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Plant growth enhancement by elevated CO2 eliminated by joint water and nitrogen limitation

Abstract

Rising atmospheric CO2 concentrations can fertilize plant growth. The resulting increased plant uptake of CO2 could, in turn, slow increases in atmospheric CO2 levels and associated climate warming. CO2 fertilization effects may be enhanced when water availability is low, because elevated CO2 also leads to improved plant water-use efficiency. However, CO2 fertilization effects may be weaker when plant growth is limited by nutrient availability. How variation in soil nutrients and water may act together to influence CO2 fertilization is unresolved. Here we report plant biomass levels from a five-year, open-air experiment in a perennial grassland under two contrasting levels of atmospheric CO2, soil nitrogen and summer rainfall, respectively. We find that the presence of a CO2 fertilization effect depends on the amount of available nitrogen and water. Specifically, elevated CO2 levels led to an increase in plant biomass of more than 33% when summer rainfall, nitrogen supply, or both were at the higher levels (ambient for rainfall and elevated for soil nitrogen). But elevated CO2 concentrations did not increase plant biomass when both rainfall and nitrogen were at their lower level. We conclude that given widespread, simultaneous limitation by water and nutrients, large stimulation of biomass by rising atmospheric CO2 concentrations may not be ubiquitous.

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Figure 1: Biomass tracks rainfall inputs across treatments and years.
Figure 2: Biomass in relation to treatments and number of limiting resources.

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References

  1. Arneth, A. et al. Terrestrial biogeochemical cycles in the climate system. Nature Geosci. 3, 525–532 (2010).

    Article  Google Scholar 

  2. Rastetter, E. B. & Shaver, G. R. A model of multiple element limitation for acclimating vegetation. Ecology 73, 1157–1174 (1992).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  7. Rastetter, E. B., Agren, G. I. & Shaver, G. R. Responses of N-limited ecosystems to increased CO2: A balanced-nutrition coupled-element-cycles model. Ecol. Appl. 7, 444–460 (1997).

    Google Scholar 

  8. Morgan, J. et al. C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature 476, 202–205 (2011).

    Article  Google Scholar 

  9. Donohue, R. J., Roderick, M. L., McVicar, T. R. & Farquhar, G. D. Impact of CO2 fertilization on maximum foliage cover across the globe’s warm, arid environments. Geophys. Res. Lett. 40, 3031–3035 (2013).

    Article  Google Scholar 

  10. Dukes, J. S. et al. Responses of grassland production to single and multiple global environmental changes. PLoS Biol. 3, e319 (2005).

    Article  Google Scholar 

  11. Garten, C. T. Jr et al. Role of N2-fixation in constructed oldfield communities under different regimes of [CO2], temperature, and water availability. Ecosystems 11, 125–137 (2008).

    Article  Google Scholar 

  12. Engel, E. C., Weltzin, J. F., Norby, R. J. & Classen, A. T. Responses of an old field plant community to interacting factors of elevated [CO2], warming, and soil moisture. J. Plant Ecol. 2, 1–11 (2009).

    Article  Google Scholar 

  13. Andresen, L. C., Michelsen, A., Ambus, P. & Beier, C. Belowground heathland responses after 2 years of combined warming, elevated CO2 and summer drought. Biogeochemistry 101, 27–42 (2010).

    Article  Google Scholar 

  14. Derner, J. D. et al. Above- and below-ground responses of C3–C4 species mixtures to elevated CO2 and soil water availability. Glob. Change Biol. 9, 452–460 (2003).

    Article  Google Scholar 

  15. Morgan, J. A. et al. Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2 . Oecologia 140, 11–25 (2004).

    Article  Google Scholar 

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

    Article  Google Scholar 

  17. Gill, R. A. et al. Nonlinear grassland responses to past and future atmospheric CO2 . Nature 417, 279–282 (2002).

    Article  Google Scholar 

  18. Langley, J. A. & Megonigal, J. P. Ecosystem response to elevated CO2 limited by nitrogen-induced plant species shift. Nature 466, 96–99 (2010).

    Article  Google Scholar 

  19. 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, 351–372 (2005).

    Article  Google Scholar 

  20. Adair, E. C., Reich, P. B., Trost, J. & Hobbie, S. E. Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Glob. Change Biol. 17, 3546–3563 (2011).

