Abstract
Severe droughts in the Northern Hemisphere cause a widespread decline of agricultural yield, the reduction of forest carbon uptake, and increased CO2 growth rates in the atmosphere. Plants respond to droughts by partially closing their stomata to limit their evaporative water loss, at the expense of carbon uptake by photosynthesis. This trade-off maximizes their water-use efficiency (WUE), as measured for many individual plants under laboratory conditions and field experiments. Here we analyse the 13C/12C stable isotope ratio in atmospheric CO2 to provide new observational evidence of the impact of droughts on the WUE across areas of millions of square kilometres and spanning one decade of recent climate variability. We find strong and spatially coherent increases in WUE along with widespread reductions of net carbon uptake over the Northern Hemisphere during severe droughts that affected Europe, Russia and the United States in 2001–2011. The impact of those droughts on WUE and carbon uptake by vegetation is substantially larger than simulated by the land-surface schemes of six state-of-the-art climate models. This suggests that drought-induced carbon–climate feedbacks may be too small in these models and improvements to their vegetation dynamics using stable isotope observations can help to improve their drought response.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Monteith, J. L. Evaporation and environment. Proc. Soc. Exp. Biol. 19, 205–234 (1965).
Jarvis, P. G. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Phil. Trans. R. Soc. Lond. B 273, 593–610 (1976).
Teuling, A. J. et al. Contrasting response of European forest and grassland energy exchange to heatwaves. Nat. Geosci. 3, 722–727 (2010).
Buckley, T. N. The control of stomata by water balance. New Phytol. 168, 275–292 (2005).
Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013).
Swann, A. L. S. et al. Plant responses to increasing CO2 reduce estimates of climate impacts on drought severity. Proc. Natl Acad. Sci. USA 113, 10019–10024 (2016).
van der Sleen, P. et al. No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nat. Geosci. 8, 24–28 (2015).
Keeling, R. F. et al. Atmospheric evidence for a global secular increase in carbon isotopic discrimination of land photosynthesis. Proc. Natl Acad. Sci. USA 114, 10361–10366 (2017).
Frank, D. C. et al. Water-use efficiency and transpiration across European forests during the Anthropocene. Nat. Clim. Change 5, 579–583 (2015).
Medlyn, B. et al. How do leaf and ecosystem measures of water-use efficiency compare? New Phytol. 216, 758–770 (2017).
Reichstein, M. et al. Severe drought effects on ecosystem CO2 and H2O fluxes at three Mediterranean evergreen sites: revision of current hypotheses? Glob. Change Biol. 8, 999–1017 (2002).
Bowling, D. et al. Partitioning net ecosystem carbon exchange with isotopic fluxes of CO2. Glob. Change Biol. 7, 127–145 (2001).
Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).
Jung, M. et al. Compensatory water effects link yearly global land CO2 sink changes to temperature. Nature 541, 516–520 (2017).
Booth, B. B. et al. High sensitivity of future global warming to land carbon cycle processes. Env. Res. Lett. 7, 024002–024008 (2012).
Piao, S. et al. Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO2 trends. Glob. Change Biol. 19, 2117–2132 (2013).
Köhler, I. H. et al. Intrinsic water-use efficiency of temperate semi-natural grassland has increased since 1857: an analysis of carbon isotope discrimination of herbage from the Park Grass Experiment. Glob. Change Biol. 16, 1531–1541 (2010).
Farquhar, G. D. et al. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9, 121–137 (1982).
Ballantyne, A. P. et al. Apparent seasonal cycle in isotopic discrimination of carbon in the atmosphere and biosphere due to vapor pressure deficit. Glob. Biogeochem. Cyc. 24, GB3018 (2010).
van der Velde, I. R. et al. The CarbonTracker Data Assimilation System for CO2 and δ13C (CTDAS-C13 v1.0): retrieving Information on land–atmosphere exchange processes. Geosci. Model Dev. 11, 283–304 (2018).
Vicente-Serrano, S. M. et al. A multiscalar drought index sensitive to global warming: the Standardized Precipitation Evapotranspiration Index. J. Clim 23, 1696–1718 (2010).
