Soil microbial respiration adapts to ambient temperature in global drylands


Heterotrophic soil microbial respiration—one of the main processes of carbon loss from the soil to the atmosphere—is sensitive to temperature in the short term. However, how this sensitivity is affected by long-term thermal regimes is uncertain. There is an expectation that soil microbial respiration rates adapt to the ambient thermal regime, but whether this adaptation magnifies or reduces respiration sensitivities to temperature fluctuations remains unresolved. This gap in understanding is particularly pronounced for drylands because most studies conducted so far have focused on mesic systems. Here, we conduct an incubation study using soil samples from 110 global drylands encompassing a wide gradient in mean annual temperature. We test how mean annual temperature affects soil respiration rates at three assay temperatures while controlling for substrate depletion and microbial biomass. Estimated soil respiration rates at the mean microbial biomass were lower in sites with higher mean annual temperatures across the three assayed temperatures. The patterns observed are consistent with expected evolutionary trade-offs in the structure and function of enzymes under different thermal regimes. Therefore, our results suggest that soil microbial respiration adapts to the ambient thermal regime in global drylands.

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Fig. 1: Expected outcomes of the effect of MAT of the source site on potential soil microbial respiration rates at three assay temperatures under three competing hypotheses.
Fig. 2: Estimated effects of MAT on potential respiration rates at a common microbial biomass value and with substrate in excess.
Fig. 3: Comparison of the estimated effects of MAT on potential respiration rates, at a common microbial biomass value and with substrate in excess, between our model and a model assuming no MAT effect.
Fig. 4: Estimated effects of microsite (vegetated versus open areas) on potential respiration rates at a common microbial biomass value and with substrate in excess.

Data availability

Data in the support of these findings and the R code for the statistical models are available from Figshare (;


  1. 1.

    Dorrepaal, E. et al. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–619 (2009).

    CAS  Google Scholar 

  2. 2.

    Melillo, J. M. et al. Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proc. Natl Acad. Sci. USA 108, 9508–9512 (2011).

    CAS  PubMed  Google Scholar 

  3. 3.

    Frey, S. D., Lee, J., Melillo, J. M. & Six, J. The temperature response of soil microbial efficiency and its feedback to climate. Nat. Clim. Change 3, 395–398 (2013).

    CAS  Google Scholar 

  4. 4.

    Tucker, C. L., Bell, J., Pendall, E. & Ogle, K. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob. Change Biol. 19, 252–263 (2013).

    Google Scholar 

  5. 5.

    IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer L. A.) (IPCC, 2014).

  6. 6.

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

    CAS  Google Scholar 

  7. 7.

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

    Google Scholar 

  8. 8.

    Oechel, W. C. et al. Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406, 978–981 (2000).

    CAS  PubMed  Google Scholar 

  9. 9.

    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).

    CAS  PubMed  Google Scholar 

  10. 10.

    Rustad, L. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001).

    CAS  PubMed  Google Scholar 

  11. 11.

    Melillo, J. M. et al. Soil warming and carbon-cycle feedbacks to the climate system. Science 298, 2173–2176 (2002).

    CAS  PubMed  Google Scholar 

  12. 12.

    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).

    Google Scholar 

  13. 13.

    Eliasson, P. E. et al. The response of heterotrophic CO2 flux to soil warming. Glob. Change Biol. 11, 167–181 (2005).

    Google Scholar 

  14. 14.

    Hartley, I. P., Heinemeyer, A. & Ineson, P. Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob. Change Biol. 13, 1761–1770 (2007).

    Google Scholar 

  15. 15.

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

    PubMed  Google Scholar 

  16. 16.

    Schindlbacher, A., Schnecker, J., Takriti, M., Borken, W. & Wanek, W. Microbial physiology and soil CO2 efflux after 9 years of soil warming in a temperate forest: no indications for thermal adaptations. Glob. Change Biol. 21, 4265–4277 (2015).

    Google Scholar 

  17. 17.

    Hochachka, P. W. & Somero, G. N. Biochemical Adaptation Mechanism and Process in Physiological Evolution (Oxford Univ. Press, New York, 2002).

  18. 18.

    Bradford, M. A., Watts, B. W. & Davies, C. A. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob. Change Biol. 16, 1576–1588 (2010).

    Google Scholar 

  19. 19.

    Hartley, I. P., Hopkins, D. W., Garnett, M. H., Sommerkorn, M. & Wookey, P. A. Soil microbial respiration in arctic soil does not acclimate to temperature. Ecol. Lett. 11, 1092–1100 (2008).

    PubMed  Google Scholar 

  20. 20.

    Karhu, K. et al. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–84 (2014).

    CAS  Google Scholar 

  21. 21.

    Nazaries, L. et al. Shifts in the microbial community structure explain the response of soil respiration to land-use change but not to climate warming. Soil Biol. Biochem. 89, 123–134 (2015).

    CAS  Google Scholar 

  22. 22.

    Nie, M. et al. Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecol. Lett. 16, 234–241 (2013).

    PubMed  Google Scholar 

  23. 23.

    De Frenne, P. et al. Latitudinal gradients as natural laboratories to infer species’ responses to temperature. J. Ecol. 101, 784–795 (2013).

