes such as plant diversity and production, as drivers of N2O emission rates, in addition to environmental factors. We measured N2O emissions monthly during 1 year in 12 sites covering a large portion of the Rio de la Plata grasslands, Argentina, and related these emissions with climate, soil and vegetation attributes. We performed spatial and temporal models of N2O emissions separately, to evaluate which drivers control N2O in space and over time independently. Our results showed that in the spatial model, N2O emissions decreased with increments in plant species richness, with concomitant reductions in soil \({\text{NO}}_{3}^{ - } ,\) whereas N2O emissions increased with primary productivity. By contrast, in the temporal model, monthly precipitation and monthly temperature were the main drivers of N2O emissions, with positive correlations, showing important differences with the spatial model. Overall, our results show that biological drivers may exert substantial control of N2O emissions at large spatial scales, together with climate and soil variables. Our results suggest that biodiversity conservation of natural grasslands may reduce regional greenhouse gas emissions, besides maintaining other important ecosystem services.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. Abalos D, De Deyn GB, Kuyper TW, van Groenigen JW (2014) Plant species identity surpasses species richness as a key driver of N2O emissions from grassland. Glob Change Biol 20:265–275.

  2. Abalos D, van Groenigen JW, De Deyn GB (2017) What plant functional traits can reduce nitrous oxide emissions from intensively managed grasslands? Glob Change Biol 38:42–49.

  3. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156.

  4. Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. Accessed 27 May 2019

  5. Blake GR, Hartge H (1986) Bulk density. In: Klute A (ed) Methods of soil analysis, 2nd edn. ASA, Madison, pp 363–375

  6. Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54:464–465.

  7. Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorus in soils. Soil Sci 59:39–45

  8. Brentrup F, Kiisters J, Lammel J, Kuhlmann H (2000) Methods to estimate on-field nitrogen emissions from crop production as an input to LCA studies in the agricultural sector. Int J Life Cycle Assess 5:349–357.

  9. Burkart SE, León RJC, Conde MC, Perelman SB (2011) Plant species diversity in remnant grasslands on arable soils in the cropping Pampa. Plant Ecol 212:1009–1024.

  10. Butterbach-Bahl K, Baggs EM, Dannenmann M et al (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans R Soc Lond B Biol Sci 368:20130122.

  11. Chapin FS, Matson PA, Vitousek PM, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New York, p 436

  12. Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

  13. Cosentino VNR, Fernandez PL, Figueiro Aureggi SA, Taboada MA (2012) N2O emissions from a cultivated mollisol: optimal time of day for sampling and the role of soil temperature. Rev Bras Ciencia do Solo 36:1814–1819.

  14. Davidson EA, Keller M, Erickson HE et al (2000) Testing a Conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50:667–680.;2

  15. De Klein CAM, Harvey M (2015) Nitrous oxide chamber methodology guidelines. In: de Klein CAM, Harvey M (eds) Version 1.1. Ministry for Primary Industries, New zealand, pp 1–148 (ISBN 978-0-478-40585-9)

  16. Díaz S, Demissew S, Carabias J et al (2015) The IPBES conceptual framework—connecting nature and people. Curr Opin Environ Sustain 14:1–16.

  17. Erisman JW, Galloway JN, Seitzinger S et al (2013) Consequences of human modification of the global nitrogen cycle. Philos Trans R Soc B Biol Sci.

  18. Firestone M, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the Atmosphere. Wiley, Hoboken, pp 7–21

  19. Flombaum P, Sala OE (2008) Higher effect of plant species diversity on productivity in natural than artificial ecosystems. Proc Natl Acad Sci USA 105:6087–6090.

  20. Groffman PM, Turner CL (1995) Plant productivity and nitrogen gas fluxes in a tallgrass prairie landscape. Landsc Ecol 10:255–266

  21. Groffman PM, Brumme R, Butterbach-Bahl K et al (2000) Evaluating annual nitrous oxide fluxes at the ecosystem scale. Glob Biogeochem Cycles 14:1061–1070.

  22. Groffman PM, Butterbach-Bahl K, Fulweiler RW et al (2009) Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93:49–77.

  23. Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978.

  24. IPCC (2014) Climate Change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Page Core Writing Team, RK Pachauri and LA Meyer, p 151

  25. Keeney DR, Nelson D (1982) Nitrogen-Inorganic forms. In: Page AL (ed) Methods of Soil Analysis Part2 Chemical and Microbiological Properties. American Society of Agronomy, 2nd edn. Soil Science Society of American Publisher, Madison, pp 643–693

  26. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-33. Accessed 27 May 2019

  27. Lauenroth WK, Sala OE (1992) Long-term forage production of North American shortgrass steppe. Ecol Appl 2:397–403.

  28. Lee DS, Bouwman AF, Asman WAH, Dentener FJ, van der Hoek KW, Olivier JGJ (1997) Emissions of nitric oxide, nitrous oxide and ammonia from grasslands on a global scale. In: Jarvis SC, Pains BF (eds) Gaseous nitrogen emissions from grasslands. CAB International, Wallingford, pp 353–371

  29. Linn DM, Doran JW (1984) Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci Soc Am J 48:1267–1272

  30. Niklaus PA, Wardle DA, Tate KR (2006) Effects of plant species diversity and composition on nitrogen cycling and the trace gas balance of soils. Plant Soil 282:83–98.

