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.

  • Letter
  • Published:

Prolonged suppression of ecosystem carbon dioxide uptake after an anomalously warm year

Abstract

Terrestrial ecosystems control carbon dioxide fluxes to and from the atmosphere1,2 through photosynthesis and respiration, a balance between net primary productivity and heterotrophic respiration, that determines whether an ecosystem is sequestering carbon or releasing it to the atmosphere. Global1,3,4,5 and site-specific6 data sets have demonstrated that climate and climate variability influence biogeochemical processes that determine net ecosystem carbon dioxide exchange (NEE) at multiple timescales. Experimental data necessary to quantify impacts of a single climate variable, such as temperature anomalies, on NEE and carbon sequestration of ecosystems at interannual timescales have been lacking. This derives from an inability of field studies to avoid the confounding effects of natural intra-annual and interannual variability in temperature and precipitation. Here we present results from a four-year study using replicate 12,000-kg intact tallgrass prairie monoliths located in four 184-m3 enclosed lysimeters7. We exposed 6 of 12 monoliths to an anomalously warm year in the second year of the study8 and continuously quantified rates of ecosystem processes, including NEE. We find that warming decreases NEE in both the extreme year and the following year by inducing drought that suppresses net primary productivity in the extreme year and by stimulating heterotrophic respiration of soil biota in the subsequent year. Our data indicate that two years are required for NEE in the previously warmed experimental ecosystems to recover to levels measured in the control ecosystems. This time lag caused net ecosystem carbon sequestration in previously warmed ecosystems to be decreased threefold over the study period, compared with control ecosystems. Our findings suggest that more frequent anomalously warm years9, a possible consequence of increasing anthropogenic carbon dioxide levels10, may lead to a sustained decrease in carbon dioxide uptake by terrestrial ecosystems.

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

Access options

Buy this article

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

Figure 1: Four-year time courses covering pretreatment (11 February 2002 to 10 February 2003), treatment and post-treatment years.
Figure 2: Effects of an anomalously warm year on annual ecosystem C flows.
Figure 3: Actual change in ecosystem annual NEP for control and warmed ecosystems from 2002 to 2003, 2002 to 2004, and 2002 to 2005.

Similar content being viewed by others

References

  1. Keeling, C. D., Chin, J. F. S. & Whorf, T. P. Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382, 146–149 (1996)

    Article  ADS  CAS  Google Scholar 

  2. Schimel, D. S. Terrestrial ecosystems and the carbon-cycle. Glob. Change Biol. 1, 77–91 (1995)

    Article  ADS  Google Scholar 

  3. Myneni, R. B., Keeling, C. D., Tucker, C. J., Asrar, G. & Nemani, R. R. Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386, 698–702 (1997)

    Article  ADS  CAS  Google Scholar 

  4. Randerson, J. T., Thompson, M. V., Conway, T. J., Fung, I. Y. & Field, C. B. The contribution of terrestrial sources and sinks to trends in the seasonal cycle of atmospheric carbon dioxide. Glob. Biogeochem. Cycles 11, 535–560 (1997)

    Article  ADS  CAS  Google Scholar 

  5. Vukicevic, T., Braswell, B. H. & Schimel, D. A diagnostic study of temperature controls on global terrestrial carbon exchange. Tellus 53B, 150–170 (2001)

    Article  ADS  CAS  Google Scholar 

  6. Law, B. E. et al. Environmental controls over carbon dioxide and water vapor exchange of terrestrial vegetation. Agric. Forest Meteorol. 113, 97–120 (2002)

    Article  ADS  Google Scholar 

  7. Griffin, K. L. et al. EcoCELLs: Tools for mesocosm scale measurements of gas exchange. Plant Cell Environ. 19, 1210–1221 (1996)

    Article  CAS  Google Scholar 

  8. Verburg, P. S. J., Larsen, J. D., Johnson, D. W., Schorran, D. E. & Arnone, J. A. Impacts of an anomalously warm year on soil CO2 fluxes in experimentally manipulated tallgrass prairie ecosystems. Glob. Change Biol. 11, 1720–1732 (2005)

    Article  ADS  Google Scholar 

  9. Easterling, D. R. et al. Climate extremes: Observations, modeling, and impacts. Science 289, 2068–2074 (2000)

    Article  ADS  CAS  Google Scholar 

  10. Intergovernmental Panel on Climate Change. Climate Change 2007: The Physical Science Basis: Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2007)

  11. Braswell, B. H., Schimel, D. S., Linder, E. & Moore, B. The response of global terrestrial ecosystems to interannual temperature variability. Science 278, 870–872 (1997)

    Article  ADS  CAS  Google Scholar 

  12. Tian, H. Q. et al. Effect of interannual climate variability on carbon storage in Amazonian ecosystems. Nature 396, 664–667 (1998)

