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.

Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift

Abstract

Terrestrial ecosystems gain carbon through photosynthesis and lose it mostly in the form of carbon dioxide (CO2). The extent to which the biosphere can act as a buffer against rising atmospheric CO2 concentration in global climate change projections remains uncertain at the present stage1,2,3,4. Biogeochemical theory predicts that soil nitrogen (N) scarcity may limit natural ecosystem response to elevated CO2 concentration, diminishing the CO2-fertilization effect on terrestrial plant productivity in unmanaged ecosystems3,4,5,6,7. Recent models have incorporated such carbon–nitrogen interactions and suggest that anthropogenic N sources could help sustain the future CO2-fertilization effect8,9. However, conclusive demonstration that added N enhances plant productivity in response to CO2-fertilization in natural ecosystems remains elusive. Here we manipulated atmospheric CO2 concentration and soil N availability in a herbaceous brackish wetland where plant community composition is dominated by a C3 sedge and C4 grasses, and is capable of responding rapidly to environmental change10. We found that N addition enhanced the CO2-stimulation of plant productivity in the first year of a multi-year experiment, indicating N-limitation of the CO2 response. But we also found that N addition strongly promotes the encroachment of C4 plant species that respond less strongly to elevated CO2 concentrations. Overall, we found that the observed shift in the plant community composition ultimately suppresses the CO2-stimulation of plant productivity by the third and fourth years. Although extensive research has shown that global change factors such as elevated CO2 concentrations and N pollution affect plant species differently11,12,13 and that they may drive plant community changes14,15,16,17, we demonstrate that plant community shifts can act as a feedback effect that alters the whole ecosystem response to elevated CO2 concentrations. Moreover, we suggest that trade-offs between the abilities of plant taxa to respond positively to different perturbations may constrain natural ecosystem response to global change.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: The magnitude of the CO 2 effect.
Figure 2: Porewater ammonium concentrations over four growing seasons averaged over three depths.
Figure 3: The trajectories of plant biomass according to contributions from C 3 and C 4 plants in each treatment group.

References

  1. Denman, K. L. et al. in Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon, S. et al.) (Cambridge University Press, 2007)

    Google Scholar 

  2. Luo, Y. Q. Terrestrial carbon-cycle feedback to climate warming. Annu. Rev. Ecol. Evol. Syst. 38, 683–712 (2007)

    Article  Google Scholar 

  3. Reich, P. B., Hungate, B. A. & Luo, Y. Q. Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu. Rev. Ecol. Evol. Syst. 37, 611–636 (2006)

    Article  Google Scholar 

  4. Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y. Q. & Field, C. B. Nitrogen and climate change. Science 302, 1512–1513 (2003)

    CAS  Article  Google Scholar 

  5. Oren, R. et al. Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411, 469–472 (2001)

    ADS  CAS  Article  Google Scholar 

  6. Reich, P. B. et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2 . Nature 440, 922–925 (2006)

    ADS  CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  8. Sokolov, A. P. et al. Consequences of considering carbon-nitrogen interactions on the feedbacks between climate and the terrestrial carbon cycle. J. Clim. 21, 3776–3796 (2008)

    ADS  Article  Google Scholar 

  9. Thornton, P. E. et al. Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model. Biogeosci. Discuss. 6, 3303–3354 (2009)

    ADS  Article  Google Scholar 

  10. Langley, J. A., Mckee, K. L., Cahoon, D. R., Cherry, J. A. & Megonigal, J. P. Elevated CO2 stimulates marsh elevation gain, counterbalancing sea level rise. Proc. Natl Acad. Sci. USA 106, 6182–6186 (2009)

    ADS  CAS  Article  Google Scholar 

  11. Ainsworth, E. A. & Long, S. P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2 . New Phytol. 165, 351–371 (2005)

    Article  Google Scholar 

  12. Jablonski, L. M., Wang, X. Z. & Curtis, P. S. Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol. 156, 9–26 (2002)

    Article  Google Scholar 

  13. Xia, J. Y. & Wan, S. Q. Global response patterns of terrestrial plant species to nitrogen addition. New Phytol. 179, 428–439 (2008)

    CAS  Article  Google Scholar 

  14. Reich, P. B. et al. Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. New Phytol. 150, 435–448 (2001)

    CAS  Article  Google Scholar 

  15. Reich, P. B. Elevated CO2 reduces losses of plant diversity caused by nitrogen deposition. Science 326, 1399–1402 (2009)

