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Empirical evidence for resilience of tropical forest photosynthesis in a warmer world

Nature Plants volume 6, pages 1225–1230 (2020)Cite this article

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Abstract

Tropical forests may be vulnerable to climate change1,2,3 if photosynthetic carbon uptake currently operates near a high temperature limit4,5,6. Predicting tropical forest function requires understanding the relative contributions of two mechanisms of high-temperature photosynthetic declines: stomatal limitation (H1), an indirect response due to temperature-associated changes in atmospheric vapour pressure deficit (VPD)7, and biochemical restrictions (H2), a direct temperature response8,9. Their relative control predicts different outcomes—H1 is expected to diminish with stomatal responses to future co-occurring elevated atmospheric [CO2], whereas H2 portends declining photosynthesis with increasing temperatures. Distinguishing the two mechanisms at high temperatures is therefore critical, but difficult because VPD is highly correlated with temperature in natural settings. We used a forest mesocosm to quantify the sensitivity of tropical gross ecosystem productivity (GEP) to future temperature regimes while constraining VPD by controlling humidity. We then analytically decoupled temperature and VPD effects under current climate with flux-tower-derived GEP trends in situ from four tropical forest sites. Both approaches showed consistent, negative sensitivity of GEP to VPD but little direct response to temperature. Importantly, in the mesocosm at low VPD, GEP persisted up to 38 °C, a temperature exceeding projections for tropical forests in 2100 (ref. 10). If elevated [CO2] mitigates VPD-induced stomatal limitation through enhanced water-use efficiency as hypothesized9,11, tropical forest photosynthesis may have a margin of resilience to future warming.

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Fig. 1: Air temperature distributions recorded at the B2-TF mesocosm, a seasonally dry tropical forest (Tesopaco) and Amazon forest sites (K34, K67 and K83).
Fig. 2: Relative to in situ tropical forests, VPD is reduced at high temperatures in the B2-TF by maintaining high humidity.
Fig. 3: GEP is sustained to higher temperatures in the B2-TF than in in situ tropical forests, whereas all forests respond similarly to VPD.
Fig. 4: VPD has a negative effect on tropical forest GEP, while air temperature has a positive effect or no effect.

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Data availability

The datasets analysed in this study (eddy flux and environmental data) are available at https://daac.ornl.gov/cgi-bin/dsviewer.pl?ds_id=1174 (for K34 and K83) and https://ameriflux.lbl.gov/sites/siteinfo/BR-Sa1 (for K67). The datasets for Tesopaco and the B2-TF are available at https://github.com/m-n-smith/B2-temp-paper-datasets.

Code availability

The R code used to conduct the analyses presented in this paper is available upon request from the corresponding authors.

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Acknowledgements

We thank E. A. Yepez and J. Garatuza-Payan for providing the Tesopaco eddy flux data and J. Berry for the leaf-level chlorophyll fluorescence measurements, collected at B2 in collaboration with J.A. We thank M. Strangstalien, B. Enquist and A. Swann for useful comments on the manuscript. This work was supported by the National Science Foundation’s (NSF) Partnerships for International Research and Education (PIRE) (no. OISE-0730305) and the Philecological Foundation, with additional support from the US Department of Energy (DOE) (GOAmazon award no. 3002937712), the National Aeronautics and Space Administration (NASA) (LBA-DMIP project, award no. NNX09AL52G) and the University of Arizona’s Agnese Nelms Haury Program in Environment and Social Justice. M.N.S. and J.W. were supported by the NASA Earth and Space Science Fellowship (NESSF) program (grant no. NNX14AK95H). In addition, J.W. was partly supported by the DOE’s next-generation ecosystem experiments project in the tropics (NGEE-Tropics) at Brookhaven National Laboratory. T.C.T. was supported by the NSF Division of Biological Infrastructure with grant no. NSF‐PRFB‐1711997. The meteorological data collection and quality control analysis of the B2-TF dataset by R.R. were also supported by the NESSF program (grant no. NNX09AO33H) and the UK National Environment Research Council (NERC, grant nos NE/M003086/1 and NE/R004897/1).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA

    Marielle N. Smith, Tyeen C. Taylor, Natalia Restrepo-Coupe & Scott R. Saleska

  2. Department of Forestry, Michigan State University, East Lansing, MI, USA

    Marielle N. Smith

  3. Department of Civil and Environmental Engineering, University of Michigan, Ann Arbor, MI, USA

    Tyeen C. Taylor

  4. Biosphere 2, University of Arizona, Oracle, AZ, USA

    Joost van Haren & John Adams

  5. Department of Civil Engineering, University of Bristol, Bristol, UK

    Rafael Rosolem

  6. Cabot Institute, University of Bristol, Bristol, UK

    Rafael Rosolem

  7. School of Life Sciences, University of Technology Sydney, Sydney, New South Wales, Australia

    Natalia Restrepo-Coupe

  8. School of Biological Sciences, The University of Hong Kong, Pokfulam, China

    Jin Wu

  9. Embrapa Amazônia Oriental, Santarém, Brazil

    Raimundo C. de Oliveira

  10. Department of Environmental Physics, University of Western Pará (UFOPA), Santarém, Brazil

    Rodrigo da Silva

  11. Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil

    Alessandro C. de Araujo

  12. Embrapa Amazônia Oriental, Belém, Brazil

    Alessandro C. de Araujo

  13. Laboratório de Ecologia Isotópica, Centro de Energia Nuclear na Agricultura (CENA), Universidade de São Paulo, Piracicaba, Brazil

    Plinio B. de Camargo

  14. Ecology and Evolutionary Biology & Center for Environmental Biology, University of California, Irvine, CA, USA

    Travis E. Huxman

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Contributions

M.N.S., T.C.T., S.R.S. and T.E.H. conceived the study, designed the analyses and led the data interpretation, with extensive help from J.v.H. and R.R. M.N.S. performed the data analysis and drafted the manuscript, with substantial input from T.C.T., S.R.S. and T.E.H. R.R. provided the carbon exchange data for the B2-TF and advice on its analysis. N.R.-C., R.C.d.O., R.d.S., A.C.d.A., P.B.d.C. and S.R.S. contributed to the installation, maintenance or analysis of the eddy flux data from the LBA tower sites. J.W. provided advice on the binned regression analysis. J.A. collected and analysed the leaf-level chlorophyll fluorescence measurements in the B2-TF. All authors contributed to writing the final manuscript.

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Correspondence to Marielle N. Smith or Scott R. Saleska.

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Peer review information Nature Plants thanks Molly Cavaleri and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Notes 1–3, Figs. 1–6 and references.

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Smith, M.N., Taylor, T.C., van Haren, J. et al. Empirical evidence for resilience of tropical forest photosynthesis in a warmer world. Nat. Plants 6, 1225–1230 (2020). https://doi.org/10.1038/s41477-020-00780-2

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