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Exploring the Role of Cryptic Nitrogen Fixers in Terrestrial Ecosystems: A Frontier in Nitrogen Cycling Research

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Abstract

Biological nitrogen fixation represents the largest natural flux of new nitrogen (N) into terrestrial ecosystems, providing a critical N source to support net primary productivity of both natural and agricultural systems. When they are common, symbiotic associations between plants and bacteria can add more than 100 kg N ha−1 y−1 to ecosystems. Yet, these associations are uncommon in many terrestrial ecosystems. In most cases, N inputs derive from more cryptic sources, including mutualistic and/or free-living microorganisms in soil, plant litter, decomposing roots and wood, lichens, insects, and mosses, among others. Unfortunately, large gaps remain in the understanding of cryptic N fixation. We conducted a literature review to explore rates, patterns, and controls of cryptic N fixation in both unmanaged and agricultural ecosystems. Our analysis indicates that, as is common with N fixation, rates are highly variable across most cryptic niches, with N inputs in any particular cryptic niche ranging from near zero to more than 20 kg ha−1 y−1. Such large variation underscores the need for more comprehensive measurements of N fixation by organisms not in symbiotic relationships with vascular plants in terrestrial ecosystems, as well as identifying the factors that govern cryptic N fixation rates. We highlight several challenges, opportunities, and priorities in this important research area, and we propose a conceptual model that posits an interacting hierarchy of biophysical and biogeochemical controls over N fixation that should generate valuable new hypotheses and research.

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Acknowledgements

This paper is a contribution from a working group on biological nitrogen fixation supported by the U.S. Geological Survey John Wesley Powell Center and Ecosystems Mission Area to S.S.P., S.C.R., D.N.L.M., and C.C.C. C.C.C. acknowledges support from grants from the National Science Foundation to investigate nutrient cycling in terrestrial ecosystems (DEB-1754126, DEB-1556643, DEB-2027263). S.A.B. acknowledges support from the United Kingdom Natural Environment Research Council (NE/M019497/1, NE/S009663/1) and The Leverhulme Trust. M.G.T. acknowledges support from the Vilas Trust of the University of Wisconsin-Madison and the National Science Foundation (DEB-2027261). V.G.S. acknowledges support by the US Department of Energy, Office of Science, Biological and Environmental Research (BER) under contract DE-AC05-00OR22725. M.J.G. acknowledges support from the Swedish Research Council VR. We thank S. Jovan and A. Staccone for contributing to the development of the database. The paper also benefitted from useful discussions with B. Weber and E. Rodriguez-Caballero. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. We are grateful for constructive feedback from the editors, E. Rastetter, and two anonymous reviewers.

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Authors and Affiliations

  1. Department of Ecosystem and Conservation Sciences, W.A. Franke College of Forestry and Conservation, University of Montana, Missoula, Montana, 59812, USA

    Cory C. Cleveland & Katherine A. Dynarski

  2. Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon, 97331, USA

    Carla R. G. Reis

  3. Forest and Rangeland Ecosystem Science Center, US Geological Survey, Corvallis, Oregon, 97331, USA

    Steven S. Perakis

  4. Cary Institute of Ecosystem Studies, Millbrook, New York, 12545, USA

    Sarah A. Batterman

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

    Sarah A. Batterman

  6. Smithsonian Tropical Research Institute, Ancon, Panama

    Sarah A. Batterman

  7. The Land Institute, Salina, Kansas, 67401, USA

    Timothy E. Crews

  8. Association for Tropical Biology and Conservation, Minneapolis, Minnesota, 55405, USA

    Maga Gei

  9. Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden

    Michael J. Gundale

  10. Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, New York, 10027, USA

    Duncan N. L. Menge

  11. CSIRO Agriculture and Food, GPO Box 1700, Canberra, ACT, 2601, Australia

    Mark B. Peoples

  12. Southwest Biological Science Center, U.S. Geological Survey, Moab, Utah, 84532, USA

    Sasha C. Reed

  13. Environmental Science Division and Climate Change Science Institute, Oak Ridge National Laboratory, Oak Ridge, Tennessee, 37830, USA

    Verity G. Salmon

  14. Department of Biology and School of the Environment, McGill University, Montreal, Quebec, H3A 1B1, Canada

    Fiona M. Soper

  15. Department of Organismic and Evolutionary Biology, Harvard University, 1300 Centre St., Roslindale, Massachusetts, 02131, USA

    Benton N. Taylor

  16. Department of Integrative Biology, University of Wisconsin-Madison, Madison, Wisconsin, 53706, USA

    Monica G. Turner

  17. Odum School of Ecology, University of Georgia, Athens, Georgia, 30602, USA

    Nina Wurzburger

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Correspondence to Cory C. Cleveland.

Additional information

Author Contribution: All authors contributed to discussions about the ideas expressed in this paper. C.R.G.R. and S.P. led the development of the database, and all authors participated in the literature search and provided data to the database. C.C.C. and K.A.D. led the writing, and all co-authors provide text and revisions to the submitted version of the manuscript.

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Cleveland, C.C., Reis, C.R.G., Perakis, S.S. et al. Exploring the Role of Cryptic Nitrogen Fixers in Terrestrial Ecosystems: A Frontier in Nitrogen Cycling Research. Ecosystems 25, 1653–1669 (2022). https://doi.org/10.1007/s10021-022-00804-2

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