    Article  Google Scholar 

  21. Lee, T. D., Barrott, S. H. & Reich, P. B. Photosynthetic responses of 13 grassland species across 11 years of free-air CO2 enrichment is modest, consistent and independent of N supply. Glob. Change Biol. 17, 2893–2904 (2011).

    Article  Google Scholar 

  22. Volk, M., Niklaus, P. A. & Körner, C. Soil moisture effects determine CO2 responses of grassland species. Oecologia 125, 380–388 (2000).

    Article  Google Scholar 

  23. Dermody, O., Weltzin, J. F., Engel, E. C., Allen, P. & Norby, R. J. How do elevated [CO2], warming, and reduced precipitation interact to affect soil moisture and LAI in an old field ecosystem? Plant Soil 301, 255–266 (2007).

    Article  Google Scholar 

  24. 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  Google Scholar 

  25. Larsen, K. S. et al. Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: Synthesizing results of the CLIMAITE project after two years of treatments. Glob. Change Biol. 17, 1884–1899 (2011).

    Article  Google Scholar 

  26. Luo, Y. et al. Modeled interactive effects of precipitation, temperature, and [CO2] on ecosystem carbon and water dynamics in different climatic zones. Glob. Change Biol. 14, 1986–1999 (2008).

    Article  Google Scholar 

  27. Reich, P. B. & Hobbie, S. E. Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nature Clim. Change 3, 278–282 (2013).

    Article  Google Scholar 

  28. McCarthy, H. R. et al. Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: Interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol. 185, 514–528 (2010).

    Article  Google Scholar 

  29. Inauen, N., Korner, C. & Hiltbrunner, E. No growth stimulation by CO2 enrichment in alpine glacier forefield plants. Glob. Change Biol. 18, 985–999 (2012).

    Article  Google Scholar 

  30. 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 deposition regimes? A field test with 16 grassland species. New Phytol. 150, 435–448 (2001).

    Article  Google Scholar 

  31. Knapp, A. K. & Smith, M. D. Variation among biomes in temporal dynamics of aboveground primary production. Science 291, 481–484 (2001).

    Article  Google Scholar 

  32. Goward, S. N. & Prince, S. D. Transient effects of climate on vegetation dynamics: Satellite observations. J. Biogeogr. 22, 549–563 (1995).

    Article  Google Scholar 

  33. Hoover, D. L., Knapp, A. K. & Smith, M. D. Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95, 2646–2656 (2014).

    Article  Google Scholar 

  34. Davis, M. A. et al. Survival, growth and photosynthesis of tree seedlings competing with herbaceous vegetation along a water-light-nitrogen gradient. Plant Ecol. 145, 341–350 (1999).

    Article  Google Scholar 

  35. Harpole, W. S. & Tilman, D. Grassland species loss resulting from reduced niche dimension. Nature 446, 791–793 (2007).

    Article  Google Scholar 

  36. Galloway, J. N. et al. Nitrogen cycles: Past, present, and future. Biogeochemistry 70, 153–226 (2004).

    Article  Google Scholar 

  37. Bala, G., Devaraju, N., Chaturvedi, R. K., Caldeira, K. & Nemani, R. Nitrogen deposition: How important is it for global terrestrial carbon uptake? Biogeosciences 10, 7147–7160 (2013).

    Article  Google Scholar 

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Acknowledgements

This research has been supported by the US National Science Foundation (NSF) Long-Term Ecological Research (DEB-9411972, DEB-0080382, DEB-0620652, and DEB-1234162), Biocomplexity Coupled Biogeochemical Cycles (DEB-0322057), Long-Term Research in Environmental Biology (DEB-0716587, DEB-1242531) and Ecosystem Sciences (NSF DEB-1120064) Programs; as well as the U.S. Department of Energy Program for Ecosystem Research (DE-FG02-96ER62291) and National Institute for Climatic Change Research (DE-FC02-06ER64158).

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This experiment was designed and implemented by all three authors; P.B.R. did the analyses and wrote the initial draft; all three authors contributed to editing and revising the manuscript.

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Correspondence to Peter B. Reich.

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The authors declare no competing financial interests.

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Reich, P., Hobbie, S. & Lee, T. Plant growth enhancement by elevated CO2 eliminated by joint water and nitrogen limitation. Nature Geosci 7, 920–924 (2014). https://doi.org/10.1038/ngeo2284

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