Skip to main content

Thank you for visiting nature.com. 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.

  • Matters Arising
  • Published:

Reply to: Data do not support large-scale oligotrophication of terrestrial ecosystems

Nature Ecology & Evolution volume 3, pages 1287–1288 (2019)Cite this article

Subjects

The Original Article was published on 22 July 2019

replying to Hiltbrunner, E., Körner, C., Meier, R., Braun, S. & Kahmen, A. Nature Ecology & Evolution https://doi.org/10.1038/s41559-019-0948-5 (2019).

Hiltbrunner et al.1 apply a reductionist approach to argue that the evidence for widespread terrestrial oligotrophication2 should be replaced with a two-factor explanation (growth dilution and depositional signatures) that does not invoke reductions in N availability, that is, the supply of N relative to plant demand. Contrary to any “adjustment of leaf photosynthetic capacity and a widening of leaf C:N ratios,” there is little evidence that observed declines in foliar [N] are caused solely by photosynthetic downregulation. Photosynthetic downregulation is not universal and probably could be caused by reduced N availability3. A comprehensive synthesis of data on responses of plant productivity and N acquisition to elevated CO2 in free-air carbon dioxide enrichment (FACE) experiments demonstrated that there were declines in N uptake in low-N ecosystems as a result of decreased ‘access’ to N, not reduced demand4. The growth dilution hypothesis was ‘refuted’ as an explanation for these declines4.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Parsimony diagram representing the relative evidence for different explanations behind declines in foliar [N] and δ15N.

References

  1. Hiltbrunner, E., Körner, C., Meier, R., Braun, S. & Kahmen, A. Data do not support large-scale oligotrophication of terrestrial ecosystems. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-019-0948-5 (2019).

    Article  Google Scholar 

  2. Craine, J. M. et al. Isotopic evidence for oligotrophication of terrestrial ecosystems. Nat. Ecol. Evol. 2, 1735–1744 (2018).

    Article  PubMed  Google Scholar 

  3. Luo, Y. et al. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54, 731–739 (2004).

    Article  Google Scholar 

  4. Feng, Z. et al. Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. Glob. Change Biol. 21, 3152–3168 (2015).

    Article  Google Scholar 

  5. McLauchlan, K. K. et al. Centennial-scale reductions in nitrogen availability in temperate forests of the United States. Sci. Rep. 7, 7856 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Holtgrieve, G. W. et al. A coherent signature of anthropogenic nitrogen deposition to remote watersheds of the Northern Hemisphere. Science 334, 1545–1548 (2011).

    Article  CAS  PubMed  Google Scholar 

  7. McLauchlan, K. K., Ferguson, C. J., Wilson, I. E., Ocheltree, T. W. & Craine, J. M. Thirteen decades of foliar isotopes indicate declining nitrogen availability in central North American grasslands. New Phytol. 187, 1135–1145 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Elliott, E. M., Yu, Z., Cole, A. S. & Coughlin, J. G. Isotopic advances in understanding reactive nitrogen deposition and atmospheric processing. Sci. Total Environ. 662, 393–403 (2019).

    Article  CAS  PubMed  Google Scholar 

  9. Hogberg, P. Development of nitrogen-15 enrichment in a nitrogen-fertilized forest soil-plant system. Soil Biol. Biochem. 23, 335–338 (1991).

    Article  Google Scholar 

  10. Craine, J. M. et al. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396, 1–26 (2015).

    Article  CAS  Google Scholar 

  11. BassiriRad, H. et al. Widespread foliage delta N-15 depletion under elevated CO2: inferences for the nitrogen cycle. Glob. Change Biol. 9, 1582–1590 (2003).

    Article  Google Scholar 

  12. Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E. & McMurtrie, R. E. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010).

    Article  CAS  PubMed  Google Scholar 

  13. Groffman, P. M. et al. Nitrogen oligotrophication in northern hardwood forests. Biogeochemistry 141, 523–539 (2018).

    Article  CAS  Google Scholar 

  14. Craine, J. M., Elmore, A. & Angerer, J. P. Long-term declines in dietary nutritional quality for North American cattle. Environ. Res. Lett. 12, 044019 (2017).

    Article  Google Scholar 

  15. Ziska, L. H. et al. Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proc. R. Soc. B 283, 20160414 (2016).

    Article  PubMed  Google Scholar 

  16. Gruneberg, E., Ziche, D. & Wellbrock, N. Organic carbon stocks and sequestration rates of forest soils in Germany. Glob. Change Biol. 20, 2644–2662 (2014).

    Article  Google Scholar 

  17. Durán, J. et al. Climate change decreases nitrogen pools and mineralization rates in northern hardwood forests. Ecosphere 7, e01251 (2016).

    Article  Google Scholar 

  18. Eshleman, K. N., Sabo, R. D. & Kline, K. M. Surface water quality is improving due to declining atmospheric N deposition. Environ. Sci. Technol. 47, 12193–12200 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Sabo, R. D. et al. Watershed-scale changes in terrestrial nitrogen cycling during a period of decreased atmospheric nitrate and sulfur deposition. Atmos. Environ. 146, 271–279 (2016).

    Article  CAS  Google Scholar 

  20. Lucas, R. W. et al. Long‐term declines in stream and river inorganic nitrogen (N) export correspond to forest change. Ecol. Appl. 26, 545–556 (2016).

    Article  PubMed  Google Scholar 

  21. Bernal, S., Hedin, L. O., Likens, G. E., Gerber, S. & Buso, D. C. Complex response of the forest nitrogen cycle to climate change. Proc. Natl Acad. Sci. USA 109, 3406–3411 (2012).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

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. MB Isotope Bioscience Laboratory, Ghent University, Ghent, Belgium

    Pascal Boeckx

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

    Sylvain Delzon

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

    Yunting Fang

  7. NERC Centre for Ecology and Hydrology, Midlothian, UK

    Alan Gray

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

    Rossella Guerrieri

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

    Michael J. Gundale

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

    Peter Hietz

  11. Universidad Nacional de la Patagonia Austral, Instituto Nacional de Tecnología Agropecuaria, CONICET, Santa Cruz, Argentina

    Pablo L. Peri

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

    Pamela H. Templer

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

    Christiane Werner

Authors
  1. Joseph M. Craine
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew J. Elmore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lixin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pascal Boeckx
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sylvain Delzon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yunting Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alan Gray
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rossella Guerrieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Michael J. Gundale
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Peter Hietz
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. David M. Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Pablo L. Peri
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Pamela H. Templer
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Christiane Werner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph M. Craine.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Craine, J.M., Elmore, A.J., Wang, L. et al. Reply to: Data do not support large-scale oligotrophication of terrestrial ecosystems. Nat Ecol Evol 3, 1287–1288 (2019). https://doi.org/10.1038/s41559-019-0949-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0949-4

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene