Skip to main content

Temperature Dependence of Soil Respiration Modulated by Thresholds in Soil Water Availability Across European Shrubland Ecosystems

Abstract

Soil respiration (SR) is a major component of the global carbon cycle and plays a fundamental role in ecosystem feedback to climate change. Empirical modelling is an essential tool for predicting ecosystem responses to environmental change, and also provides important data for calibrating and corroborating process-based models. In this study, we evaluated the performance of three empirical temperature–SR response functions (exponential, Lloyd–Taylor and Gaussian) at seven shrublands located within three climatic regions (Atlantic, Mediterranean and Continental) across Europe. We investigated the performance of SR models by including the interaction between soil moisture and soil temperature. We found that the best fit for the temperature functions depended on the site-specific climatic conditions. Including soil moisture, we identified thresholds in the three different response functions that improved the model fit in all cases. The direct soil moisture effect on SR, however, was weak at the annual time scale. We conclude that the exponential soil temperature function may only be a good predictor for SR in a narrow temperature range, and that extrapolating predictions for future climate based on this function should be treated with caution as modelled outputs may underestimate SR. The addition of soil moisture thresholds improved the model fit at all sites, but had a far greater ecological significance in the wet Atlantic shrubland where a fundamental change in the soil CO2 efflux would likely have an impact on the whole carbon budget.

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

Figure 1
Figure 2
Figure 3

References

  1. Ågren GI, Wetterstedt JÅM. 2007. What determines the temperature response of soil organic matter decomposition? Soil Biol Biochem 39:1794–8.

    Article  Google Scholar 

  2. Ågren GI, McMurtrie RE, Parton WJ, Pastor J, Shugart HH. 1991. State-of-the-art of models of production-decomposition linkages in conifer and grassland ecosystems. Ecol Appl 1:118–38.

    Article  PubMed  Google Scholar 

  3. Balogh J, Pintér K, Sz Fóti, Papp M, Cserhalmi D, Nagy Z. 2011. Dependence of soil respiration on soil moisture, clay content, soil organic matter, and CO2 uptake in dry grasslands. Soil Biol Biochem 43:1006–13.

    CAS  Article  Google Scholar 

  4. Beier C, Emmett B, Gundersen P, Tietema A, Peňuelas J, Estiarte M, Gordon C, Gorissen A, Llorens L, Roda F, Williams D. 2004. Novel approaches to study climate change effects on terrestrial ecosystems in the field: drought and passive nighttime warming. Ecosystems 7:583–97.

    Article  Google Scholar 

  5. Beier C, Emmett B, Tietema A, Schmidt IK, Peñuelas J, Kovács-Láng E, Duce P, de Angelis P, Gorissen A, Estiarte M, de Dato G, Sowerby A, Kröel-Dulay G, Lellei-Kovács E, Kull O, Mand P, Petersen H, Gjelstrup P, Spano D. 2009. Carbon and nitrogen balances for six shrublands across Europe. Glob Biogeochem Cycles 23:GB4008.

    Article  Google Scholar 

  6. Billings SA, Ballantyne FIV. 2013. How interactions between microbial resource demands, soil organic matter stoichiometry, and substrate reactivity determine the direction and magnitude of soil respiratory responses to warming. Glob Change Biol 19:90–102.

    Article  Google Scholar 

  7. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD. 2008. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–27.

    Article  PubMed  Google Scholar 

  8. Burnham KP, Anderson DR. 2002. Model selection and multimodel inference: a practical information-theoretic approach. 2nd edn. New York: Springer.

    Google Scholar 

  9. Chen S, Lin G, Huang J, Jenerette GD. 2009. Dependence of carbon sequestration on the differential responses of ecosystem photosynthesis and respiration to rain pulses in a semiarid steppe. Glob Change Biol 15:2450–61.

    Article  Google Scholar 

  10. Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH. 2008. Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–20.

    Article  Google Scholar 

  11. Curiel Yuste J, Ma S, Baldocchi DD. 2010. Plant-soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect predictions of soil CO2 efflux. Biogeochemistry 98:127–38.

    CAS  Article  Google Scholar 

  12. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73.

    CAS  Article  PubMed  Google Scholar 

  13. Davidson EA, Belk E, Boone RD. 1998. Soil water content and temperature as independent or confounded factors controlling soil respiration in temperate mixed hardwood forest. Glob Change Biol 4:217–27.

    Article  Google Scholar 

  14. Davidson EA, Janssens IA, Luo Y. 2006. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob Change Biol 12:154–64.

    Article  Google Scholar 

  15. de Dato GD, de Angelis P, Sirca C, Beier C. 2010. Impact of drought and increasing temperatures on soil CO2 emissions in a Mediterranean shrubland (gariga). Plant Soil 327:153–66.

