Letter | Published:

Net carbon uptake has increased through warming-induced changes in temperate forest phenology

Nature Climate Change volume 4, pages 598604 (2014) | Download Citation


The timing of phenological events exerts a strong control over ecosystem function and leads to multiple feedbacks to the climate system1. Phenology is inherently sensitive to temperature (although the exact sensitivity is disputed2) and recent warming is reported to have led to earlier spring, later autumn3,4 and increased vegetation activity5,6. Such greening could be expected to enhance ecosystem carbon uptake7,8, although reports also suggest decreased uptake for boreal forests4,9. Here we assess changes in phenology of temperate forests over the eastern US during the past two decades, and quantify the resulting changes in forest carbon storage. We combine long-term ground observations of phenology, satellite indices, and ecosystem-scale carbon dioxide flux measurements, along with 18 terrestrial biosphere models. We observe a strong trend of earlier spring and later autumn. In contrast to previous suggestions4,9 we show that carbon uptake through photosynthesis increased considerably more than carbon release through respiration for both an earlier spring and later autumn. The terrestrial biosphere models tested misrepresent the temperature sensitivity of phenology, and thus the effect on carbon uptake. Our analysis of the temperature–phenology–carbon coupling suggests a current and possible future enhancement of forest carbon uptake due to changes in phenology. This constitutes a negative feedback to climate change, and is serving to slow the rate of warming.

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This research was supported by the NOAA Climate Program Office, Global Carbon Cycle Program (award NA11OAR4310054) and the Office of Science (BER), US Department of Energy. T.F.K. acknowledges support from a Macquarie University Research Fellowship. A.D.R. acknowledges additional support from the National Science Foundation’s Marcrosystem Biology program (grant EF-1065029). M.A.F. gratefully acknowledges support from NASA grant number NNX11AE75G S01. G.B. acknowledges the National Science Foundation’s grant DEB-0911461. We thank all those involved in the NACP Site Synthesis, in particular the modelling teams who provided model output. Research at the Bartlett Experimental Forest tower is supported by the National Science Foundation (grant DEB-1114804) and the USDA Forest Service’s Northern Research Station. Research at Howland Forest is supported by the Office of Science (BER), US Department of Energy. Carbon flux and biometric measurements at Harvard Forest have been supported by the Office of Science (BER), US Department of Energy (DOE) and the National Science Foundation Long-Term Ecological Research Programs. Hubbard Brook phenology data were provided by A. Bailey at the USDA Forest Service, Northern Research Station, Hubbard Brook Experimental Forest. We thank D. Dragoni for useful comments on an earlier version of the manuscript.

Author information


  1. Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia

    • Trevor F. Keenan
  2. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Trevor F. Keenan
    • , Michael Toomey
    •  & Andrew D. Richardson
  3. Department of Earth and Environment, Boston University, Boston, Massachusetts 02215, USA

    • Josh Gray
    • , Mark A. Friedl
    •  & Ian Sue Wing
  4. Department of Civil, Environmental & Geodetic Eng., The Ohio State University, Columbus, Ohio 43210, USA

    • Gil Bohrer
  5. USDA Forest Service, Northern Research Station, Durham, New Hampshire 03824, USA

    • David Y. Hollinger
  6. School of Engineering and Applied Sciences and Department of Earth and Planetary Sciences, Harvard University, Cambridge, Massachusetts 02138, USA

    • J. William Munger
  7. Harvard Forest, Petersham, Massachusetts 01366, USA

    • John O’Keefe
  8. Inst. of Meteorology and Climate Research, Karlsruhe Institute of Technology, IMK-IFU, Garmisch-Partenkirchen 82467, Germany

    • Hans Peter Schmid
  9. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA

    • Bai Yang


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T.F.K. and A.D.R. designed the study and are responsible for the integrity of the manuscript. A.D.R. planned the flux data analysis, with input from D.Y.H., J.W.M., G.B., H.P.S. and D.D. A.D.R., D.Y.H., J.W.M., G.B., H.P.S., B.Y., J.G., M.T. and J.O.K. contributed data. T.F.K. compiled the data sets, and detailed and performed the analysis. M.A.F., I.S.W. and J.G. performed the panel analysis. T.F.K. led the writing, with input from all other authors. All authors discussed and commented on the results and the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Trevor F. Keenan.

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