Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands

Abstract

Rates of atmospheric deposition of biologically active nitrogen (N) are two to seven times the pre-industrial rates in many developed nations because of combustion of fossil fuels and agricultural fertilization1,2. They are expected to increase similarly over the next 50 years in industrializing nations of Asia and South America2. Although the environmental impacts of high rates of nitrogen addition have been well studied3,4,5,6,7,8, this is not so for the lower, chronic rates that characterize much of the globe. Here we present results of the first multi-decadal experiment to examine the impacts of chronic, experimental nitrogen addition as low as 10 kg N ha-1 yr-1 above ambient atmospheric nitrogen deposition (6 kg N ha-1 yr-1 at our site). This total input rate is comparable to terrestrial nitrogen deposition in many industrialized nations2. We found that this chronic low-level nitrogen addition rate reduced plant species numbers by 17% relative to controls receiving ambient N deposition. Moreover, species numbers were reduced more per unit of added nitrogen at lower addition rates, suggesting that chronic but low-level nitrogen deposition may have a greater impact on diversity than previously thought. A second experiment showed that a decade after cessation of nitrogen addition, relative plant species number, although not species abundances, had recovered, demonstrating that some effects of nitrogen addition are reversible.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Proportional species loss versus nitrogen input rate for (a) 2002–2004 and (b) 1983–1985.
Figure 2: Relative species number versus time.
Figure 3: Losses of rare versus dominant species.
Figure 4: Recovery of relative species number after cessation of nitrogen addition.

Similar content being viewed by others

References

  1. Vitousek, P. M. et al. Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7, 737–750 (1997)

    Google Scholar 

  2. Galloway, J. N. et al. Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153–226 (2004)

    Article  CAS  Google Scholar 

  3. Bobbink, R. Effects of nutrient enrichment in Dutch chalk grassland. J. Appl. Ecol. 28, 28–41 (1991)

    Article  Google Scholar 

  4. Mountford, J. O., Lakhani, K. H. & Kirkham, F. W. Experimental assessment of the effects of nitrogen addition under hay-cutting and aftermath grazing on the vegetation of meadows on a Somerset peat moor. J. Appl. Ecol. 30, 321–332 (1993)

    Article  Google Scholar 

  5. Wedin, D. A. & Tilman, D. Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274, 1720–1723 (1996)

    Article  CAS  ADS  Google Scholar 

  6. Bobbink, R., Hornung, M. & Roelofs, J. G. M. The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J. Ecol. 86, 717–738 (1998)

    Article  CAS  Google Scholar 

  7. Gough, L., Osenberg, C. W., Gross, K. L. & Collins, S. L. Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89, 428–439 (2000)

    Article  Google Scholar 

  8. Suding, K. N. et al. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc. Natl Acad. Sci. USA 102, 4387–4392 (2005)

    Article  CAS  ADS  Google Scholar 

  9. Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea – how can it occur? Biogeochemistry 13, 87–115 (1991)

    Article  Google Scholar 

  10. Aerts, R. & Chapin, F. S. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv. Ecol. Res 30, 1–67 (2000)

    CAS  Google Scholar 

  11. Bakker, J. P. & Berendse, F. Constraints in the restoration of ecological diversity in grassland and heathland communities. Trends Ecol. Evol. 14, 63–68 (1999)

    Article  CAS  Google Scholar 

  12. Stevens, C. J., Dise, N. B., Mountford, J. O. & Gowing, D. J. Impact of nitrogen deposition on the species richness of grasslands. Science 303, 1876–1879 (2004)

    Article  CAS  ADS  Google Scholar 

  13. van den Berg, L. J. L., Tomassen, H. B. M., Roelofs, J. G. M. & Bobbink, R. Effects of nitrogen enrichment on coastal dune grassland: A mesocosm study. Environ. Pollut. 138, 77–85 (2005)

    Article  CAS  Google Scholar 

  14. Williams, M. W. & Tonnessen, K. A. Critical loads for inorganic nitrogen deposition in the Colorado Front Range, USA. Ecol. Appl. 10, 1648–1665 (2000)

    Article  Google Scholar 

  15. Bouwman, A. F., Van Vuuren, D. P., Derwent, R. G. & Posch, M. A global analysis of acidification and eutrophication of terrestrial ecosystems. Wat. Air Soil Pollut. 141, 349–382 (2002)

