Skip to main content

Thank you for visiting 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.

Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen


Nitrogen limits primary production in almost every biome on Earth1,2. Symbiotic nitrogen fixation, conducted by certain angiosperms and their endosymbiotic bacteria, is the largest potential natural source of new nitrogen into the biosphere3, influencing global primary production, carbon sequestration and element cycling. Because symbiotic nitrogen fixation represents an alternative to soil nitrogen uptake, much of the work on symbiotic nitrogen fixation regulation has focused on soil nitrogen availability4,5,6,7,8. However, because symbiotic nitrogen fixation is an energetically expensive process9, light availability to the plant may also regulate symbiotic nitrogen fixation rates10,11. Despite the importance of symbiotic nitrogen fixation to biosphere functioning, the environmental factors that most strongly regulate this process remain unresolved. Here we show that light regulates symbiotic nitrogen fixation more strongly than does soil nitrogen and that light mediates the response of symbiotic nitrogen fixation to soil nitrogen availability. In a shadehouse experiment, low light levels (comparable with forest understories) completely shut down symbiotic nitrogen fixation, whereas soil nitrogen levels that far exceeded plant demand did not fully downregulate symbiotic nitrogen fixation at high light. For in situ forest seedlings, light was a notable predictor of symbiotic nitrogen fixation activity, but soil-extractable nitrogen was not. Light as a primary regulator of symbiotic nitrogen fixation is a departure from decades of focus on soil nitrogen availability. This shift in our understanding of symbiotic nitrogen fixation regulation can resolve a long-standing biogeochemical paradox12, and it will improve our ability to predict how symbiotic nitrogen fixation will fuel the global forest carbon sink and respond to human alteration of the global nitrogen cycle.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Light is a stronger driver than soil N for plant biomass and N fixation in shadehouse-grown plants.
Fig. 2: Light drives total fixed N in plants more strongly than soil N.
Fig. 3: In situ field nodulation varies with light, but not soil N.
Fig. 4: Our results in the context of SNF theory.


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

    Article  Google Scholar 

  2. 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 

  3. Chapin, F. III, Matson, P. & Vitousek, P. Principles of Terrestrial Ecosystem Ecology (Springer, New York, NY, 2011).

    Book  Google Scholar 

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

    Article  Google Scholar 

  5. Menge, D. N. L., Wolf, A. A. & Funk, J. L. Diversity of nitrogen fixation strategies in Mediterranean legumes. Nat. Plants 1, 15064 (2015).

    CAS  Article  Google Scholar 

  6. 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 

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

    CAS  Article  Google Scholar 

  8. Batterman, S. A., Wurzburger, N. & Hedin, L. O. Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J. Ecol. 101, 1400–1408 (2013).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  10. Rastetter, E., Vitousek, P. & Field, C. Resource optimization and symbiotic nitrogen fixation. Ecosystems 4, 369–388 (2001).

    CAS  Article  Google Scholar 

  11. Vitousek, P. & Field, C. Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46, 179–202 (1999).

    CAS  Google Scholar 

  12. 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 

  13. Crews, T. E. Phosphorus regulation of nitrogen fixation in a traditional Mexican agroecosystem. Biogeochemistry 21, 141–166 (1993).

    CAS  Article  Google Scholar 

  14. Wurzburger, N. & Miniat, C. F. Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174, 1117–1126 (2014).

    Article  Google Scholar 

  15. 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).

    CAS  Article  Google Scholar 

  16. Murphy, P. M. Effect of light and atmospheric carbon dioxide concentration on nitrogen fixation by herbage legumes. Plant Soil 95, 399–409 (1986).

    CAS  Article  Google Scholar 

  17. MacDowall, F. D. H. Effects of light intensity and CO2 concentration on the kinetics of 1st month growth and nitrogen fixation of alfalfa. Can. J. Bot. 61, 731–740 (1982).

    Article  Google Scholar 

  18. Lau, J. A. et al. Direct and interactive effects of light and nutrients on the legume-rhizobia mutualism. Acta Oecol. 39, 80–86 (2012).

    Article  Google Scholar 

  19. McHargue, L. A. Factors Affecting the Nodulation and Growth of Tropical Woody Legume Seedlings (Florida International University, Miami, FL, 1999).

  20. Myster, R. W. Light and nutrient effects on growth and allocation of Inga vera (Leguminosae), a successional tree of Puerto Rico. Can. J. For. Res. 36, 1121–1128 (2006).

    Article  Google Scholar 

  21. Sprent, J. I. Growth and nitrogen fixation in Lupinus arboreus as affected by shading and water supply. New Phytol. 72, 1005–1022 (1973).

    Article  Google Scholar 

  22. Oberbauer, S. F., & Strain, B. R. Effects of light regime on the growth and physiology of Pentaclethra macroloba (Mimosaceae) in Costa Rica. J. Trop. Ecol. 1, 303–320 (1985).

    Article  Google Scholar 

  23. Vitousek, P. M. & Matson, P. A. Nitrogen transformations in a range of tropical forest soils. Soil Biol. Biochem. 20, 361–367 (1988).

