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.

  • Article
  • Published:

Grassland productivity limited by multiple nutrients

Abstract

Terrestrial ecosystem productivity is widely accepted to be nutrient limited1. Although nitrogen (N) is deemed a key determinant of aboveground net primary production (ANPP)2,3, the prevalence of co-limitation by N and phosphorus (P) is increasingly recognized48. However, the extent to which terrestrial productivity is co-limited by nutrients other than N and P has remained unclear. Here, we report results from a standardized factorial nutrient addition experiment, in which we added N, P and potassium (K) combined with a selection of micronutrients (K+μ), alone or in concert, to 42 grassland sites spanning five continents, and monitored ANPP. Nutrient availability limited productivity at 31 of the 42 grassland sites. And pairwise combinations of N, P, and K+μ co-limited ANPP at 29 of the sites. Nitrogen limitation peaked in cool, high latitude sites. Our findings highlight the importance of less studied nutrients, such as K and micronutrients, for grassland productivity, and point to significant variations in the type and degree of nutrient limitation. We suggest that multiple-nutrient constraints must be considered when assessing the ecosystem-scale consequences of nutrient enrichment.

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: Nutrient limitation of ANPP (LRRs, ln(treatment/control)) by N, P and K plus year 1 micronutrients (K+μ).
Figure 2: Correlations of nutrient limitation of ANPP (LRRs, ln(treatment/control)) among single and paired nutrients.
Figure 3: Predictors of N limitation of ANPP (LRRs, ln(treatment/control)).
Figure 4: ANPP responses to factorial N, P and K plus year 1 micronutrient (K+μ) treatments by year in 37 grasslands with three continuous years of ANPP data.

Similar content being viewed by others

References

  1. Chapin, F. S., Matson, P. A. & Vitousek, P. M. Principles of Terrestrial Ecosystem Ecology. 2nd edn (Springer, New York, 2011).

    Book  Google Scholar 

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

    Article  Google Scholar 

  3. LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).

    Article  Google Scholar 

  4. Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).

    Article  Google Scholar 

  5. Harpole, W. S. et al. Nutrient co-limitation of primary producer communities. Ecol. Lett. 14, 852–862 (2011).

    Article  Google Scholar 

  6. Bracken, M. E. S. et al. Signatures of nutrient limitation and co-limitation: responses of autotroph internal nutrient concentrations to nitrogen and phosphorus additions. Oikos 124, 113–121 (2015).

    Article  CAS  Google Scholar 

  7. Ågren, G. I., Wetterstedt, J. Å. & Billberger, M. F. K. Nutrient limitation on terrestrial plant growth – modeling the interaction between nitrogen and phosphorus. New Phytol. 194, 953–960 (2012).

    Article  Google Scholar 

  8. Carnicer, J. et al. Global biodiversity, stoichiometry and ecosystem function responses to human-induced C-N-P imbalances. J. Plant Physiol. 172, 82–91 (2015).

    Article  CAS  Google Scholar 

  9. Fisher, J. B., Badgley, G. & Blyth, E. Global nutrient limitation in terrestrial vegetation. Glob. Biogeochem. Cycles 26, GB3007 (2012).

    Article  Google Scholar 

  10. Hooper, D. U. & Johnson, L. C. Nitrogen limitation in dryland ecosystems: Responses to geographical and temporal variation in precipitation. Biogeochemistry 46, 247–293 (1999).

    CAS  Google Scholar 

  11. Hoekstra, J. M., Boucher, T. M., Ricketts, T. H. & Roberts, C. Confronting a biome crisis: global disparities of habitat loss and protection. Ecol. Lett. 8, 23–29 (2005).

    Article  Google Scholar 

  12. Galloway, J. N. et al. The nitrogen cascade. BioScience 53, 341–356 (2003).

    Article  Google Scholar 

  13. Rockstrom, J. et al. A safe operating space for humanity. Nature 461, 472–475 (2009).

    Article  Google Scholar 

  14. 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  Google Scholar 

  15. Fenn, M. E. et al. Ecological effects of nitrogen deposition in the Western United States. BioScience 53, 404–420 (2003).