    Article  CAS  ADS  Google Scholar 

  16. Nilsson, J. & Grennfelt, P. E. Critical loads for sulfur and nitrogen. Report from a workshop held at Stokhoster, Sweden, 19–24 March 1988. Miljo Rapport 1988: 15 (Nordic Council of Ministers, Copenhagen, 1988)

  17. Smart, S. M. et al. Large-scale changes in the abundance of common higher plant species across Britain between 1978, 1990 and 1998 as a consequence of human activity: tests of hypothesised changes in trait representation. Biol. Conserv. 124, 355–371 (2005)

    Article  Google Scholar 

  18. Mountford, J. O., Lakhani, K. H. & Holland, R. J. Reversion of grassland vegetation following the cessation of fertilizer application. J. Veg. Sci. 7, 219–228 (1996)

    Article  Google Scholar 

  19. Strengbom, J., Nordin, A., Nasholm, T. & Ericson, L. Slow recovery of boreal forest ecosystem following decreased nitrogen input. Funct. Ecol. 15, 451–457 (2001)

    Article  Google Scholar 

  20. Milchunas, D. G. & Lauenroth, W. K. Inertia in plant community structure – state changes after cessation of nutrient-enrichment stress. Ecol. Appl. 5, 452–458 (1995)

    Article  Google Scholar 

  21. Boxman, A. W., van der Ven, P. J. M. & Roelefs, J. G. M. Ecosystem recovery after a decrease in nitrogen input to a Scots pine stand at Ysselsteyn, the Netherlands. For. Ecol. Mgmt 101, 155–163 (1998)

    Article  Google Scholar 

  22. Tilman, D. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol. Monogr. 57, 189–214 (1987)

    Article  Google Scholar 

  23. Inouye, R. & Tilman, D. Convergence and divergence of old-field vegetation after 11 yr of nitrogen addition. Ecology 76, 1872–1887 (1995)

    Article  Google Scholar 

  24. Tilman, D. & El Haddi, A. Drought and biodiversity in grasslands. Oecologia 89, 257–264 (1992)

    Article  CAS  ADS  Google Scholar 

  25. Bobbink, R., Ashmore, M., Braun, S., Flückiger, W. & Van den Wyngaert, I. J. J. in Manual on Methodologies and Criteria for Mapping Critical Levels/Loads and Geographic Areas Where They Are Exceeded (eds Achermann, B. & Bobbink, R.) 40–170 (United Nations, Economic Commission for Europe Convention on Long-range Transboundary Air Pollution, Federal Environmental Agency (Umweltbundesamt), Berlin, 2002)

    Google Scholar 

  26. Power, S. A., Green, E. R., Barker, C. G., Bell, J. N. B. & Ashmore, M. R. Ecosystem recovery: heathland response to a reduction in nitrogen deposition. Glob. Change Biol. 12, 1241–1252 (2006)

    Article  ADS  Google Scholar 

  27. Roem, W. J., Klees, H. & Berendse, F. Effects of nutrient addition and acidification on plant species diversity and seed germination in heathland. J. Appl. Ecol. 39, 937–948 (2002)

    Article  CAS  Google Scholar 

  28. Tilman, D. Species richness of experimental productivity gradients: how important is colonization limitation. Ecology 74, 2179–2191 (1993)

    Article  Google Scholar 

Download references

Acknowledgements

We thank C. Stevens, J. Galloway, S. Collins, K. Suding, J. Hille Ris Lambers, and J. Fargione for their comments on the manuscript, and T. Mielke and the summer interns at Cedar Creek for their work. This project was supported by the Long-Term Ecological Research Network funded by the National Science Foundation.

Author Contributions D.T. envisioned, set up and managed the long-term experiment. C.C. performed the analysis and wrote much of the paper. Both authors discussed the results, and developed and commented on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher M. Clark.

Supplementary information

Supplementary Information

This file provides additional detail on the statistical analyses and results that support the main text, and includes Supplementary Notes, Supplementary Tables 1-3 and Supplementary Figure 1 with Legends. (PDF 172 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clark, C., Tilman, D. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451, 712–715 (2008). https://doi.org/10.1038/nature06503

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06503

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing