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Isotopic evidence for oligotrophication of terrestrial ecosystems

Nature Ecology & Evolution volume 2, pages 1735–1744 (2018)Cite this article

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Matters Arising to this article was published on 22 July 2019

Abstract

Human societies depend on an Earth system that operates within a constrained range of nutrient availability, yet the recent trajectory of terrestrial nitrogen (N) availability is uncertain. Examining patterns of foliar N concentrations and isotope ratios (δ15N) from more than 43,000 samples acquired over 37 years, here we show that foliar N concentration declined by 9% and foliar δ15N declined by 0.6–1.6‰. Examining patterns across different climate spaces, foliar δ15N declined across the entire range of mean annual temperature and mean annual precipitation tested. These results suggest declines in N supply relative to plant demand at the global scale. In all, there are now multiple lines of evidence of declining N availability in many unfertilized terrestrial ecosystems, including declines in δ15N of tree rings and leaves from herbarium samples over the past 75–150 years. These patterns are consistent with the proposed consequences of elevated atmospheric carbon dioxide and longer growing seasons. These declines will limit future terrestrial carbon uptake and increase nutritional stress for herbivores.

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Fig. 1: Relationships between residual foliar δ15N of non-N2-fixing species and predictors.
Fig. 2: Results of the regressions of residual foliar δ15N and residual log-transformed foliar [N].
Fig. 3: Conceptual diagram summarizing N availability bifurcation hypothesis for global terrestrial ecosystems.

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Data availability

The data sets generated during and/or analysed during the current study are available in the Dryad repository (https://doi.org/10.5061/dryad.v2k2607). All codes used for statistical analyses and figure generation are available on Dryad (https://doi.org/10.5061/dryad.v2k2607).

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Acknowledgements

Funding for this research was in part provided by the BRIDGE Project (ANR-2006 Biodiversity Call) and from an ‘Investissement d’Avenir’ grant managed by the Agence Nationale de la Recherche (CEBA, grant no. ANR-10-LABX-0025) (J.C.R.); by the European Research Council through the Advanced Grant Project TREEPEACE (grant no. FP7-339728) and the Cluster of Excellence COTE (grant no. ANR-10-LABX-45) (S.D.); by NASA project no. NNX12AK56G and EU MSCA individual fellowship (project no. 705432) (R.G.); by COILEX (grant no. CGL2008-01671), ECOLPIN (grant no. AGL2011-24296) and EU MSCA individual fellowship (project no. 750252) (S.M.J.); and by the Russian Science Foundation (grant no. 16-14-10208) (M.M.). No funding was provided to J.M.C. or A.J.E. in support of this research.

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Authors and Affiliations

  1. Jonah Ventures, Boulder, CO, USA

    Joseph M. Craine

  2. Appalachian Laboratory, University of Maryland Center for Environmental Science, Frostburg, MD, USA

    Andrew J. Elmore & David M. Nelson

  3. Department of Earth Sciences, Indiana University-Purdue University Indianapolis, Indianapolis, IN, USA

    Lixin Wang

  4. Facultad de Ciencias Exactas y Naturales (FCEN-UNCuyo), Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales (IANIGLA-CONICET), Mendoza, Argentina

    Julieta Aranibar

  5. MB Isotope Bioscience Laboratory – ISOFYS, Ghent University, Ghent, Belgium

    Marijn Bauters & Pascal Boeckx

  6. CAVElab, Computational and Applied Vegetation Ecology, Ghent University, Ghent, Belgium

    Marijn Bauters

  7. Department of Geology , University of Cincinnati, Cincinnati, OH, USA

    Brooke E. Crowley & Stella G. Mosher

  8. Department of Anthropology, University of Cincinnati, OH, USA

    Brooke E. Crowley

  9. Swiss Federal Institute for Forest, Snow and Landscape Research – WSL Forest soils and Biogeochemistry, Birmensdorf, Switzerland

