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:

Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle

Nature Plants volume 1, Article number: 15182 (2015) Cite this article

Subjects

Abstract

Dinitrogen fixation by plants (in symbiosis with root bacteria) is a major source of new nitrogen for land ecosystems1. A long-standing puzzle2 is that trees capable of nitrogen fixation are abundant in nitrogen-rich tropical forests, but absent or restricted to early successional stages in nitrogen-poor extra-tropical forests. This biome-scale pattern presents an evolutionary paradox3, given that the physiological cost4 of nitrogen fixation predicts the opposite pattern: fixers should be out-competed by non-fixers in nitrogen-rich conditions, but competitively superior in nitrogen-poor soils. Here we evaluate whether this paradox can be explained by the existence of different fixation strategies in tropical versus extra-tropical trees: facultative fixers (capable of downregulating fixation5,6 by sanctioning mutualistic bacteria7) are common in the tropics, whereas obligate fixers (less able to downregulate fixation) dominate at higher latitudes. Using a game-theoretic approach, we assess the ecological and evolutionary conditions under which these fixation strategies emerge, and examine their dependence on climate-driven differences in the nitrogen cycle. We show that in the tropics, transient soil nitrogen deficits following disturbance and rapid tree growth favour a facultative strategy and the coexistence of fixers and non-fixers. In contrast, sustained nitrogen deficits following disturbance in extra-tropical forests favour an obligate fixation strategy, and cause fixers to be excluded in late successional stages. We conclude that biome-scale differences in the abundance of nitrogen fixers can be explained by the interaction between individual plant strategies and climatic constraints on the nitrogen cycle over evolutionary time.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: Climate and biome differences in soil nitrogen deficit and evolutionary stable strategies (ESS) of dinitrogen fixation.
Figure 2: Forest composition as a function of soil nitrogen.
Figure 3: Forest succession of dinitrogen fixers and non-fixers.

Similar content being viewed by others

References

  1. Vitousek, P. M., Menge, D. N. L., Reed, S. C. & Cleveland, C. C. Biological nitrogen fixation: rates, patterns, and ecological controls in terrestrial ecosystems. Phil. Trans. R. Soc. Lond. B 368, 20130119 (2013).

    Article  Google Scholar 

  2. Jenny, H. Causes of the high nitrogen and organic matter content of certain tropical forest soils. Soil Sci. 69, 63–69 (1950).

    Article  CAS  Google Scholar 

  3. Hedin, L. O., Brookshire, E. N. J., Menge, D. N. L. & Barron, A. R. The nitrogen paradox in tropical forest ecosystems. Annu. Rev. Ecol. Evol. Syst. 40, 613–635 (2009).

    Article  Google Scholar 

  4. Gutschick, V. P. Evolved strategies in nitrogen acquisition by plants. Am. Nat. 118, 607–637 (1981).

    Article  CAS  Google Scholar 

  5. Barron, A. R., Purves, D. W. & Hedin, L. O. Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165, 511–520 (2011).

    Article  Google Scholar 

  6. Menge, D. N. L., Levin, S. A. & Hedin, L. O. Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am. Nat. 174, 465–477 (2009).

    Article  Google Scholar 

  7. West, S. A., Kiers, E. T., Simms, E. L. & Denison, R. F. Sanctions and mutualism stability: why do rhizobia fix nitrogen?. Proc. R. Soc. Lond. B. 269, 685–694 (2002).

    Article  Google Scholar 

  8. 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 

  9. Crews, T. E. The presence of nitrogen fixing legumes in terrestrial communities: evolutionary vs ecological considerations. Biogeochemistry 46, 233–246 (1999).

    CAS  Google Scholar 

  10. Crocker, R. L. & Major, J. Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. J. Ecol. 43, 427–448 (1955).

    Article  Google Scholar 

  11. McKey, D. in Advances in Legume Systematics: Part 5 – The Nitrogen Factor (eds Sprent, J. L. & McKey, D. ) 211–228 (Royal Botanic Gardens, 1994).

    Google Scholar 

  12. Houlton, B. Z., Wang, Y. P., Vitousek, P. M. & Field, C. B. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330 (2008).