    CAS  Article  Google Scholar 

  16. Domínguez MT, Sowerby A, Smith AR, Robinson DA, Van Baarsel S, Mills RTE, Marshall MR, Koller E, Lebron I, Hall J, Emmett BA. 2015. Sustained impact of drought on wet shrublands mediated by soil physical changes. Biogeochemistry 122:151–63.

    Article  Google Scholar 

  17. Emmett B, Beier C, Estiarte M, Tietema A, Kristensen HL, Williams D, Peñuelas J, Schmidt I, Sowerby A. 2004. The response of soil processes to climate change: results from manipulation studies of shrublands across an environmental gradient. Ecosystems 7:625–37.

    Article  Google Scholar 

  18. Fernandez DP, Neff JC, Belnap J, Reynolds RL. 2006. Soil respiration in the cold desert environment of the Colorado Plateau (USA): abiotic regulators and thresholds. Biogeochemistry 78:247–65.

    Article  Google Scholar 

  19. González-Ubierna S, de la Cruz MT, Casermeiro MÁ. 2014. Climate factors mediate soil respiration dynamics in Mediterranean agricultural environments: an empirical approach. Soil Res 52:543–53.

    Article  Google Scholar 

  20. Guidolotti G, Rey A, D’Andrea E, Matteucci G, De Angelis P. 2013. Effect of environmental variables and stand structure on ecosystem respiration components in a Mediterranean beech forest. Tree Physiol 33:960–72.

    CAS  Article  PubMed  Google Scholar 

  21. Hothorn T, Hornik K, Zeileis A. 2006. Unbiased recursive partitioning: a conditional inference framework. J Comput Graph Stat 15:651–74.

    Article  Google Scholar 

  22. Howard DM, Howard PJA. 1993. Relationships between CO2 evolution, moisture content and temperature for a range of soil types. Soil Biol Biochem 25:1537–46.

    Article  Google Scholar 

  23. IPCC 2013. The physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, Eds. Climate change 2013: contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.

  24. Johnson JB, Omland KS. 2004. Model selection in ecology and evolution. Trends Ecol Evol 19:101–8.

    Article  PubMed  Google Scholar 

  25. Kirschbaum MUF. 2004. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Change Biol 10:1870–7.

    Article  Google Scholar 

  26. Kopittke GR, van Loon EE, Tietema A, Asscheman D. 2013. Soil respiration on an aging managed heathland: identifying an appropriate empirical model for predictive purposes. Biogeosciences 10:3007–38.

    CAS  Article  Google Scholar 

  27. Kopittke GR, Tietema A, van Loon EE, Asscheman D. 2014. Fourteen annually repeated droughts suppressed autotrophic soil respiration and resulted in an ecosystem change. Ecosystems 17:242–57.

    CAS  Article  Google Scholar 

  28. Kotroczó Zs, Veres Zs, Fekete I, Krakomperger Zs, Tóth JA, Lajtha K, Tóthmérész B. 2014. Soil enzyme activity in response to long-term organic matter manipulation. Soil Biol Biochem 70:237–43.

    Article  Google Scholar 

  29. Leirós MC, Trasar-Cepeda C, Seoane S, Gil-Sotres F. 1999. Dependence of mineralization of soil organic matter on temperature and moisture. Soil Biol Biochem 31:327–35.

    Article  Google Scholar 

  30. Lellei-Kovács E, Kovács-Láng E, Kalapos T, Botta-Dukát Z, Barabás S, Beier C. 2008. Experimental warming does not enhance soil respiration in a semiarid temperate forest-steppe ecosystem. Commun Ecol 9:29–37.

    Article  Google Scholar 

  31. Lellei-Kovács E, Kovács-Láng E, Botta-Dukát Z, Kalapos T, Emmett B, Beier C. 2011. Thresholds and interactive effects of soil moisture on the temperature response of soil respiration. Eur J Soil Biol 47:247–55.

    Article  Google Scholar 

  32. Lloyd J, Taylor JA. 1994. On the temperature dependence of soil respiration. Funct Ecol 8:315–23.

    Article  Google Scholar 

  33. Maestre FT, Escolar C, de Guevara ML, Quero JL, Lázaro R, Delgado-Baquerizo M, Ochoa V, Berdugo M, Gozalo B, Gallardo A. 2013. Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Change Biol 19:3835–47.

    Article  Google Scholar 

  34. Mielnick PC, Dugas WA. 2000. Soil CO2 flux in a tallgrass prairie. Soil Biol Biochem 32:221–8.

    CAS  Article  Google Scholar 

  35. Mikkelsen TN, Beier C, Jonasson S, Holmstrup M, Schmidt IK, Ambus P, Pilegaard K, Michelsen A, Albert K, Andresen LC, Arndal MF, Bruun N, Christensen S, Danbæk S, Gundersen P, Jørgensen P, Linden LG, Kongstad J, Maraldo K, Priemé A, Riis-Nielsen T, Ro-Poulsen H, Stevnbak K, Selsted MB, Sørensen P, Larsen KS, Carter MS, Ibrom A, Martinussen T, Miglietta F, Sverdrup H. 2008. Experimental design of multifactor climate change experiments with elevated CO2, warming and drought: the CLIMAITE project. Funct Ecol 22:185–95.

