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 recognized4,​5,​6,​7,​8. 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.

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  1. 1.

    , & Principles of Terrestrial Ecosystem Ecology. 2nd edn (Springer, New York, 2011).

  2. 2.

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

  3. 3.

    & Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).

  4. 4.

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

  5. 5.

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

  6. 6.

    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).

  7. 7.

    , & Nutrient limitation on terrestrial plant growth – modeling the interaction between nitrogen and phosphorus. New Phytol. 194, 953–960 (2012).

  8. 8.

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

  9. 9.

    , & Global nutrient limitation in terrestrial vegetation. Glob. Biogeochem. Cycles 26, GB3007 (2012).

  10. 10.

    & Nitrogen limitation in dryland ecosystems: Responses to geographical and temporal variation in precipitation. Biogeochemistry 46, 247–293 (1999).

  11. 11.

    , , & Confronting a biome crisis: global disparities of habitat loss and protection. Ecol. Lett. 8, 23–29 (2005).

  12. 12.

    et al. The nitrogen cascade. BioScience 53, 341–356 (2003).

  13. 13.

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

  14. 14.

    , , & Impact of nitrogen deposition on the species richness of grasslands. Science 303, 1876–1879 (2004).

  15. 15.

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

  16. 16.

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

  17. 17.

    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).

  18. 18.

    , & 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).

  19. 19.

    & Spatial and temporal patterns of growth and nutrient uptake of five co-existing grasses. J. Ecol. 72, 259–272 (1984).

  20. 20.

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

  21. 21.

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

  22. 22.

    , , & N and P fertilization on rangeland production in Midwest Argentina. J. Range Manage. 53, 410–414 (2000).

  23. 23.

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

  24. 24.

    , & The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).

  25. 25.

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

  26. 26.

    & The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).

  27. 27.

    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).

  28. 28.

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

  29. 29.

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

  30. 30.

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

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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


  1. USDA-ARS Grassland Soil and Water Research Lab, Temple, Texas 76502, USA

    • Philip A. Fay
  2. CSIRO Land and Water Flagship, Private Bag 5, Wembley, Western Australia 6913, Australia

    • Suzanne M. Prober
  3. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa 50011, USA

    • W. Stanley Harpole
  4. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, Leipzig D-04103, Germany

    • W. Stanley Harpole
  5. Department of Physiological Diversity, Helmholtz Center for Environmental Research – UFZ, Permoserstr. 15, Leipzig 04318, Germany

    • W. Stanley Harpole
  6. Institute of Biology, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, Halle (Saale) 06108, Germany

    • W. Stanley Harpole
  7. School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588, USA

    • Johannes M. H. Knops
  8. School of Environmental and Forest Sciences, University of Washington, Seattle, Washington 98195, USA

    • Jonathan D. Bakker
  9. Department of Ecology, Evolution, and Behavior, University of MN, St. Paul, Minnesota 55108, USA

    • Elizabeth T. Borer
    • , Eric M. Lind
    • , Eric W. Seabloom
    •  & Peter D. Wragg
  10. Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada

    • Andrew S. MacDougall
  11. Department of Wildland Resources and the Ecology Center, Utah State University, Logan, Utah 84322, USA

    • Peter B. Adler
  12. USDA-ARS Rangeland Resources Research Unit, Fort Collins, Colorado 80526, USA

    • Dana M. Blumenthal
  13. School of Natural Sciences, Zoology, Trinity Centre for Biodiversity Research, Trinity College Dublin, Dublin 2, Ireland

    • Yvonne M. Buckley
  14. Research Station of Alpine Meadow and Wetland Ecosystems, Lanzhou University, Lanzhou 730000, China

    • Chengjin Chu
    •  & Guozhen Du
  15. Ecology, Behavior & Evolution Section, University of California, La Jolla, San Diego, California 92093, USA

    • Elsa E. Cleland
  16. Department of Biology, MSC03-2020, University of New Mexico, Albuquerque, New Mexico 88003, USA

    • Scott L. Collins
    •  & Laura M. Ladwig
  17. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309, USA

    • Kendi F. Davies
    •  & Brett A. Melbourne
  18. Department of Plant Biology, University of Illinois, Urbana, Illinois 61801, USA

    • Xiaohui Feng
  19. School of Earth, Environment and Biological Sciences, Queensland University of Technology, Brisbane, Queensland 4001, Australia

    • Jennifer Firn
  20. Department of Entomology, University of Maryland, College Park, Maryland 20742, USA

    • Daniel S. Gruner
  21. School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg 3209, South Africa

    • Nicole Hagenah
    •  & Kevin P. Kirkman
  22. Ecology and Biodiversity Group, Department of Biology, Utrecht University, Padualaan 8, Utrecht, CH 3584, Netherlands

    • Yann Hautier
  23. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA

    • Robert W. Heckman
    •  & Charles E. Mitchell
  24. USDA-ARS Agroecosystem Management Research Unit, Lincoln, Nebraska 68538, USA

    • Virginia L. Jin
  25. Department of Forest, Rangeland, and Watershed Stewardship, Colorado State University, Fort Collins, Colorado 80523, USA

    • Julia Klein
  26. Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, China

    • Qi Li
  27. Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546, USA

    • Rebecca L. McCulley
  28. School of Biological Sciences, Monash University, Victoria 3800, Australia

    • Joslin L. Moore
  29. Department of Botany, La Trobe University, Bundoora 3083, Victoria, Australia

    • John W. Morgan
  30. Swiss Federal Institute for Forest, Snow and Landscape Research, Community Ecology, Birmensdorf 8903, Switzerland

    • Anita C. Risch
    •  & Martin Schütz
  31. Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK

    • Carly J. Stevens
  32. School of Natural Resources, University of Nebraska, Lincoln, Nebraska 68583, USA

    • David A. Wedin
  33. Department of Entomology and Nematology, University of California, Davis, California 95616, USA

    • Louie H. Yang


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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Philip A. Fay.

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