    Article  Google Scholar 

  16. Mahowald, N. et al. Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob. Biogeochem. Cycles 22, GB4026 (2008).

    Article  Google Scholar 

  17. Phoenix, G. K. et al. Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Glob. Change Biol. 18, 1197–1215 (2012).

    Article  Google Scholar 

  18. Øgaard, A. F., Krogstad, T. & Løes, A. K. Potassium uptake by grass from a clay and a silt soil in relation to soil tests. Acta Agr. Scand. B-S P 51, 97–105 (2001).

    Google Scholar 

  19. Veresoglou, D. S. & Fitter, A. H. Spatial and temporal patterns of growth and nutrient uptake of five co-existing grasses. J. Ecol. 72, 259–272 (1984).

    Article  CAS  Google Scholar 

  20. Kayser, M. & Isselstein, J. Potassium cycling and losses in grassland systems: a review. Grass Forage Sci. 60, 213–224 (2005).

    Article  CAS  Google Scholar 

  21. Borer, E. T. et al. Finding generality in ecology: a model for globally distributed experiments. Methods Ecol. Evol. 5, 65–73 (2014).

    Article  Google Scholar 

  22. Guevara, J. C., Stasi, C. R., Estevez, O. R. & Le Houerou, H. N. N and P fertilization on rangeland production in Midwest Argentina. J. Range Manage. 53, 410–414 (2000).

    Article  Google Scholar 

  23. Clark, C. M. & Tilman, D. Recovery of plant diversity following N cessation: effects of recruitment, litter, and elevated N cycling. Ecology 91, 3620–3630 (2010).

    Article  Google Scholar 

  24. Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).

    Article  Google Scholar 

  25. Olff, H. & Pegtel, D. Characterisation of the type and extent of nutrient limitation in grassland vegetation using a bioassay with intact sods. Plant Soil 163, 217–224 (1994).

    Article  CAS  Google Scholar 

  26. Walker, T. W. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).

    Article  CAS  Google Scholar 

  27. Laliberte, E. et al. Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J. Ecol. 100, 631–642 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Jones, L. et al. A review and application of the evidence for nitrogen impacts on ecosystem services. Ecosystem Services 7, 76–88 (2014).

    Article  Google Scholar 

  30. Hijmans, R. J. et al. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Minnesota Supercomputer Institute for hosting project data, the University of Minnesota Institute on the Environment for hosting Nutrient Network meetings, and each site investigator for funding their site-level operations. Network coordination and data management were supported by funds from the National Science Foundation Research Coordination Network (NSF-DEB-1042132) to E.T.B. and E.W.S., from the Long Term Ecological Research program (NSF-DEB-1234162) to the Cedar Creek LTER, and from the Institute on the Environment (DG-0001-13). P.A.F. acknowledges USDA-NIFA (2010-65615-20632). USDA is an equal opportunity employer and provider.

Author information

Authors and Affiliations

Authors

Contributions

P.A.F. wrote the manuscript, drafted the figures, and led the data analysis; E.M.L. developed the database; S.M.P. and W.S.H. contributed to data analysis; S.M.P., W.S.H., J.M.H.K., J.D.B., E.T.B., A.S.M., E.W.S. and P.D.W. contributed conceptual development and data interpretation. All co-authors contributed data and manuscript editing. This work was generated using data from the Nutrient Network (http://www.nutnet.org) experiment.

Corresponding author

Correspondence to Philip A. Fay.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fay, P., Prober, S., Harpole, W. et al. Grassland productivity limited by multiple nutrients. Nature Plants 1, 15080 (2015). https://doi.org/10.1038/nplants.2015.80

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.80

This article is cited by

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