Abstract
The Earth’s carbon and hydrologic cycles are intimately coupled by gas exchange through plant stomata1,2,3. However, uncertainties in the magnitude4,5,6 and consequences7,8 of the physiological responses9,10 of plants to elevated CO2 in natural environments hinders modelling of terrestrial water cycling and carbon storage11. Here we use annually resolved long-term δ13C tree-ring measurements across a European forest network to reconstruct the physiologically driven response of intercellular CO2 (Ci) caused by atmospheric CO2 (Ca) trends. When removing meteorological signals from the δ13C measurements, we find that trees across Europe regulated gas exchange so that for one ppmv atmospheric CO2 increase, Ci increased by ∼0.76 ppmv, most consistent with moderate control towards a constant Ci/Ca ratio. This response corresponds to twentieth-century intrinsic water-use efficiency (iWUE) increases of 14 ± 10 and 22 ± 6% at broadleaf and coniferous sites, respectively. An ensemble of process-based global vegetation models shows similar CO2 effects on iWUE trends. Yet, when operating these models with climate drivers reintroduced, despite decreased stomatal opening, 5% increases in European forest transpiration are calculated over the twentieth century. This counterintuitive result arises from lengthened growing seasons, enhanced evaporative demand in a warming climate, and increased leaf area, which together oppose effects of CO2-induced stomatal closure. Our study questions changes to the hydrological cycle, such as reductions in transpiration and air humidity, hypothesized to result from plant responses to anthropogenic emissions.
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References
Cao, L., Bala, G., Caldeira, K., Nemani, R. & Ban-Weiss, G. Importance of carbon dioxide physiological forcing to future climate change. Proc. Natl Acad. Sci. USA 107, 9513–9518 (2010).
Schlesinger, W. H. & Jasechko, S. Transpiration in the global water cycle. Agric. Forest Meteorol. 189–190, 115–117 (2014).
Leuzinger, S. & Körner, C. Water savings in mature deciduous forest trees under elevated CO2 . Glob. Change Biol. 13, 2498–2508 (2007).
Saurer, M. et al. Spatial variability and temporal trends in water-use efficiency of European forests. Glob. Change Biol. 20, 3700–3712 (2014).
Marshall, J. D. & Monserud, R. A. Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105, 13–21 (1996).
Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013).
Koutavas, A. CO2 fertilization and enhanced drought resistance in Greek firs from Cephalonia Island, Greece. Glob. Change Biol. 19, 529–539 (2013).
van der Sleen, P. et al. No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nature Geosci. 8, 24–28 (2015).
Ainsworth, E. A. & Rogers, A. The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant Cell Environ. 30, 258–270 (2007).
Drake, B. G., Gonzàlez-Meler, M. A. & Long, S. P. More efficient plants: A consequence of rising atmospheric CO2? Annu. Rev. Plant Biol. 48, 609–639 (1997).
IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).
Jung, M. et al. Recent decline in the global land evapotranspiration trend due to limited moisture supply. Nature 467, 951–954 (2010).
Still, C. J., Berry, J. A., Collatz, G. J. & DeFries, R. S. Global distribution of C-3 and C-4 vegetation: Carbon cycle implications. Glob. Biogeochem. Cycle 17, 14 (2003).
Shevliakova, E. et al. Historical warming reduced due to enhanced land carbon uptake. Proc. Natl Acad. Sci. USA 110, 16730–16735 (2013).
Gedney, N. et al. Detection of a direct carbon dioxide effect in continental river runoff records. Nature 439, 835–838 (2006).
Betts, R. A. et al. Projected increase in continental runoff due to plant responses to increasing carbon dioxide. Nature 448, 1037–1041 (2007).
Medlyn, B. E. et al. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob. Change Biol. 17, 2134–2144 (2011).
Farquhar, G. D., Ehleringer, J. R. & Hubick, K. T. Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503–537 (1989).
Feng, X. H. Trends in intrinsic water-use efficiency of natural trees for the past 100–200 years: A response to atmospheric CO2 concentration. Geochim. Cosmochim. Acta 63, 1891–1903 (1999).
