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

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.

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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.

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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.

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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.

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Correspondence to Efrat Sheffer.

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The authors declare no competing financial interests.

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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

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