    ADS  CAS  Article  Google Scholar 

  16. Erickson, J. E., Megonigal, J. P., Peresta, G. & Drake, B. G. Salinity and sea level mediate elevated CO2 effects on C3-C4 plant interactions and tissue nitrogen in a Chesapeake Bay tidal wetland. Glob. Change Biol. 13, 202–215 (2007)

    ADS  Article  Google Scholar 

  17. Zavaleta, E. S. et al. Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecol. Monogr. 73, 585–604 (2003)

    Article  Google Scholar 

  18. Schneider, M. K. et al. Ten years of free-air CO2 enrichment altered the mobilization of N from soil in Lolium perenne L. swards. Glob. Change Biol. 10, 1377–1388 (2004)

    ADS  Article  Google Scholar 

  19. Dukes, J. S. et al. Responses of grassland production to single and multiple global environmental changes. PLoS Biol. 3, 1829–1837 (2005)

    CAS  Article  Google Scholar 

  20. Hooper, D. U. & Vitousek, P. M. The effects of plant composition and diversity on ecosystem processes. Science 277, 1302–1305 (1997)

    CAS  Article  Google Scholar 

  21. Craine, J. M. et al. The role of plant species in biomass production and response to elevated CO2 and N. Ecol. Lett. 6, 623–630 (2003)

    Article  Google Scholar 

  22. Levine, J. M., Brewer, J. S. & Bertness, M. D. Nutrients, competition and plant zonation in a New England salt marsh. J. Ecol. 86, 285–292 (1998)

    Article  Google Scholar 

  23. Pennings, S. C. et al. Do individual plant species show predictable responses to nitrogen addition across multiple experiments? Oikos 110, 547–555 (2005)

    Article  Google Scholar 

  24. Tilman, D. Plant Strategies and the Dynamics and Structure of Plant Communities (Princeton University Press, 1988)

    Google Scholar 

  25. Craine, J. M. Resource Strategies of Wild Plants (Princeton University Press, 2009)

    Book  Google Scholar 

  26. Reynolds, H. L. & Pacala, S. W. An analytical treatment of root-to-shoot ratio and plant competition for soil nutrient and light. Am. Nat. 141, 51–70 (1993)

    CAS  Article  Google Scholar 

  27. Keller, J., Wolf, A., Weisenhorn, P., Drake, B. & Megonigal, J. Elevated CO2 affects porewater chemistry in a brackish marsh. Biogeochemistry 96, 101–117 (2009)

    CAS  Article  Google Scholar 

  28. de Graaff, M. A., van Groenigen, K. J., Six, J., Hungate, B. & van Kessel, C. Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob. Change Biol. 12, 2077–2091 (2006)

    ADS  Article  Google Scholar 

  29. Chapman, S. K., Langley, J. A., Hart, S. C. & Koch, G. W. Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol. 169, 27–34 (2006)

    CAS  Article  Google Scholar 

  30. Smith, M. D., Knapp, A. K. & Collins, S. L. A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology 90, 3279–3289 (2009)

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge the support of D. Cahoon, our primary US Geological Survey collaborator, who co-developed the experimental design of this study. We thank J. Duls, J. Keller, M. Sigrist, G. Peresta, B. Drake, E. Sage, A. Martin, D. McKinley, N. Mudd and K. White for the construction and maintenance of the field site at the Smithsonian Climate Change Facility. We appreciate comments from S. Chapman, A. Classen, J. Hines, B. Hungate, T. Mozdzer, A. Sutton-Grier and D. Whigham. The field study was supported by the USGS Global Change Research Program (cooperative agreement 06ERAG0011), the US Department of Energy (grant DE-FG02-97ER62458), the US Department of Energy’s Office of Science (BER) through the Coastal Center of the National Institute of Climate Change Research at Tulane University, and the Smithsonian Institution.

Author information

Authors and Affiliations

Authors

Contributions

Both J.A.L. and J.P.M. designed the experiment, interpreted the data and wrote the paper.

Corresponding author

Correspondence to J. Adam Langley.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figure 1 with legend, Supplementary Methods and References. (PDF 743 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Langley, J., Megonigal, J. Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466, 96–99 (2010). https://doi.org/10.1038/nature09176

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09176

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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