    Google Scholar 

  36. Moyano FE, Manzoni S, Chenu C. 2013. Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biol Biochem 59:72–85.

    CAS  Article  Google Scholar 

  37. Murthy R, Griffin KL, Zarnoch SJ, Dougherty PM, Watson B, Haren JV, Patterson RL, Mahato T. 2003. Carbon dioxide efflux from a 550 m2 soil across a range of soil temperatures. For Ecol Manag 178:311–27.

    Article  Google Scholar 

  38. Pavelka M, Acosta M, Marek MV, Kutsch W, Janous D. 2007. Dependence of the Q10 values on the depth of the soil temperature measuring point. Plant Soil 292:171–9.

    CAS  Article  Google Scholar 

  39. Peñuelas J, Prieto P, Beier C, Cesaraccio C, de Angelis P, de Dato G, Emmett BA, Estiarte M, Garadnai J, Gorissen A, Kovács-Láng E, Kröel-Dulay G, Llorens L, Pellizzaro G, Riis-Nielsen T, Schmidt IK, Sirca C, Sowerby A, Spano D, Tietema A. 2007. Response of plant species richness and primary productivity in shrublands along a north-south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003. Glob Change Biol 13:2563–81.

    Article  Google Scholar 

  40. Qi Y, Xu M, Wu J. 2002. Temperature sensitivity of soil respiration and its effects on ecosystem carbon budget: nonlinearity begets surprises. Ecol Model 153:131–42.

    CAS  Article  Google Scholar 

  41. R Development Core Team. 2008. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.R-project.org.

  42. Reichstein M, Beer C. 2008. Soil respiration across scales: the importance of a model-data integration framework for data interpretation. J Plant Nutr Soil Sci 171:344–54.

    CAS  Article  Google Scholar 

  43. Reichstein M, Tenhunen JD, Roupsard O, Ourcival JM, Rambal S, Miglietta F, Peressotti A, Pecchiari M, Tirone G, Valentini R. 2002. Severe drought effects on ecosystem CO2 and H2O fluxes at three Mediterranean evergreen sites: revision of current hypotheses? Glob Change Biol 8:999–1017.

    Article  Google Scholar 

  44. Rey A, Pegoraro E, Tedeschi V, De Parri I, Jarvis PG, Valentini R. 2002. Annual variation in soil respiration and its components in a coppice oak forest in Central Italy. Glob Change Biol 8:851–66.

    Article  Google Scholar 

  45. Robinson DA, Jones SB, Lebron I, Reinsch S, Domínguez MT, Smith AR, Jones DL, Marshall MR, Emmett BA. 2016. Experimental evidence for drought induced alternative stable states of soil moisture. Sci Rep 6:20018.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Rodrigo A, Recous S, Neel C, Mary B. 1997. Modelling temperature and moisture effects on C-N transformations in soils: comparison of nine models. Ecol Model 102:325–39.

    CAS  Article  Google Scholar 

  47. Sardans J, Peñuelas J, Estiarte M, Prieto P. 2008. Warming and drought alter C and N concentration, allocation and accumulation in a Mediterranean shrubland. Glob Change Biol 14:2304–16.

    Article  Google Scholar 

  48. Saxton KE, Rawls WJ. 2006. Soil water characteristic estimates by texture and organic matter for hydrologic solutions. Soil Sci Soc Am J 70:1569–78.

    CAS  Article  Google Scholar 

  49. Shen Z, Shi B, Wang B, Jiang H-J. 2013. The temperature dependence of soil organic matter decomposition and CO2 efflux: a review. Acta Ecol Sin 33:3011–19 (in Chinese).

    Article  Google Scholar 

  50. Skopp J, Jawson MD, Doran JW. 1990. Steady-state aerobic microbial activity as a function of soil water content. Soil Sci Soc Am J 54:1619–25.

    Article  Google Scholar 

  51. Sowerby A, Emmett B, Tietema A, Beier C. 2008. Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils. Glob Change Biol 14:2388–404.

    Article  Google Scholar 

  52. Subke J-A, Bahn M. 2010. On the temperature sensitivity of soil respiration: can we use the immeasurable to predict the unknown? Soil Biol Biochem 42:1653–6.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Suseela V, Conant RT, Wallenstein MD, Dukes JS. 2012. Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Change Biol 18:336–48.

    Article  Google Scholar 

  54. Tuomi M, Vanhala P, Karhu K, Fritze H, Liski J. 2008. Heterotrophic soil respiration—comparison of different models describing its temperature dependence. Ecol Model 211:182–90.