  31. Niklaus PA, Le Roux X, Poly F et al (2016) Plant species diversity affects soil atmosphere fluxes of methane and nitrous oxide. Oecologia 181:919–930.

  32. Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R package version 2.4-3. Accessed 27 May 2019

  33. Parkin TB, Venterea RT (2010) Chamber-based trace gas flux measurements. USDA-ARS GRACEnet Project Protocols 2010:1–39

  34. Paruelo JM, Epstein HE, Lauenroth WK, Burke IC (1997) ANPP estimates from NDVI for the Central grassland region of the United States. Ecology 78:953.

  35. Perelman SB, Leon RJC, Oesterheld M (2001) Cross-scale vegetation patterns of flooding Pampa grasslands. J Ecol 89:562–577.

  36. Piñeiro G, Paruelo JM, Oesterheld M (2006) Potential long-term impacts of livestock introduction on carbon and nitrogen cycling in grasslands of Southern South America. Glob Chang Biol 12:1267–1284.

  37. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 27 May 2019

  38. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125.

  39. Robertson GP (1989) Nitrification and denitrification in humid tropical ecosystems: potential controls on nitrogen retention. Miner Nutr Trop For Savanna Ecosyst 9:55–69

  40. Robertson GP, Coleman DC, Bledsoe CS, Sollins P (1999) Standard soil methods for long-term ecological research. Oxford University Press, Oxford

  41. Saggar S, Jha N, Deslippe J et al (2013) Denitrification and N2O:N2 production in temperate grasslands: processes, measurements, modelling and mitigating negative impacts. Sci Total Environ 465:173–195.

  42. Sala OE (2001) Productivity of temperate grasslands. In: Roy J, Saugier B, Mooney HA (eds) Terrestrial global productivity. Academic Press, San Diego, pp 285–300

  43. Sala OE, Chapin FS, Armesto JJ et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774.

  44. Sala OE, Gherardi LA, Reichmann L et al (2012) Legacies of precipitation fluctuations on primary production: theory and data synthesis. Philos Trans R Soc B Biol Sci 367:3135–3144.

  45. Scherer-Lorenzen AM, Palmborg C, Prinz A (2013) The role of plant diversity and composition for nitrate leaching in grasslands. Ecology 84:1539–1552.;2

  46. Smith KA (2017) Changing views of nitrous oxide emissions from agricultural soil: key controlling processes and assessment at different spatial scales. Eur J Soil Sci 12:1–19.

  47. Soriano A (1991) Rio de la plata grasslands. In: Coupland RT (ed) Ecosystems of the world. Elsevier, Amsterdam, pp 367–407

  48. Summer ME, Miller WP (1996) Cation exchange capacity and exchange coefficients. In: Page AI, Miller RH, Keeney DR (eds) Methods of soil analysis. Chemical and microbiological methods. American Society of Agronomy, Madison, pp 1201–1229

  49. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720.

  50. Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–493.

  51. Wolf K, Veldkamp E, Homeier J, Martinson GO (2011) Nitrogen availability links forest productivity, soil nitrous oxide and nitric oxide fluxes of a tropical montane forest in southern Ecuador. Glob Biogeochem Cycles.

  52. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York

Download references


We thank people that collaborated in field sampling as well as the Della Chiesa family and staff at Estancia San Claudio for logistic support. We thank the Laboratorio de Servicios Analíticos Especiales and its staff (Veronica Feuring and Alina Crelier) for analyzing gas samples.


This work was funded by Secretaría de Agricultura, Ganadería y Pesca del Ministerio de Agricultura, Ganadería y Pesca, Agencia Nacional de Promoción Científica y Tecnológica (PICT 2014-3026 and 2015-2827), Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 112-2015- 0100709) and the Inter-American Institute for Global Change Research (CRN 3005) which is supported by the US National Science Foundation (Grant GEO-1128040).

Author information

JMPG, LY, TDC and GP conceived the ideas and designed the methodology, JMPG and TDC collected and analyzed the data. JMPG led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Correspondence to Juan Manuel Piñeiro-Guerra.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Carly Stevens.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Piñeiro-Guerra, J.M., Yahdjian, L., Della Chiesa, T. et al. Nitrous oxide emissions decrease with plant diversity but increase with grassland primary productivity. Oecologia 190, 497–507 (2019) doi:10.1007/s00442-019-04424-x

Download citation


  • Ecosystem services
  • Greenhouse gases
  • Climate change
  • Biodiversity–ecosystem function relationship
  • Spatial and temporal drivers