Mekonnen, Z. A. et al. Carbon sources and sinks of North America as affected by major drought events during the past 30 Years. Agr. Forest Meteorol. 244–245, 42–56 (2017).
Schwalm, C. R. et al. Reduction in carbon uptake during turn of the century drought in western North America. Nat. Geosci. 5, 551–556 (2012).
Spinoni, J. et al. The biggest drought events in Europe from 1950 to 2012. J. Hydrol. Reg. Stud. 3, 509–524 (2015).
Yurganov, L. N. et al. Satellite- and ground-based CO total column observations over 2010 Russian fires: accuracy of top-down estimates based on thermal IR satellite data. Atm. Chem. Phys. 11, 7925–7942 (2011).
Krol, M. et al. How much CO was emitted by the 2010 fires around Moscow? Atm. Chem. Phys. 13, 4737–4747 (2013).
Luterbacher, J. et al. Exceptional European warmth of autumn 2006 and winter 2007: Historical context, the underlying dynamics, and its phenological impacts. Geophys. Res. Lett. 34, L12704 (2007).
Peters, W. et al. An atmospheric perspective on North American carbon dioxide exchange: CarbonTracker. Proc. Natl Acad. Sci. USA 104, 18925–18930 (2007).
Reichstein, M. et al. Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis. Glob. Change Biol. 13, 634–651 (2007).
Peters, W. et al. Seven years of recent European net terrestrial carbon dioxide exchange constrained by atmospheric observations. Glob. Change Biol. 16, 1317–1337 (2010).
Guerlet, S. et al. Reduced carbon uptake during the 2010 Northern Hemisphere summer from GOSAT. Geophys. Res. Lett. 40, 2378–2383 (2013).
Werner, C. et al. Linking carbon and water cycles using stable isotopes across scales: progress and challenges. Biogeosciences 9, 3083–3111 (2011).
Brüggemann, N. et al. Carbon allocation and carbon isotope fluxes in the plant–soil–atmosphere continuum: a review. Biogeosciences 8, 3457–3489 (2011).
van der Velde, I. R. et al. Biosphere model simulations of interannual variability in terrestrial 13C/12C exchange. Glob. Biogeochem. Cyc. 27, 637–649 (2013).
Farquhar, G. Models of integrated photosynthesis of cells and leaves. Phil. Trans. R. Soc. Lond. B 323, 357–367 (1989).
Baldocchi, D. An analytical solution for coupled leaf photosynthesis and stomatal conductance models. Tree Physiol. 14, 1069–1079 (1994).
Beer, C. et al. Temporal and among-site variability of inherent water use efficiency at the ecosystem level. Glob. Biogeochem. Cyc. 23, GB2018 (2009).
Mystakidis, S. et al. Hydrological and biogeochemical constraints on terrestrial carbon cycle feedbacks. Env. Res. Lett. 12, 014009–014020 (2017).
Taylor, K. E. et al. An overview of CMIP5 and the experiment design. Bull. Am. Meteorol. Soc. 93, 485–498 (2012).
Jones, C. D. et al. C4MIP—the Coupled Climate–Carbon Cycle Model Intercomparison Project: experimental protocol for CMIP6. Geosci. Model Dev. 9, 2853–2880 (2016).
Bodin, P. E. et al. Comparing the performance of different stomatal conductance models using modelled and measured plant carbon isotope ratios (δ¹³C): implications for assessing physiological forcing. Glob. Change Biol. 19, 1709–1719 (2013).
Miralles, D. et al. Mega-heatwave temperatures due to combined soil desiccation and atmospheric heat accumulation. Nat. Geosci. 7, 345–349 (2014).
De Kauwe, M. G. et al. Ideas and perspectives: how coupled Is the vegetation to the boundary layer? Biogeosciences 14, 4435–4453 (2017).
Zhou, S. et al. How should we model plant responses to drought? An analysis of stomatal and non-stomatal responses to water stress. Agr. Forest Meteorol. 182-183, 204–214 (2013).
Novick, K. A. et al. The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nat. Clim. Change 6, 1023–1027 (2016).
Egea, G. et al. Towards an improved and more flexible representation of water stress in coupled photosynthesis—stomatal conductance models. Agr. Forest Meteorol. 151, 1370–1384 (2011).