    Article  Google Scholar 

  55. Vicca S, Bahn M, Estiarte M, van Loon EE, Vargas R, Alberti G, Ambus P, Arain MA, Beier C, Bentley LP, Borken W, Buchmann N, Collins SL, de Dato G, Dukes JS, Escolar C, Fay P, Guidolotti G, Hanson PJ, Kahmen A, Kröel-Dulay G, Ladreiter-Knauss T, Larsen KS, Lellei-Kovács E, Lebrija-Trejos E, Maestre FT, Marhan S, Marshall M, Meir P, Miao Y, Muhr J, Niklaus PA, Ogaya R, Peñuelas J, Poll C, Rustad LE, Savage K, Schindlbacher A, Schmidt IK, Smith AR, Sotta ED, Suseela V, Tietema A, van Gestel N, van Straaten O, Wan S, Weber U, Janssens IA. 2014. Can current moisture responses predict soil CO2 efflux under altered precipitation regimes? A synthesis of manipulation experiments. Biogeosciences 11:2991–3013.

    CAS  Article  Google Scholar 

  56. von Lützow M, Kögel-Knabner I. 2009. Temperature sensitivity of soil organic matter decomposition—what do we know? Biol Fertil Soils 46:1–15.

    Article  Google Scholar 

  57. Wang WJ, Dalal RC, Moody PW, Smith CJ. 2003. Relationships of soil respiration to microbial biomass, substrate availibility and clay content. Soil Biol Biochem 35:273–84.

    CAS  Article  Google Scholar 

  58. Wang C, Yang J, Zhang Q. 2006. Soil respiration in six temperate forests in China. Glob Change Biol 12:2103–14.

    Article  Google Scholar 

  59. Wang B, Zha TS, Jia X, Wu B, Zhang YQ, Qin SG. 2014. Soil moisture modifies the response of soil respiration to temperature in a desert shrub ecosystem. Biogeosciences 11:259–68.

    Article  Google Scholar 

  60. Wu Z, Dijkstra P, Koch GW, Peñuelas J, Hungate BA. 2011. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Change Biol 17:927–42.

    Article  Google Scholar 

  61. Xu L, Baldocchi DD, Tang J. 2004. How soil moisture, rain pulses, and growth alter the response of ecosystem respiration to temperature. Glob Biogeochem Cycles 18:GB4002.

    Google Scholar 

  62. Yan L, Chen S, Huang J, Lin G. 2011. Water regulated effects of photosynthetic substrate supply on soil respiration in a semiarid steppe. Glob Change Biol 17:1990–2001.

    Article  Google Scholar 

  63. Zeileis A, Hothorn T, Hornik K. 2005. Model-based recursive partitioning. J Comput Graph Stat 17:492–514.

    Article  Google Scholar 

  64. Zhang LH, Chen YN, Zhao RF, Li WH. 2010. Significance of temperature and soil water content on soil respiration in three desert ecosystems in Northwest China. J Arid Environ 74:1200–11.

    Article  Google Scholar 

  65. Zhou X, Sherry RA, An Y, Wallace LL, Luo Y. 2006. Main and interactive effects of warming, clipping, and doubled precipitation on soil CO2 efflux in a grassland ecosystem. Glob Biogeochem Cycles 20:GB1003.

    Google Scholar 

  66. Zhou X, Wan SQ, Luo YQ. 2007. Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Glob Change Biol 13:761–75.

    Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the support of the INCREASE Project (http://increase.ku.dk) funded by the EC FP7-Infrastructure-2008-1 Grant Agreement 227628, and the Hungarian Scientific Research Fund (OTKA K112576 and PD115637). ME and JP research was supported by the European Research Council Synergy Grant ERC-2013-SyG-610028 IMBALANCE-P, the Spanish Government Grant CGL2013-48074-P and the Catalan Government Grant SGR 2014-274. We thank the two anonymous reviewers for helpful comments and suggestions.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Eszter Lellei-Kovács.

Additional information

Author contributions

EKL and ELK conceived the study; ELK, GDD, ME, GG, GRK, GKD, KSL, JP, ARS, AS, AT and IKS performed the research; BDZ and ELK analyzed the data; and ELK wrote the paper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 117 kb)

Supplementary material 2 (PDF 350 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lellei-Kovács, E., Botta-Dukát, Z., de Dato, G. et al. Temperature Dependence of Soil Respiration Modulated by Thresholds in Soil Water Availability Across European Shrubland Ecosystems. Ecosystems 19, 1460–1477 (2016). https://doi.org/10.1007/s10021-016-0016-9

Download citation

Keywords

  • annual soil respiration
  • empirical soil respiration models
  • soil moisture threshold
  • shrubland
  • temperature dependence
  • temperature sensitivity