    Google Scholar 

  24. 24.

    Prăvălie, R. Drylands extent and environmental issues. A global approach. Earth Sci. Rev. 161, 259–278 (2016).

    Google Scholar 

  25. 25.

    Plaza, C. et al. Soil resources and element stocks in drylands to face global issues. Sci. Rep. 8, 13788 (2018).

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Huang, J., Yu, H., Guan, X., Wang, G. & Guo, R. Accelerated dryland expansion under climate change. Nat. Clim. Change 6, 166–171 (2016).

    Google Scholar 

  27. 27.

    Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. USA 113, 13797–13802 (2016).

    CAS  PubMed  Google Scholar 

  28. 28.

    Escolar, C., Maestre, F. T. & Rey, A. Biocrusts modulate warming and rainfall exclusion effects on soil respiration in a semi-arid grassland. Soil Biol. Biochem. 80, 9–17 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Middleton, N. J. & Thomas, D. S. G. World Atlas of Desertification (Hodder Arnold, London, 1997).

  30. 30.

    Maestre, F. T. & Cortina, J. Small-scale spatial variation in soil CO2 efflux in a Mediterranean semiarid steppe. Appl. Soil Ecol. 23, 199–209 (2003).

    Google Scholar 

  31. 31.

    Housman, D. C. et al. Heterogeneity of soil nutrients and subsurface biota in a dryland ecosystem. Soil Biol. Biochem. 39, 2138–2149 (2007).

    CAS  Google Scholar 

  32. 32.

    Rey, A. et al. Impact of land degradation on soil respiration in a steppe (Stipa tenacissima L.) semi-arid ecosystem in the SE of Spain. Soil Biol. Biochem. 43, 393–403 (2011).

    CAS  Google Scholar 

  33. 33.

    Conant, R. T., Dalla-Betta, P., Klopatek, C. C. & Klopatek, J. M. Controls on soil respiration in semiarid soils. Soil Biol. Biochem. 36, 945–951 (2004).

    CAS  Google Scholar 

  34. 34.

    Muñoz-Rojas, M., Lewandrowski, W., Erickson, T. E., Dixon, K. W. & Merritt, D. J. Soil respiration dynamics in fire affected semi-arid ecosystems: effects of vegetation type and environmental factors. Sci. Total Environ. 572, 1385–1394 (2016).

    PubMed  Google Scholar 

  35. 35.

    Conant, R. T., Klopatek, J. M. & Klopatek, C. C. Environmental factors controlling soil respiration in three semiarid ecosystems. Soil Sci. Soc. Am. J. 64, 383–390 (2000).

    CAS  Google Scholar 

  36. 36.

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

    CAS  PubMed  Google Scholar 

  37. 37.

    Rustad, L. E., Huntington, T. G. & Boone, R. D. Controls on soil respiration: implications for climate change. Biogeochemistry 48, 1–6 (2000).

    Google Scholar 

  38. 38.

    Ochoa-Hueso, R. et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. J. Ecol. 106, 242–253 (2018).

    CAS  Google Scholar 

  39. 39.

    Bradford, M. A. et al. Decreased mass specific respiration under experimental warming is robust to the microbial biomass method employed. Ecol. Lett. 12, E15–E18 (2009).

    Google Scholar 

  40. 40.

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

    CAS  Google Scholar 

  41. 41.

    Bradford, M. A. et al. Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation. Nat. Ecol. Evol. (2019).

  42. 42.

    Rousk, J. Biomass or growth? How to measure soil food webs to understand structure and function. Soil Biol. Biochem. 102, 45–47 (2016).

    CAS  Google Scholar 

  43. 43.

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

    Google Scholar 

  44. 44.

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

    CAS  PubMed  Google Scholar 

  45. 45.

    Kirschbaum, M. U. F. The temperature dependence of organic-matter decomposition: still a topic of debate. Soil Biol. Biochem. 38, 2510–2518 (2006).

    CAS  Google Scholar 

  46. 46.

    Maestre, F. T. et al. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc. Natl Acad. Sci. USA 112, 15684–15689 (2015).

    CAS  PubMed  Google Scholar 

  47. 47.

    Crowther, T. W. et al. Untangling the fungal niche: the trait-based approach. Front. Microbiol. 5, 579 (2014).

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Evans, S. E. & Wallenstein, M. D. Climate change alters ecological strategies of soil bacteria. Ecol. Lett. 17, 155–164 (2014).

    PubMed  Google Scholar 

  49. 49.

    Maestre, F. T. et al. Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Zornoza, R., Mataix-Solera, J., Guerrero, C., Arcenegui, V. & Mataix-Beneyto, J. Storage effects on biochemical properties of air-dried soil samples from southeastern Spain. Arid Land Res. Manag. 23, 213–222 (2009).

    CAS  Google Scholar 

  51. 51.

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Google Scholar 

  52. 52.

    Delgado-Baquerizo, M. et al. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502, 672–676 (2013).

    CAS  PubMed  Google Scholar 

  53. 53.

