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The energetic and carbon economic origins of leaf thermoregulation

Nature Plants volume 2, Article number: 16129 (2016) Cite this article

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A Corrigendum to this article was published on 26 August 2016

Abstract

Leaf thermoregulation has been documented in a handful of studies, but the generality and origins of this pattern are unclear. We suggest that leaf thermoregulation is widespread in both space and time, and originates from the optimization of leaf traits to maximize leaf carbon gain across and within variable environments. Here we use global data for leaf temperatures, traits and photosynthesis to evaluate predictions from a novel theory of thermoregulation that synthesizes energy budget and carbon economics theories. Our results reveal that variation in leaf temperatures and physiological performance are tightly linked to leaf traits and carbon economics. The theory, parameterized with global averaged leaf traits and microclimate, predicts a moderate level of leaf thermoregulation across a broad air temperature gradient. These predictions are supported by independent data for diverse taxa spanning a global air temperature range of ∼60 °C. Moreover, our theory predicts that net carbon assimilation can be maximized by means of a trade-off between leaf thermal stability and photosynthetic stability. This prediction is supported by globally distributed data for leaf thermal and photosynthetic traits. Our results demonstrate that the temperatures of plant tissues, and not just air, are vital to developing more accurate Earth system models.

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Figure 1: Leaf thermal traits and the leaf economics spectrum.
Figure 2: Leaf thermoregulation across global air temperature gradients.
Figure 3: Relationship between T90 and τ.
Figure 4: Sensitivity of leaf thermal time constants τ to variation in seven constituent leaf traits.

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Acknowledgements

This paper is dedicated to the memory of Dr David M. Gates, who began studying the thermoregulation and energy budgets of leaves more than a half century ago. The authors thank B. Blonder for providing thoughtful comments on an earlier version of the paper, L. Stockton for helping collect leaf trait and gas exchange data, H. Adams, A. Collins, T. Dickman, C. Grossiord, A. Henderson, J. Reithel and S. Sevanto for providing meteorological and phenological data, and J. Finch and J. Draper for supplying the Brachypodium distachyon image used in Fig. 1. S.T.M. was supported by a Director's Fellowship from the Los Alamos National Laboratory. S.T.M., M.D.W., J.Z., M.K. and B.J.E. were supported by NSF MacroSystems award 1065861. B.R.H. was supported under NSF award IOS-0950998 and NSF MacroSystems award 1241873. N.G.M. was supported by SUMO and NGEE-Tropics support from the Department of Energy, Office of Science. B.J.E. was supported by a fellowship from the Aspen Center for Environmental Studies.

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Authors and Affiliations

  1. Earth and Environmental Sciences Division, Los Alamos National Laboratory, MS J495, Los Alamos, 87545, New Mexico, USA

    Sean T. Michaletz & Nate G. McDowell

  2. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, 85721, Arizona, USA

    Sean T. Michaletz & Brian J. Enquist

  3. Department of Biology, EEB Graduate Program, University of Oklahoma, Norman, 73069, Oklahoma, USA

    Michael D. Weiser & Michael Kaspari

  4. and Department of Microbiology and Plant Biology, Institute for Environmental Genomics, University of Oklahoma, Norman, 73019, Oklahoma, USA

    Jizhong Zhou

  5. State Key Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China

    Jizhong Zhou

  6. Earth Science Division, Lawrence Berkeley Laboratory, Berkeley, 94270, California, USA

    Jizhong Zhou

  7. Smithsonian Tropical Research Institute, Balboa, Republic of Panama

    Michael Kaspari

  8. Department of Biology, University of Pennsylvania, Philadelphia, 19104, Pennsylvania, USA

    Brent R. Helliker

  9. The Santa Fe Institute, 1399 Hyde Park Rd, Santa Fe, 87501, New Mexico, USA

    Brian J. Enquist

  10. The iPlant Collaborative, Thomas W. Keating Bioresearch Building, 1657 East Helen Street, Tucson, 85721, Arizona, USA

    Brian J. Enquist

  11. Aspen Center for Environmental Studies, 100 Puppy Smith Street, Aspen, 81611, Colorado, USA

    Brian J. Enquist

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Contributions

S.T.M., M.D.W., N.G.M., J.Z., M.K., B.R.H. and B.J.E. compiled data, developed theory, performed analyses and wrote the paper.

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Correspondence to Sean T. Michaletz.

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Additional theory, Supplementary references, Supplementary Figs 1-4 and Supplementary Tables 1-3. (PDF 786 kb)

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Michaletz, S., Weiser, M., McDowell, N. et al. The energetic and carbon economic origins of leaf thermoregulation. Nature Plants 2, 16129 (2016). https://doi.org/10.1038/nplants.2016.129

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