Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Water limitation regulates positive feedback of increased ecosystem respiration

Abstract

Terrestrial ecosystem respiration increases exponentially with temperature, constituting a positive feedback loop accelerating global warming. However, the response of ecosystem respiration to temperature strongly depends on water availability, yet where and when the water effects are important, is presently poorly constrained, introducing uncertainties in climate–carbon cycle feedback projections. Here, we disentangle the effects of temperature and precipitation (a proxy for water availability) on ecosystem respiration by analysing eddy covariance CO2 flux measurements across 212 globally distributed sites. We reveal a threshold precipitation function, determined by the balance between precipitation and ecosystem water demand, which separates temperature-limited and water-limited respiration. Respiration is temperature limited for precipitation above that threshold function, whereas in drier areas water limitation reduces the temperature sensitivity of respiration and its positive feedback to global warming. If the trend of expansion of water-limited areas with warming climate over the last decades continues, the positive feedback of ecosystem respiration is likely to be weakened and counteracted by the increasing water limitation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The statistical performance of models of ecosystem respiration (Re) as a function of mean annual temperature (T) and precipitation (P), Re(T) and Re(P).
Fig. 2: Comparative threshold functions for mean temperature (T) or mean precipitation (P) regulation of ecosystem respiration (Re).

Similar content being viewed by others

Data availability

All data used for this study are publicly accessible and downloadable and all results of this study can be reproduced according to the methods provided. The FLUXNET2015 dataset used here are publicly available at https://fluxnet.org/data/fluxnet2015-dataset/. The CMIP6 data are publicly available at https://esgf-node.llnl.gov/projects/cmip6/. Information on the 212 sites used in this paper and their groupings are available on GitHub (https://github.com/chuixiangyi/Water-limitation).

Code availability

The Matlab code used for the analysis is available on GitHub (https://github.com/chuixiangyi/).

References

  1. The Intergovernmental Panel on Climate Change. Climate Change 2021: The Physical Science Basis (eds Masson-Delmotte, V. et al.) (Cambridge Univ. Press, 2021).

  2. Lloyd, J. & Taylor, J. On the temperature dependence of soil respiration. Funct. Ecol. 8, 315–323 (1994).

    Article  Google Scholar 

  3. van’t Hoff, J. H. Lectures on Theoretical and Physical Chemistry; Part 1 Chemical Dynamics (Edward Arnold, 1898).

  4. Tjoelker, M. G., Oleksyn, J. & Reich, P. B. Modelling respiration of vegetation: evidence for a temperature-dependent Q10. Glob. Change Biol. 7, 223–330 (2001).

    Article  Google Scholar 

  5. Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000).

    Article  CAS  PubMed  Google Scholar 

  6. Barford, C. C. et al. Factors controlling long- and short-term sequestration of atmospheric CO2 in a mid-latitude forest. Science 294, 1688–1691 (2001).

    Article  CAS  PubMed  Google Scholar 

  7. Niu, B. et al. Warming homogenizes apparent temperature sensitivity of ecosystem respiration. Sci. Adv. 7, 15 (2021).

    Article  Google Scholar 

  8. Johnston, A. S. A. et al. Temperature thresholds of ecosystem respiration at a global scale. Nat. Ecol. Evol. 5, 487–494 (2021).

    Article  PubMed  Google Scholar 

  9. Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Nature 540, 104–108 (2016).

    Article  CAS  PubMed  Google Scholar 

  10. Fan, N. et al. Global apparent temperature sensitivity of terrestrial carbon turnover modulated by hydrometeorological factors. Nat. Geosci. 15, 989–994 (2022).

    Article  CAS  Google Scholar 

  11. Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).

    Article  CAS  Google Scholar 

  12. Wieder, W. R., Bonan, G. B. & Allison, S. D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change 3, 909–912 (2013).

    Article  CAS  Google Scholar 

  13. Tang, J. & Riley, W. J. Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat. Clim. Change 5, 56–60 (2015).

    Article  CAS  Google Scholar 

  14. Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).

    Article  PubMed  Google Scholar 

  15. Giardina, C. P. & Ryan, M. G. Evidence that decomposition rates of organic matter in mineral soil do not vary with temperature. Nature 404, 858–861 (2000).

    Article  CAS  PubMed  Google Scholar 

  16. Davidson, E. A., Trumbore, S. E. & Amundson, R. Soil warming and organic carbon content. Nature 408, 789–790 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Knorr, W., Prentice, I., House, J. & Holland, E. Long-term sensitivity of soil carbon turnover to warming. Nature 433, 298–301 (2005).

