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

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 rate of warming.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agricult. For. Meteorol. 169, 156–173 (2013).

  2. 2.

    et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497 (2012).

  3. 3.

    , , , & Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386, 698–702 (1997).

  4. 4.

    et al. Large-scale variations in the vegetation growing season and annual cycle of atmospheric CO2 at high northern latitudes from 1950 to 2011. Glob. Change Biol. 19, 3167–3183 (2013).

  5. 5.

    et al. Temperature and vegetation seasonality diminishment over northern lands. Nature Clim. Change 3, 581–586 (2013).

  6. 6.

    et al. Enhanced seasonal exchange of CO2 by northern ecosystems since 1960. Science 341, 1085–1089 (2013).

  7. 7.

    , , & Spatial analysis of growing season length control over net ecosystem exchange. Glob. Change Biol. 11, 1777–1787 (2005).

  8. 8.

    et al. Evidence of increased net ecosystem productivity associated with a longer vegetated season in a deciduous forest in south-central Indiana, USA. Glob. Change Biol. 17, 886–897 (2011).

  9. 9.

    et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–52 (2008).

  10. 10.

    et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 365, 3227–3246 (2010).

  11. 11.

    Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (ed Stocker, T. F.et al.) (Cambridge Univ. Press, 2013).

  12. 12.

    & Phenological data series of cherry tree flowering in Kyoto, Japan, and its application to reconstruction of springtime temperatures since the 9th century. Int. J. Climatol. 914, 905–914 (2008).

  13. 13.

    , & The impact of climate change on cherry trees and other species in Japan. Biol. Conserv. 142, 1943–1949 (2009).

  14. 14.

    & Is spring starting earlier? The Holocene 18, 95–104 (2008).

  15. 15.

    & Global warming and flowering times in Thoreau’s Concord: A community perspective. Ecology 89, 332–341 (2008).

  16. 16.

    , , & Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982–2008. Glob. Change Biol. 17, 2385–2399 (2011).

  17. 17.

    et al. Spring phenology in boreal Eurasia over a nearly century time scale. Glob. Change Biol. 14, 603–614 (2008).

  18. 18.

    & Latitudinal patterns in the phenological responses of leaf colouring and leaf fall to climate change in Japan. Glob. Ecol. Biogeogr. 17, 556–561 (2008).

  19. 19.

    & Trends in fall phenology across the deciduous forests of the Eastern USA. Agricult. For. Meteorol. 157, 96–105 (2012).

  20. 20.

    , , , & Land surface phenology from MODIS: Characterization of the Collection 5 global land cover dynamics product. Remote Sens. Environ. 114, 1805–1816 (2010).

  21. 21.

    et al. A comparison of multiple phenology data sources for estimating seasonal transitions in deciduous forest carbon exchange. Agricult. For. Meteorol. 151, 1741–1752 (2011).

  22. 22.

    et al. Trend change detection in NDVI time series: Effects of inter-annual variability and methodology. Remote Sens. 5, 2113–2144 (2013).

  23. 23.

    , , & Predicting climate change impacts on the amount and duration of autumn colors in a New England forest. PLoS One 8, e57373 (2013).

  24. 24.

    , , , & Shifting plant phenology in response to global change. Trends Ecol. Evol. 22, 357–365 (2007).

  25. 25.

    et al. Terrestrial biosphere models need better representation of vegetation phenology: Results from the North American Carbon Program Site Synthesis. Glob. Change Biol. 18, 566–584 (2012).

  26. 26.

    et al. Terrestrial biosphere model performance for inter-annual variability of land-atmosphere CO2 exchange. Glob. Change Biol. 18, 1971–1987 (2012).

  27. 27.

    , , , & Increase in observed net carbon dioxide uptake by land and oceans during the past 50 years. Nature 488, 70–72 (2012).

  28. 28.

    et al. Ecological impacts of a widespread frost event following early spring leaf-out. Glob. Change Biol. 18, 2365–2377 (2012).

  29. 29.

    Why does phenology drive species distribution? Phil. Trans. R. Soc. Lond. B. Biol. Sci. 365, 3149–3160 (2010).

  30. 30.

    , , , & Earlier springs decrease peak summer productivity in North American boreal forests. Environ. Res. Lett. 8, 024027 (2013).

  31. 31.

    , , , & Phenology of a northern hardwood forest canopy. Glob. Change Biol. 12, 1174–1188 (2006).

  32. 32.

    et al. Cross-site evaluation of eddy covariance GPP and RE decomposition techniques. Agricult. For. Meteorol. 148, 821–838 (2008).

  33. 33.

    , , & Landscape controls on the timing of spring, autumn, and growing season length in mid-Atlantic forests. Glob. Change Biol. 18, 656–674 (2012).

  34. 34.

    Analysis of panel data (Cambridge University Press, 2003).

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

Affiliations

  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

Authors

  1. Search for Trevor F. Keenan in:

  2. Search for Josh Gray in:

  3. Search for Mark A. Friedl in:

  4. Search for Michael Toomey in:

  5. Search for Gil Bohrer in:

  6. Search for David Y. Hollinger in:

  7. Search for J. William Munger in:

  8. Search for John O’Keefe in:

  9. Search for Hans Peter Schmid in:

  10. Search for Ian Sue Wing in:

  11. Search for Bai Yang in:

  12. Search for Andrew D. Richardson in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Trevor F. Keenan.

Supplementary information

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nclimate2253

Further reading

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