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

Nature Climate Change volume 4, pages 598–604 (2014)Cite this article

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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.

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Figure 1: Long-term changes in satellite-derived spring phenology.
Figure 2: Long-term changes in ground observations of spring phenology.
Figure 3: The relationship between phenology and carbon fluxes.
Figure 4: Decadal trends in carbon cycling.
Figure 5: The temperature sensitivity of spring and autumn phenology.

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References

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  4. Barichivich, J. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Churkina, G., Schimel, D., Braswell, B. H. & Xiao, X. Spatial analysis of growing season length control over net ecosystem exchange. Glob. Change Biol. 11, 1777–1787 (2005).

    Article  Google Scholar 

  8. Dragoni, D. 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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Richardson, A. D. 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).

    Article  Google Scholar 

  11. IPCC, 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. Aono, Y. & Kazui, K. 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).

    Article  Google Scholar 

  13. Primack, R. B., Higuchi, H. & Miller-Rushing, A. J. The impact of climate change on cherry trees and other species in Japan. Biol. Conserv. 142, 1943–1949 (2009).

    Article  Google Scholar 

  14. Thompson, R. & Clark, R. M. Is spring starting earlier? The Holocene 18, 95–104 (2008).

    Article  Google Scholar 

  15. Miller-Rushing, A. J. & Primack, R. B. Global warming and flowering times in Thoreau’s Concord: A community perspective. Ecology 89, 332–341 (2008).

    Article  Google Scholar 

  16. Jeong, S-J., Ho, C-H., Gim, H-J. & Brown, M. E. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  20. Ganguly, S., Friedl, M. A., Tan, B., Zhang, X. & Verma, M. Land surface phenology from MODIS: Characterization of the Collection 5 global land cover dynamics product. Remote Sens. Environ. 114, 1805–1816 (2010).

    Article  Google Scholar 

  21. Garrity, S. R. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  23. Archetti, M., Richardson, A. D., O’Keefe, J. & Delpierre, N. Predicting climate change impacts on the amount and duration of autumn colors in a New England forest. PLoS One 8, e57373 (2013).

    Article  CAS  Google Scholar 

  24. Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. a & Schwartz, M. D. Shifting plant phenology in response to global change. Trends Ecol. Evol. 22, 357–365 (2007).

    Article  Google Scholar 

  25. Richardson, A. D. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  27. Ballantyne, A. P., Alden, C. B., Miller, J. B., Tans, P. P. & White, J. W. C. Increase in observed net carbon dioxide uptake by land and oceans during the past 50 years. Nature 488, 70–72 (2012).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  30. Buermann, W., Bikash, P. R., Jung, M., Burn, D. H. & Reichstein, M. Earlier springs decrease peak summer productivity in North American boreal forests. Environ. Res. Lett. 8, 024027 (2013).

    Article  Google Scholar 

  31. Richardson, A. D., Bailey, A. S., Denny, E. G., Martin, C. W. & O’Keefe, J. Phenology of a northern hardwood forest canopy. Glob. Change Biol. 12, 1174–1188 (2006).

    Article  Google Scholar 

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

    Article  Google Scholar 

  33. Elmore, A. J., Guinn, S. M., Minsley, B. J. & Richardson, A. D. Landscape controls on the timing of spring, autumn, and growing season length in mid-Atlantic forests. Glob. Change Biol. 18, 656–674 (2012).

    Article  Google Scholar 

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

    Book  Google Scholar 

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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.

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Authors and 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

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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.

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Correspondence to Trevor F. Keenan.

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The authors declare no competing financial interests.

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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

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