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

ABSTRACT 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

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Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS INCREASED CARBON ASSIMILATION AND EFFICIENT WATER USAGE MAY NOT COMPENSATE FOR CARBON LOSS IN EUROPEAN FORESTS Article Open

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University Press, 2003). Book  Google Scholar  Download references ACKNOWLEDGEMENTS 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 AUTHORS AND AFFILIATIONS * Department

of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia Trevor F. Keenan * Department of Organismic and Evolutionary Biology, Harvard University, Cambridge,

Massachusetts 02138, USA Trevor F. Keenan, Michael Toomey & Andrew D. Richardson * Department of Earth and Environment, Boston University, Boston, Massachusetts 02215, USA Josh Gray, 

Mark A. Friedl & Ian Sue Wing * Department of Civil, Environmental & Geodetic Eng., The Ohio State University, Columbus, Ohio 43210, USA Gil Bohrer * USDA Forest Service, Northern

Research Station, Durham, New Hampshire 03824, USA David Y. Hollinger * School of Engineering and Applied Sciences and Department of Earth and Planetary Sciences, Harvard University,

Cambridge, Massachusetts 02138, USA J. William Munger * Harvard Forest, Petersham, Massachusetts 01366, USA John O’Keefe * Inst. of Meteorology and Climate Research, Karlsruhe Institute of

Technology, IMK-IFU, Garmisch-Partenkirchen 82467, Germany Hans Peter Schmid * Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA Bai

Yang Authors * Trevor F. Keenan View author publications You can also search for this author inPubMed Google Scholar * Josh Gray View author publications You can also search for this author

inPubMed Google Scholar * Mark A. Friedl View author publications You can also search for this author inPubMed Google Scholar * Michael Toomey View author publications You can also search

for this author inPubMed Google Scholar * Gil Bohrer View author publications You can also search for this author inPubMed Google Scholar * David Y. Hollinger View author publications You

can also search for this author inPubMed Google Scholar * J. William Munger View author publications You can also search for this author inPubMed Google Scholar * John O’Keefe View author

publications You can also search for this author inPubMed Google Scholar * Hans Peter Schmid View author publications You can also search for this author inPubMed Google Scholar * Ian Sue

Wing View author publications You can also search for this author inPubMed Google Scholar * Bai Yang View author publications You can also search for this author inPubMed Google Scholar *

Andrew D. Richardson View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS 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. CORRESPONDING AUTHOR Correspondence to Trevor F. Keenan. ETHICS DECLARATIONS COMPETING INTERESTS The

authors declare no competing financial interests. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION (PDF 16915 KB) RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE

THIS ARTICLE Keenan, T., Gray, J., Friedl, M. _et al._ Net carbon uptake has increased through warming-induced changes in temperate forest phenology. _Nature Clim Change_ 4, 598–604 (2014).

https://doi.org/10.1038/nclimate2253 Download citation * Received: 28 October 2013 * Accepted: 17 April 2014 * Published: 01 June 2014 * Issue Date: July 2014 * DOI:

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