    Article  ADS  CAS  Google Scholar 

  13. Körner, C. in Ecology of Photosynthesis (eds Schulze, E. D. & Caldwell, M. M.) 463–490 (Springer, 1994)

    Google Scholar 

  14. Bunce, J. A. Low humidity effects on photosynthesis in single leaves of C-4 plants. Oecologia 54, 233–235 (1982)

    Article  ADS  Google Scholar 

  15. Oren, R. et al. Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ. 22, 1515–1526 (1999)

    Article  Google Scholar 

  16. Wever, L., Flanagan, L. B. & Carlson, P. J. Seasonal and interannual variation in evapotranspiration, energy balance and surface conductance in a northern temperate grassland. Agric. For. Meteorol. 112, 31–49 (2002)

    Article  ADS  Google Scholar 

  17. Grace, J., Lloyd, J., Miranda, A. C., Miranda, H. & Gash, J. H. C. Fluxes of carbon dioxide and water vapour over a C-4 pasture in south-western Amazonia (Brazil). Aust. J. Plant Physiol. 25, 519–530 (1998)

    Google Scholar 

  18. Vourlitis, G. L. & Oechel, W. C. Eddy covariance measurements of CO2 and energy fluxes of an Alaskan tussock tundra ecosystem. Ecology 80, 686–701 (1999)

    Article  Google Scholar 

  19. Novick, K. A. et al. Carbon dioxide and water vapor exchange in a warm temperate grassland. Oecologia 138, 259–274 (2004)

    Article  ADS  CAS  Google Scholar 

  20. Saleska, S. R., Harte, J. & Torn, M. S. The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow. Glob. Change Biol. 5, 125–141 (1999)

    Article  ADS  Google Scholar 

  21. Rustad, L. E. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001)

    Article  ADS  CAS  Google Scholar 

  22. Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005)

    Article  ADS  CAS  Google Scholar 

  23. Reichstein, M. et al. Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis. Glob. Change Biol. 13, 634–651 (2007)

    Article  ADS  Google Scholar 

  24. Knapp, A. K., Briggs, J. M. & Koelliker, J. K. Frequency and extent of water limitation to primary production in a mesic temperate grassland. Ecosystems (N. Y., Print) 4, 19–28 (2001)

    Article  Google Scholar 

  25. Suyker, A. E., Verma, S. B. & Burba, G. G. Interannual variability in net CO2 exchange of a native tallgrass prairie. Glob. Change Biol. 9, 255–265 (2003)

    Article  ADS  Google Scholar 

  26. Schimel, D. S., Churkina, G., Braswell, B. H. & Trenbath, J. in A History of Atmospheric CO2 and its Effects on Plants, Animals and Ecosystems (eds Baldwin, I. T. et al.) 350–368 (Springer, 2005)

    Google Scholar 

Download references

Acknowledgements

We thank E. Kessler and the University of Oklahoma for the use of the Kessler Farm Field Laboratory; R. Kreidberg for editorial assistance; and J. Amthor, M. Bahn, C. Körner, D. Obrist and G. Wohlfahrt, for critical review of an early draft of this manuscript. This study was funded by the US National Science Foundation’s Integrated Research Challenges in Environmental Biology program, with additional support from the Desert Research Institute (DRI) for necessary upgrades to the EcoCELL facility. We are very grateful to DRI, the University of Oklahoma, and the University of Nevada–Reno teams for technical assistance, facilities support, and administrative expertise (also see Supplementary Information).

Author Contributions J.A.A. and P.S.J.V. headed up the study including leading proposal writing, project coordination, data interpretation and analysis, and manuscript preparation. P.S.J.V., R.L.J., J.D.L., D.E.S., J.A.A. and W.G.C. were directly involved in all aspects of the study on a day-to-day basis, with A.J.L., J.A.A., L.L.W. and R.A.S. focusing on plant community aspects; C.M.B. contributing to hydrological measurements; J.D.L. contributing to quantification of plant canopy dynamics; P.S.J.V. contributing particularly to measurements of soil CO2 fluxes and soil C and N; and D.W.J. contributing to estimation of soil nutrients. D.S.S., Y.L., B.H.B., J.S.C., P.S.J.V. and J.A.A. developed the idea for the research. C.v.N. built and managed the database for the project and contributed to data analyses. P.E.B. coordinated outreach activities to local schools and brought research to the communities of Reno and Las Vegas. R.L.J., J.D.L. and P.S.J.V. worked closely with J.A.A. on data analysis and manuscript preparation. All authors discussed the results and commented on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John A. Arnone III.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Text, Supplementary References, Supplementary Table 1 and Supplementary Figures 1-8 with Legends (PDF 6448 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arnone III, J., Verburg, P., Johnson, D. et al. Prolonged suppression of ecosystem carbon dioxide uptake after an anomalously warm year. Nature 455, 383–386 (2008). https://doi.org/10.1038/nature07296

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature07296

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