    Article  CAS  PubMed  Google Scholar 

  18. Bradford, M. A. et al. Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Change 6, 751–758 (2016).

    Article  Google Scholar 

  19. Luo, Y., Wan, S., Hui, D. & Wallace, L. L. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413, 622–625 (2001).

    Article  CAS  PubMed  Google Scholar 

  20. Mahecha, M. D. et al. Global convergence in the temperature sensitivity of respiration at ecosystem level. Science 329, 838–840 (2010).

    Article  CAS  PubMed  Google Scholar 

  21. Reichstein, M. et al. Modeling temporal and large-scale spatial variability of soil respiration from soil water availability, temperature and vegetation productivity indices. Glob. Biogeochem. Cycles 17, 15.1–15.15 (2003).

    Article  Google Scholar 

  22. Raich, J. W. et al. Potential net primary productivity in South America: application of a global model. Ecol. Appl. 1-4, 399–429 (1991).

    Article  Google Scholar 

  23. Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    Article  CAS  PubMed  Google Scholar 

  24. Davidson, E. A., Janssens, I. A. & Luo, Y. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob. Change Biol. 12, 154–164 (2006).

    Article  Google Scholar 

  25. Yvon-Durocher, G. et al. Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487, 472–476 (2012).

    Article  CAS  PubMed  Google Scholar 

  26. Kirschbaum, M. U. F. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob. Change Biol. 10, 1870–1877 (2004).

    Article  Google Scholar 

  27. Atkin, O. K. & Tjoelker, M. G. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci. 8, 343–351 (2003).

    Article  CAS  PubMed  Google Scholar 

  28. Pastorello, G. et al. The FLUXNET2015 dataset and the ONEFlux processing pipeline for eddy covariance data. Sci. Data 7, 225 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hashimoto, S. et al. Global spatiotemporal distribution of soil respiration modeled using a global database. Biogeosciences 12, 4121–4132 (2015).

    Article  Google Scholar 

  30. Du, Y. et al. The response of soil respiration to precipitation change is asymmetric and differs between grasslands and forests. Glob. Change Biol. 26, 6015–6024 (2020).

    Article  Google Scholar 

  31. Liu, W., Zhang, Z. & Wan, S. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob. Change Biol. 15, 184–195 (2009).

    Article  Google Scholar 

  32. Yi, C. & Jackson, N. A review of measuring ecosystem resilience to disturbance. Environ. Res. Lett. 16, 053008 (2021).

    Article  Google Scholar 

  33. Jaramillo, F., Prieto, C., Lyon, S. W. & Destouni, G. Multimethod assessment of evapotranspiration shifts due to non-irrigated agricultural development in Sweden. J. Hydrol. 484, 55–62 (2013).

    Article  Google Scholar 

  34. Langbein, W. B. Annual Runoff in the United States (USGS, 1949).

  35. Jaramillo, F. & Destouni, G. Local flow regulation and irrigation raise global human water consumption and footprint. Science 350, 1248–1251 (2015).

    Article  CAS  PubMed  Google Scholar 

  36. Razavi, B. S., Blagodatskaya, E. & Kuzyakov, Y. Nonlinear temperature sensitivity of enzyme kinetics explains canceling effect—a case study on loamy haplic Luvisol. Front. Microbiol. 6, 1126 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Moyano, F. E., Manzoni, S. & Chenu, C. Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biol. Biochem. 59, 72–85 (2013).

    Article  CAS  Google Scholar 

  38. Katul, G. G., Oren, R., Manzoni, S., Higgins, C. & Parlange, M. B. Evapotranspiration: a process driving mass transport and energy exchange in the soil–plant–atmosphere–climate system. Rev. Geophys. 50, RG3002 (2012).

    Article  Google Scholar 

  39. Zhou, H. et al. Relative importance of climatic variables, soil properties and plant traits to spatial variability in net CO2 exchange across global forests and grasslands. Agr. For. Meteorol. 307, 108506 (2021).

    Article  Google Scholar 

  40. Allen, A. P., Gillooly, J. F. & Brown, J. H. Linking the global carbon cycle to individual metabolism. Funct. Ecol. 19, 202–213 (2005).

    Article  Google Scholar 

  41. Enquist, B. J. et al. Scaling metabolism from organisms to ecosystems. Nature 423, 639–642 (2003).

    Article  CAS  PubMed  Google Scholar 

  42. German, D. P., Marcelo, K. R., Stone, M. M. & Allison, S. D. The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob. Change Biol. 18, 1468–1479 (2012).

    Article  Google Scholar 

  43. Stone, M. M. et al. Temperature sensitivity of soil enzyme kinetics under N-fertilization in two temperate forests. Glob. Change Biol. 18, 1173–1184 (2012).