    Melissa A. Dawes

  10. BIOGECO, INRA University of Bordeaux, Pessac, France

    Sylvain Delzon

  11. Centro de Investigación en Ecosistemas de la Patagonia, Coyhaique, Chile

    Alex Fajardo

  12. CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China

    Yunting Fang

  13. Research Institute for Humanity and Nature, Kyoto, Japan

    Lei Fujiyoshi

  14. NERC Centre for Ecology and Hydrology, Penicuik, UK

    Alan Gray

  15. Centre for Ecological Research and Forestry Applications, Barcelona, Spain

    Rossella Guerrieri

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

    Michael J. Gundale

  17. Department of Science and Primary Industries, Ara Institute of Canterbury, Christchurch, New Zealand

    David J. Hawke

  18. Institute of Botany, University of Natural Resources and Life Sciences, Vienna, Austria

    Peter Hietz

  19. Earth and Life Institute, Université Catholique de Louvain, Louvain-la-Neuve, Belgium

    Mathieu Jonard

  20. Computational and Applied Vegetation Ecology lab, Department of Environment, Ghent University, Ghent, Belgium

    Elizabeth Kearsley

  21. Department of Plant Ecology, Forestry and Forest Products Research Institute, Tsukuba, Japan

    Tanaka Kenzo

  22. Soil Science Department, Moscow M.V. Lomonosov State University, Moscow, Russia

    Mikhail Makarov

  23. Department of Ecology, Faculty of Sciences, University of Granada, Granada, Spain

    Sara Marañón-Jiménez

  24. CREAF, Barcelona, Spain

    Sara Marañón-Jiménez

  25. CSIC, Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Spain

    Sara Marañón-Jiménez

  26. Department of Biology, California State University Dominguez Hills, Carson, CA, USA

    Terrence P. McGlynn

  27. Department of Entomology, Natural History Museum of Los Angeles County, Los Angeles, CA, USA

    Terrence P. McGlynn

  28. Department of Geology and Geography, West Virginia University, Morgantown, WV, USA

    Brenden E. McNeil

  29. Instituto Nacional de Tecnología Agropecuaria, CONICET Universidad Nacional de la Patagonia Austral, Río Gallegos, Argentina

    Pablo L. Peri

  30. INRA, UMR Ecologie des Forêts de Guyane, Campus Agronomique, Kourou, Guyane Française, France

    Jean Christophe Roggy

  31. Department of Biology, Boston University, Boston, MA, USA

    Rebecca Sanders-DeMott & Pamela H. Templer

  32. Department of Natural Resources and the Environment, University of New Hampshire, Durham, NH, USA

    Rebecca Sanders-DeMott & Xingliang Xu

  33. Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, China

    Minghua Song

  34. Department of Anthropology, Trent University, Peterborough, Ontario, Canada

    Paul Szpak

  35. South African National Biodiversity Institute, Cape Town, South Africa

    Dewidine Van der Colff

  36. Ecosystem Physiology, University of Freiburg, Freiburg, Germany

    Christiane Werner

  37. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China

    Yang Yang

  38. Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, China

    Guirui Yu

  39. College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China

    Guirui Yu

  40. Faculty of Biology, Department of Vertebrate Ecology and Zoology, University of Gdańsk, Gdańsk, Poland

    Katarzyna Zmudczyńska-Skarbek

Authors
  1. Joseph M. Craine
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  2. Andrew J. Elmore
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  34. Christiane Werner
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  35. Xingliang Xu
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Contributions

J.M.C. and A.J.E. conceived of the research, conducted analyses, generated figures and prepared the original draft. All authors contributed data and provided comments on manuscripts.

Corresponding author

Correspondence to Joseph M. Craine.

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Competing interests

Although J.M.C. is an owner of Jonah Ventures, a for-profit DNA sequencing company, the authors declare no competing interests in the publication of this research.

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Craine, J.M., Elmore, A.J., Wang, L. et al. Isotopic evidence for oligotrophication of terrestrial ecosystems. Nat Ecol Evol 2, 1735–1744 (2018). https://doi.org/10.1038/s41559-018-0694-0

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