    CAS  Article  Google Scholar 

  24. Chou, C. B., Hedin, L. O. & Pacala, S. W. Functional groups, species and light interact with nutrient limitation during tropical rainforest sapling bottleneck. J. Ecol. 106, 157–167 (2018).

    CAS  Article  Google Scholar 

  25. Chazdon, R. L. & Pearcy, R. W. The importance of sunflecks for forest understory plants. Bioscience 41, 760–766 (1991).

    Article  Google Scholar 

  26. Pons, T. L., Perreijn, K., van Kessel, C. & Werger, M. J. A. Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytol. 173, 154–167 (2007).

    CAS  Article  Google Scholar 

  27. 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 

  28. Menge, D. N. L. et al. Why are nitrogen-fixing trees rare at higher compared to lower latitudes? Ecology 98, 3127–3140 (2017).

    Article  Google Scholar 

  29. Brookshire, E. N. J., Gerber, S., Menge, D. N. L. & Hedin, L. O. Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecol. Lett. 15, 9–16 (2012).

    CAS  Article  Google Scholar 

  30. Liang, S. et al. Global LAnd Surface Satellite (GLASS) Products (Springer, New York, NY, 2014).

    Book  Google Scholar 

  31. Sollins, P., Sancho, M. F., Mata, C. R. & Sanford, R. L. in La Selva: Ecology and Natural History of a Neotropical Rain Forest (ed McDade, L.) Ch. 4 (University of Chicago Press: Chicago, IL, 1994).

  32. Flores, E. M. in Tropical Tree Seed Manual: Agricultural Handbook (Academia Nacional de Ciencias de Costa Rica, San Jose, 2002).

  33. Lieberman, D. & Lieberman, M. Forest tree growth and dynamics at La Selva, Costa Rica (1969–1982). J. Trop. Ecol. 3, 347–358 (1987).

    Article  Google Scholar 

  34. Joker, D. & Salazar, R. Pentaclethra macroloba. Seed Leafl. 35, 1–3 (2000).

    Google Scholar 

  35. Brady, N. C. & Weil, R. R. The Nature and Properties of Soils (Prentice Hall, Upper Saddle River, NJ, 2002).

  36. Chalk, P. M. Estimation of N2 fixation by isotope dilution: an appraisal of techniques involving 15N enrichment and their application. Soil Biol. Biochem. 17, 389–410 (1985).

    CAS  Article  Google Scholar 

  37. Reed, S. C., Cleveland, C. C. & Townsend, A. R. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu. Rev. Ecol. Evol. Syst. 42, 489–512 (2011).

    Article  Google Scholar 

  38. Russell, A. E. & Raich, J. W. Rapidly growing tropical trees mobilize remarkable amounts of nitrogen, in ways that differ surprisingly among species. Proc. Natl Acad. Sci. USA 109, 10398–10402 (2012).

    CAS  Article  Google Scholar 

  39. Phillips, D. & Gregg, J. Uncertainty in source partitioning using stable isotopes. Oecologia 127, 171–179 (2001).

    Article  Google Scholar 

  40. Anderson, D. R. Model Based Inference in the Life Sciences: A Primer on Evidence (Springer, New York, NY, 2008).

    Book  Google Scholar 

  41. Chazdon, R. L. et al. Rates of change in tree communities of secondary Neotropical forests following major disturbances. Philos. T. Roy. Soc. B 362, 273–289 (2007).

    Article  Google Scholar 

  42. Menge, D. N. L. & Chazdon, R. L. Higher survival drives the success of nitrogen-fixing trees through succession in Costa Rican rainforests. New Phytol. 209, 965–977 (2016).

    CAS  Article  Google Scholar 

  43. Taylor,B. N., Chazdon, R. L., Bachelot, B. & Menge, D. N. L. Nitrogen-fixing trees inhibit growth of regenerating Costa Rican rainforests. Proc. Natl Acad. Sci. USA 114, 8817–8822 (2017).

    CAS  Article  Google Scholar 

  44. Tian, L. & Wu, J. Confidence intervals for the mean of lognormal data with excess zeros. Biometrical J. 48, 149–156 (2006).

    Article  Google Scholar 

  45. Bolker, B. M. & R Development Core Team. bbmle: tools for general maximum likelihood estimation. (2017).

  46. R Core Team. R: A language and environment for statistical computing. (2017).

Download references


The authors thank E. Salicetti, M. Wilcots, R. Li, S. Taylor, B. Scott, E. Utset, B. Matarrita, D. Madrigal and O. Vargas for help conducting the experiment, and collecting and processing samples. This work was supported by the Garden Club of America’s Award in Tropical Botany, Columbia University’s Earth Institute and the Institute for Latin American Studies.

Author information

Authors and Affiliations



B.N.T. designed and implemented the study, analysed data and wrote the first draft. D.N.L.M. designed the study, analysed data and revised the manuscript.

Corresponding author

Correspondence to Benton N. Taylor.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figure 1 and Supplementary Tables 1–3.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Taylor, B.N., Menge, D.N.L. Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen. Nature Plants 4, 655–661 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

Further reading


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