Green, J. K. et al. Regionally strong feedbacks between the atmosphere and terrestrial biosphere. Nat. Geosci. 10, 410–414 (2017).
Wang, H. et al. Towards a universal model for carbon dioxide uptake by plants. Nat. Plants 3, 734–741 (2017).
Ukkola, A. M. et al. Land surface models systematically overestimate the intensity, duration and magnitude of seasonal-scale evaporative droughts. Env. Res. Lett. 11, 104012–104023 (2016).
Wendeberg, M. et al. Jena Reference Air Set (JRAS): a multi-point scale anchor for isotope measurements of CO2 in air. Atm. Meas. Tech. 6, 817–822 (2013).
Seibt, U. et al. Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155, 441–454 (2008).
Ciais, P. et al. Partitioning of ocean and land uptake of CO2 as inferred by δ¹³C measurements from the NOAA Climate Monitoring and Diagnostics Laboratory Global Air Sampling Network. J. Geophys. Res. 100, 5051–5070 (1995).
Rayner, P. J. et al. Interannual variability of the global carbon cycle (1992–2005) inferred by inversion of atmospheric CO2 and δ13CO2 measurements. Glob. Biogeochem. Cyc. 22, GB3008 (2008).
Acknowledgements
This work used eddy covariance data acquired by the FLUXNET community. We acknowledge the financial support to the eddy covariance data harmonization provided by CarboEuropeIP, FAO-GTOS-TCO, iLEAPS, Max Planck Institute for Biogeochemistry, National Science Foundation, University of Tuscia, Université Laval and Environment Canada, and US Department of Energy and the database development and technical support from Berkeley Water Center, Lawrence Berkeley National Laboratory, Microsoft Research eScience, Oak Ridge National Laboratory, University of California Berkeley, University of Virginia. Ru-Fyo data were provided by A. Varlagin and J. Kurbatova from the Russian Academy of Sciences. C. Montzka is acknowledged for providing a SoilGrids-ROSETTA-based set of soil-hydraulic properties for the JULES modelling effort. We thank J. C. Lin and B. M. Raczka for their contributions to the CLM4.5 work. We thank S. E. Michel (INSTAAR) for the QA/QC of the δ¹³C data used in this study. C. Rödenbeck is acknowledged for providing additional information on gross ocean exchange. I.R.vdV. was financially supported by the Netherlands Organization for Scientific Research (NWO-VIDI 864.08.012) and by the National Computing Facilities Foundation (NCF project SH-060) for the use of supercomputing facilities. H.F.D. was supported by the US Department of Energy’s Office of Science, Terrestrial Ecosystem Science Program (award no. DE-SC0010624), and by the NASA CMS Project (award no. NNX16AP33G). P.L.V. was supported by the UK Natural Environment Research Council (NERC) funding of the National Centre for Atmospheric Science (NCAS). A.V. and P.L.V. were supported by the NERC project IMPETUS (ref. NE/L010488/1). W.P. and E.vS. received financial support from the European Research Council’s project ASICA (CoG 649087). We thank the NOAA Climate Program Office’s Atmospheric Chemistry, Carbon Cycle, and Climate (AC4) program for support, including that for the collection and analysis of CO2 and δ¹³C observations used in this study. We thank P. R. Rayner for very helpful comments on the manuscript.
Author information
Authors and Affiliations
Contributions
W.P., I.R.vdV. and J.B.M. designed the study. I.R.vdV., K.S., W.P., E.vS., I.T.vdL.-L., P.L.V., A.V., P.C., D.W., M.S., D.Z., H.F.D. and M.K.vdM. built the inverse and forward modelling frameworks. P.P.T., B.V. and J.W.C.W. were responsible for the δ¹³C and CO2 measurement programme. W.P., I.R.vdV. and E.vS. performed the analysis and wrote the main text. All the authors provided input to the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Peters, W., van der Velde, I.R., van Schaik, E. et al. Increased water-use efficiency and reduced CO2 uptake by plants during droughts at a continental scale. Nature Geosci 11, 744–748 (2018). https://doi.org/10.1038/s41561-018-0212-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41561-018-0212-7