    Lauber, C. L., Hamady, M., Knight, R. & Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111–5120 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Anderson, J. M. & Ingram, J. S. Tropical Soil Biology and Fertility: A Handbook of Methods (CAB International, Wallingford, 1993).

  55. 55.

    Kettler, T. A., Doran, J. W. & Gilbert, T. L. Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci. Soc. Am. J. 65, 849–852 (2001).

    CAS  Google Scholar 

  56. 56.

    Campbell, C. D., Chapman, S. J., Cameron, C. M., Davidson, M. S. & Potts, J. M. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl. Environ. Microbiol. 69, 3593–3599 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Davidson, E. A., Janssens, I. A. & Luo, Y. On the variability of respiration in terrestrial ecosystems: moving beyond Q 10. Glob. Change Biol. 12, 154–164 (2006).

    Google Scholar 

  58. 58.

    Lundegårdh, H. Carbon dioxide evolution of soil and crop growth. Soil Sci. 23, 415–453 (1927).

    Google Scholar 

  59. 59.

    Fierer, N., Schimel, J. P. & Holden, P. A. Variations in microbial community composition through two soil depth profiles. Soil Biol. Biochem. 35, 167–176 (2003).

    CAS  Google Scholar 

  60. 60.

    Hartley, I. P., Hopkins, D. W., Garnett, M. H., Sommerkorn, M. & Wookey, P. A. No evidence for compensatory thermal adaptation of soil microbial respiration in the study of Bradford et al. (2008). Ecol. Lett. 12, E12–E14 (2009).

    PubMed  Google Scholar 

  61. 61.

    Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).

    CAS  Google Scholar 

  62. 62.

    Gregorich, E. G., Wen, G., Voroney, R. P. & Kachanoski, R. G. Calibration of a rapid direct chloroform extraction method for measuring soil microbial biomass. Soil Biol. Biochem. 22, 1009–1011 (1990).

    CAS  Google Scholar 

  63. 63.

    Wu, J., Joergensen, R. G., Pommerening, B., Chaussod, R. & Brookes, P. C. Measurement of soil microbial biomass C by fumigation-extraction: an automated procedure. Soil Biol. Biochem. 22, 1167–1169 (1990).

    CAS  Google Scholar 

  64. 64.

    Joergensen, R. G., Wu, J. & Brookes, P. C. Measuring soil microbial biomass using an automated procedure. Soil Biol. Biochem. 43, 873–876 (2011).

    CAS  Google Scholar 

  65. 65.

    Nicolardot, B., Fauvet, G. & Cheneby, D. Carbon and nitrogen cycling through soil microbial biomass at various temperatures. Soil Biol. Biochem. 26, 253–261 (1994).

    CAS  Google Scholar 

  66. 66.

    Jasieński, M. & Bazzaz, F. The fallacy of ratios and the testability of models in biology. Oikos 84, 321–326 (1999).

    Google Scholar 

  67. 67.

    Hobbs, N. T., Andrén, H., Persson, J., Aronsson, M. & Chapron, G. Native predators reduce harvest of reindeer by Sámi pastoralists. Ecol. Appl. 22, 1640–1654 (2012).

    PubMed  Google Scholar 

  68. 68.

    Bradford, M. A. et al. A test of the hierarchical model of litter decomposition. Nat. Ecol. Evol. 1, 1836–1845 (2017).

    PubMed  Google Scholar 

  69. 69.

    Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

  70. 70.

    Mazerolle, M. J. Improving data analysis in herpetology: using Akaike's information criterion (AIC) to assess the strength of biological hypotheses. Amphibia-Reptilia 27, 169–180 (2006).

    Google Scholar 

  71. 71.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).

  72. 72.

    Baayen, R. H., Davidson, D. J. & Bates, D. M. Mixed-effects modeling with crossed random effects for subjects and items. J. Mem. Lang. 59, 390–412 (2008).

    Google Scholar 

  73. 73.

    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Google Scholar 

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This research was supported by the European Research Council (ERC)-funded projects BIOCOM (ERC grant no. 242658) and BIODESERT (ERC grant no. 647038), and by the Spanish Ministry of Economy and Competitiveness (BIOMOD project, grant no. CGL2013-44661-R). M.D. is supported by an FPU fellowship from the Spanish Ministry of Education, Culture and Sports (ref. FPU-15/00392). P.G.P. acknowledges the Spanish Ministry of Economy and Competitiveness for financial support via the Juan de la Cierva Program (grant no. IJCI‐2014‐20058). C.P. acknowledges support from the European Union’s Horizon 2020 Research and Innovation Program under the Marie Skłodowska-Curie grant no. 654132. We thank D. Mendoza for her help in the laboratory.

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F.T.M. designed the field study and wrote the grant that funded the work. P.G.P and M.D. developed the original idea of the analyses presented in the manuscript. M.D. and C.P. conducted the laboratory work. M.D. conducted the statistical analyses with the help of M.A.B. All authors contributed to data interpretation and manuscript writing.

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Correspondence to Marina Dacal.

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Dacal, M., Bradford, M.A., Plaza, C. et al. Soil microbial respiration adapts to ambient temperature in global drylands. Nat Ecol Evol 3, 232–238 (2019).

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