Article | Published:

Isotopic evidence for oligotrophication of terrestrial ecosystems

Nature Ecology & Evolutionvolume 2pages17351744 (2018) | Download Citation



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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The data sets generated during and/or analysed during the current study are available in the Dryad repository ( All codes used for statistical analyses and figure generation are available on Dryad (

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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.

Author information


  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


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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.

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.

Corresponding author

Correspondence to Joseph M. Craine.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–10 and Supplementary Tables 1–4

  2. Reporting Summary

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