Treydte, K. et al. Signal strength and climate calibration of a European tree-ring isotope network. Geophys. Res. Lett. 34, L24302 (2007).
Peñuelas, J., Canadell, J. G. & Ogaya, R. Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Global Ecology Biogeography 20, 597–608 (2011).
Saurer, M., Siegwolf, R. T. W. & Schweingruber, F. H. Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Glob. Change Biol. 10, 2109–2120 (2004).
Niinemets, U., Flexas, J. & Penuelas, J. Evergreens favored by higher responsiveness to increased CO2 . Trends Ecol. Evol. 26, 136–142 (2011).
De Kauwe, M. G. et al. Forest water use and water use efficiency at elevated CO2: A model-data intercomparison at two contrasting temperate forest FACE sites. Glob. Change Biol. 19, 1759–1779 (2013).
Klein, T. et al. Association between tree-ring and needle δ13C and leaf gas exchange in Pinus halepensis under semi-arid conditions. Oecologia 144, 45–54 (2005).
Zhao, M. S. & Running, S. W. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940–943 (2010).
Piao, S. L. et al. Changes in climate and land use have a larger direct impact than rising CO2 on global river runoff trends. Proc. Natl Acad. Sci. USA 104, 15242–15247 (2007).
Sterling, S. M., Ducharne, A. & Polcher, J. The impact of global land-cover change on the terrestrial water cycle. Nature Clim. Change 3, 385–390 (2013).
Babst, F. et al. Site- and species-specific responses of forest growth to climate across the European continent. Glob. Ecol. Biogeogr. 22, 706–717 (2013).
Donohue, R. J., Roderick, M. L., McVicar, T. R. & Farquhar, G. D. Impact of CO2 fertilization on maximum foliage cover across the globe’s warm, arid environments. Geophys. Res. Lett. 40, 3031–3035 (2013).
Boettger, T., Haupt, M., Friedrich, M. & Waterhouse, J. S. Reduced climate sensitivity of carbon, oxygen and hydrogen stable isotope ratios in tree-ring cellulose of silver fir (Abies alba Mill.) influenced by background SO2 in Franconia (Germany, Central Europe). Environ. Pollut. 185, 281–294 (2014).
Holmes, C. D. Air pollution and forest water use. Nature 507, E1–E2 (2014).
Cowling, S. A. & Field, C. B. Environmental control of leaf area production: Implications for vegetation and land-surface modeling. Glob. Biogeochem. Cycle 17, 1007 (2003)10.1029/2002gb001915
Shongwe, M. E., Graversen, R. G., van Oldenborgh, G. J., van den Hurk, B. & Doblas-Reyes, F. J. Energy budget of the extreme Autumn 2006 in Europe. Clim. Dynam. 36, 1055–1066 (2011).
Cattiaux, J., Douville, H. & Peings, Y. European temperatures in CMIP5: Origins of present-day biases and future uncertainties. Clim. Dynam. 41, 2889–2907 (2013).
Acknowledgements
We thank C. Körner, S. Seneviratne, and A. Gessler for comments, the European Union projects ISONET (EVK2-2001-00237), Carbo-Extreme (226701) and Millennium (017008), the Swiss National Science Foundation (iTREE CRSII3_136295), and N.J.L. the UK NERC (NE/B501504) and C3W for funding.
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D.C.F., B.P., M. Saurer, J.E. and G.H.S. designed the study, with input from C.H., G.H. and N.E.Z. D.C.F., B.P. and M. Saurer performed the analyses with input from J.E., C.H. and G.H.S. All authors contributed to discussion, interpretation, and the development of the data set and ISONET program (devised by G.H.S., G.H. and N.J.L.) or the TRENDY model intercomparison project (coordinated by S.S. and P.F.). D.C.F., B.P. and C.H. led the writing of this paper.
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Frank, D., Poulter, B., Saurer, M. et al. Water-use efficiency and transpiration across European forests during the Anthropocene. Nature Clim Change 5, 579–583 (2015). https://doi.org/10.1038/nclimate2614
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DOI: https://doi.org/10.1038/nclimate2614
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