    Article  CAS  Google Scholar 

  13. Uliassi, D. D. & Ruess, R. W. Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83, 88–103 (2002).

    Article  Google Scholar 

  14. Binkley, D., Senock, R. & Cromack, K. Phosphorus limitation on nitrogen fixation by Facaltaria seedlings. For. Ecol. Manag. 186, 171–176 (2003).

    Article  Google Scholar 

  15. Barron, A. R. et al. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nature Geosci. 2, 42–45 (2009).

    Article  CAS  Google Scholar 

  16. Wing, S. L., Herrera, F., Jaramillo, C. A., Go, C. & Labandeira, C. C. Late Paleocene fossils from the Cerrejon Formation, Colombia, are the earliest record of neotropical rainforest. Proc. Natl. Acad. Sci. USA 106, 18627–18632 (2009).

    Article  CAS  Google Scholar 

  17. Werner, G. D., Cornwell, W. K., Sprent, J. I., Kattge, J. & Kiers, E. T. A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Commun. 5, 4087 (2014).

    Article  CAS  Google Scholar 

  18. Batterman, S. A. et al. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227 (2013).

    Article  CAS  Google Scholar 

  19. Sullivan, B. W. et al. Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc. Natl Acad. Sci. USA 11, 8101–8106 (2014).

    Article  Google Scholar 

  20. Menge, D. N. L. & Hedin, L. O. Nitrogen fixation in different biogeochemical niches along a 120,000-year chronosequence in New Zealand. Ecology 90, 2190–2201 (2009).

    Article  Google Scholar 

  21. Binkley, D., Sollins, P. Bell, R. Sachs, D. & Myrold, D. Biogeochemistry of adjacent conifer and alder–conifer stands. Ecology 73, 2022–2033 (1992).

    Article  CAS  Google Scholar 

  22. Menge, D. N. L., Lichstein, J. W. & Ángeles-Pérez, G. Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology 95, 2236–2245 (2014).

    Article  Google Scholar 

  23. Maynard Smith, J. On Evolution (Edinburgh University Press, 1972).

    Google Scholar 

  24. Manzoni, S., Jackson, R. B., Trofymow, J. A. & Porporato, A. The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686 (2008).

    Article  CAS  Google Scholar 

  25. McGroddy, M. E., Daufresne, T. & Hedin, L. O. Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85, 2390–2401 (2004).

    Article  Google Scholar 

  26. Parton, W. et al. Global-scale similarities in nitrogen release patterns during long term decomposition. Science 315, 361–362 (2007).

    Article  CAS  Google Scholar 

  27. Menge, D. N. L., Levin, S. A. & Hedin, L. O. Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation. Proc. Natl Acad. Sci. USA 105, 1573–1578 (2008).

    Article  CAS  Google Scholar 

  28. Rastetter, E. B. et al. Resource optimization and symbiotic nitrogen fixation. Ecosystems 4, 369–388 (2001).

    Article  CAS  Google Scholar 

  29. Eshel, I., Motro, U. & Sansone, E. Continuous stability and evolutionary convergence. J. Theor. Biol. 185, 333–343 (1997).

    Article  CAS  Google Scholar 

  30. Davidson, E. A. et al. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447, 995–998 (2007).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Menge, J. A. Bonachela, and the members of the Hedin and Levin labs for helpful comments and discussions. E.S. was funded by the NatureNet Science Fellows program, and the project was funded by the Andrew W. Mellon Foundation.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, 08544, New Jersey, USA

    Efrat Sheffer, Sarah A. Batterman, Simon A. Levin & Lars O. Hedin

  2. Institute of Plant Sciences and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, The Hebrew University of Jerusalem, Israel

    Efrat Sheffer

  3. School of Geography, University of Leeds, Leeds, UK

    Sarah A. Batterman

Authors
  1. Efrat Sheffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah A. Batterman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simon A. Levin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lars O. Hedin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.S. and L.H. designed research, E.S., S.B., L.H. and S.L. conceived the theoretical work, E.S. performed modelling work and analysed output data, S.B. provided field data, E.S. and L.H. wrote the manuscript, and all authors contributed to revisions.

Corresponding author

Correspondence to Efrat Sheffer.

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

Sheffer, E., Batterman, S., Levin, S. et al. Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nature Plants 1, 15182 (2015). https://doi.org/10.1038/nplants.2015.182

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.182

This article is cited by

Search

Advanced 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