    Article  Google Scholar 

  44. Lieth, H. in Primary Productivity of the Biosphere (eds Lieth, H. & Whittaker, R. H.) 237–263 (Springer-Verlag, 1975).

  45. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    Article  CAS  PubMed  Google Scholar 

  46. Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wei, S. et al. Data‐based perfect‐deficit approach to understanding climate extremes and forest carbon assimilation capacity. Environ. Res. Lett. 9, 065002 (2014).

    Article  Google Scholar 

  48. Kirschbaum, M. U. F. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol. Biochem. 27, 753–760 (1995).

    Article  CAS  Google Scholar 

  49. Orth, R., Destouni, G., Jung, M. & Reichstein, M. Large-scale biospheric drought response intensifies linearly with drought duration in arid regions. Biogeosciences 17, 2647–2656 (2020).

    Article  Google Scholar 

  50. Jarvis, P. et al. Drying and wetting of Mediterranean soils stimulates decomposition and carbon dioxide emission: the “Birch effect”. Tree Physiol. 27, 929–940 (2007).

    Article  CAS  PubMed  Google Scholar 

  51. Yi, C., Wei, S. & Hendrey, G. Warming climate extends dryness-controlled areas of terrestrial carbon sequestration. Sci. Rep. 4, 5472 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dai, A. Increasing drought under global warming in observations and models. Nat. Clim. Change 3, 52–58 (2013).

    Article  Google Scholar 

  53. Ritchie, P. D., Parry, I., Clarke, J. J., Huntingford, C. & Cox, P. M. Increases in the temperature seasonal cycle indicate long-term drying trends in Amazonia. Commun. Earth Environ. 3, 199 (2022).

    Article  Google Scholar 

  54. Yao, F. et al. Satellites reveal widespread decline in global lake water storage. Science 380, 743–749 (2023).

    Article  CAS  PubMed  Google Scholar 

  55. The Intergovernmental Panel on Climate Change. Climate Change 2022: Impacts, Adaptation, and Vulnerability (eds Pörtner, H.-O. et al.) (Cambridge Univ. Press, 2022).

  56. Hansen, J., Sato, M. & Ruedy, R. Global Temperature in 2021 (Columbia Univ., 2022).

  57. Kasahara, H. & Shimotsu, S. Testing the number of components in normal mixture regression models. J. Am. Stat. Assoc. 110, 1632–1645 (2015).

    Article  CAS  Google Scholar 

  58. Zhu, T. H. & Zhang, H. Hypothesis testing in mixture regression models. J. R. Stat. Soc. B 66, 3–16 (2004).

    Article  Google Scholar 

  59. Titterington, D. M., Smith, A. F. M. & Makov, U. E. Statistical Analysis of Finite Mixture Distributions (Wiley, 1985).

  60. Lindsay, BG. Mixture Models: Theory, Geometry, and Applications (Institute of Statistical Mathematics, 1995).

  61. Peel, D. & MacLahlan, G. Finite Mixture Models (Wiley, 2000)

  62. Huang, M., Li, R. & Wang, S. Nonparametric mixture of regression models. J. Am. Stat. Assoc. 108, 929–941 (2013).

    Article  CAS  Google Scholar 

  63. Huang, M., Li, R., Wang, H. & Yao, W. Estimating mixture of Gaussian processes by kernel smoothing. J. Bus. Econ. Stat. 32, 259–270 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Dempster, A. P., Laird, N. M. & Rubin, D. B. Maximum likelihood from incomplete data via the EM algorithm (with discussion). J. R. Stat. Soc. B 39, 1–38 (1977).

    Article  Google Scholar 

  65. Yi, C. et al. Climate control of terrestrial carbon exchange across biomes and continents. Environ. Res. Lett. 5, 034007 (2010).

    Article  Google Scholar 

Download references

Acknowledgements

This work used eddy covariance data acquired and shared by the FLUXNET community, including these networks: AmeriFlux, AfriFlux, AsiaFlux, CarboAfrica, CarboEuropeIP, CarboItaly, CarboMont, ChinaFlux, Fluxnet-Canada, GreenGrass, ICOS, KoFlux, LBA, NECC, OzFlux-TERN, TCOS-Siberia and USCCC. The FLUXNET eddy covariance data processing and harmonization were carried out by the ICOS Ecosystem Thematic Center, AmeriFlux Management Project and Fluxdata project of FLUXNET, with the support of CDIAC and the OzFlux, ChinaFlux and AsiaFlux offices. C.Y. completed this research when he was a Fulbright Visiting Professor at University of Innsbruck with support from the US-Austria Fulbright Program. D.C. is supported by the Swedish national strategic research area BECC. G.D. has received support for this research from the Swedish Research Council (VR; grant number 2022-04672). The research of M.R. is supported by the European Research Council (ERC-Synergy project RESILIENCE, proposal no. 101071417) and by the Dutch Research Council (NWO ‘Resilience in complex systems through adaptive spatial pattern formation’, project no. OCENW.M20.169). S.M. was supported by ERC grant 101001608. G.W. acknowledges support from Austrian Research Promotion Agency grant 878893 and the Austrian Science Fund (10.55776/PAT2661823). N.K. acknowledges funding from National Oceanic and Atmospheric Administration Educational Partnership Program with Minority-Serving Institutions—Cooperative Science Center for Earth System Sciences and Remote Sensing Technologies cooperative agreement grant NA22SEC4810016.

Author information

Authors and Affiliations

Authors

Contributions

C.Y., Q.Z. and G.D. conceived the project. Q.Z. performed data processing with R.L., Z.T. and J.H. Q.Z. and C.Y. conducted data analysis. C.Y. wrote the first version of the manuscript with Q.Z., E.K., R.L., D.C., G.W., Y.K., G.D., S.M., M.R., G.H. and W.F. All authors discussed the results and contributed to the writing and to the final manuscript.

Corresponding author

Correspondence to Chuixiang Yi.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Jingfeng Xiao and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 The statistics of the empirical threshold model \(\tilde{P}(T)\).

The blue filled circles are the data of mean annual temperature and mean annual precipitation in B-group. The threshold curve (black line) is the exponential regression line with 95% confidence interval (shaded area), R2 = 0.53 and p < 0.01 for One-Tailed Test.

Extended Data Fig. 2 Differential sensitivity of Q10 to Dryness (DI).

212 sites of FLUXNET2015 were divided into six groups with six DI intervals: 0 < DI < 0.4 (9 sites); 0.4 < DI < 0.7 (61 sites); 0.7 < DI < 1.0 (58 sites); 1.0 < DI < 1.4 (38 sites); 1.4 < DI < 2.2 (23 sites); and DI > 2.2 (23 sites). The apparent group average Q10 were estimated by Q10 models (see Methods).

Extended Data Fig. 3 Differential sensitivity of Q10 to temperature revealed by Dryness (DI).

212 sites of FLUXNET2015 were divided into six groups with six DI intervals: 0 < DI < 0.4 (9 sites); 0.4 < DI < 0.7 (61 sites); 0.7 < DI < 1.0 (58 sites); 1.0 < DI < 1.4 (38 sites); 1.4 < DI < 2.2 (23 sites); and DI > 2.2 (23 sites). The filled circles and error bars represent DI-group means and their standard deviations, respectively. The blue line is the regression (y = -0.1719x + 3.2197, R2 = 0.63 for the data DI < 1, while the red line is the regression (y = -0.047x + 1.97, R2 = 0.93) for the data DI > 1.

Extended Data Fig. 4 The distribution and statistics of Q10 for each DI group.

212 sites of FLUXNET2015 were divided into six groups with six DI intervals: (a) 0 < DI < 0.4 (9 sites); (b) 0.4 < DI < 0.7 (61 sites); (c) 0.7 < DI < 1.0 (58 sites); (d) 1.0 < DI < 1.4 (38 sites); (e) 1.4 < DI < 2.2 (23 sites); and (f) DI > 2.2 (23 sites). Q10 was calculated with Q10 model (equation (14)) based on FLUXNET2015 ecosystem respiration \({R}_{e}^{{EC}}\) data and temperature data (see Methods).

Extended Data Fig. 5 The impact of precipitation (P) on ecosystem respiration (Re) across various time scales based on the data of Re and P from the same P-group sites.

(a) half-hourly; (b) daily; (c) weekly; (d) monthly; and (e) yearly. n is the number of scatter points.

Extended Data Fig. 6 The asymmetric effect of precipitation (P) on ecosystem respiration (Re).

(a) all sites; (b) T-group; (c) P-group; and (d) B-group. The y-axis represents the residuals of model Re(P) (equation(12)). The x-axis is coefficient of variation of monthly precipitation.

Supplementary information

Supplementary Information

Supplementary Methods 1–4, Figs. 1–4, Table 1 and references.

Reporting Summary

Peer Review File

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Q., Yi, C., Destouni, G. et al. Water limitation regulates positive feedback of increased ecosystem respiration. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02501-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41559-024-02501-w

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology