Reduced feeding activity of soil detritivores under warmer and drier conditions


Anthropogenic warming is projected to trigger positive feedbacks to climate by enhancing carbon losses from the soil1. While such losses are, in part, due to increased decomposition of organic matter by invertebrate detritivores, it is unknown how detritivore feeding activity will change with warming2, especially under drought conditions. Here, using four-year manipulation experiments in two North American boreal forests, we investigate how temperature (ambient, ambient + 1.7 °C and ambient + 3.4 °C) and rainfall (ambient and –40% of the summer precipitation) perturbations influence detritivore feeding activity. In contrast to general expectations1,3, warming had negligible net effects on detritivore feeding activity at ambient precipitation. However, when combined with precipitation reductions, warming decreased feeding activity by ~14%. Across all plots and dates, detritivore feeding activity was positively associated with bulk soil microbial respiration. These results suggest slower rates of decomposition of soil organic matter and thus reduced positive feedbacks to climate under anthropogenic climate change.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Soil detritivore feeding activity in response to experiment warming and reduced precipitation.
Fig. 2: Interactive effects of soil temperature and soil water content on the feeding activity of soil detritivores.


  1. 1.

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

  2. 2.

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

  3. 3.

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

  4. 4.

    Adl, S. The Ecology of Soil Decomposition (CABI Publishing, Trowbridge, 2003).

  5. 5.

    Wolters, V. Invertebrate control of soil organic matter stability. Biol. Fertil. Soils 31, 1–19 (2000).

  6. 6.

    Prescott, C. E. Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101, 133–149 (2010).

  7. 7.

    Six, J., Conant, R. T., Paul, E. A. & Paustian, K. Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241, 155–176 (2002).

  8. 8.

    Jastrow, J. D., Amonette, J. E. & Bailey, V. L. Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Clim. Change 80, 5–23 (2007).

  9. 9.

    Verhoef, H. & Brussaard, L. Decomposition and nitrogen mineralization in natural and agroecosystems: the contribution of soil animals. Biogeochemistry 11, 175–211 (1990).

  10. 10.

    Seastedt, T. The role of microarthropods in decomposition and mineralization processes. Annu. Rev. Entomol. 29, 25–46 (1984).

  11. 11.

    Pries, C. E. H., Castanha, C., Porras, R. & Torn, M. S. The whole-soil carbon flux in response to warming. Science 355, 1420–1423 (2017).

  12. 12.

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

  13. 13.

    Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).

  14. 14.

    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).

  15. 15.

    Bradford, M. A. Thermal adaptation of decomposer communities in warming soils. Front. Microbiol. 4, 1–16 (2013).

  16. 16.

    Crowther, T. W. & Bradford, M. A. Thermal acclimation in widespread heterotrophic soil microbes. Ecol. Lett. 16, 469–477 (2013).

  17. 17.

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

  18. 18.

    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).

  19. 19.

    Sihi, D., Inglett, P., Gerber, S. & Inglett, K. Rate of warming affects temperature sensitivity of anaerobic peat decomposition and greenhouse gas production. Glob. Change Biol. (2017).

  20. 20.

    Sinsabaugh, R. L., Manzoni, S., Moorhead, D. L. & Richter, A. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol. Lett. 16, 930–939 (2013).

  21. 21.

    Hagerty, S. B. et al. Accelerated microbial turnover but constant growth efficiency with warming in soil. Nat. Clim. Change 4, 903–906 (2014).

  22. 22.

    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).

  23. 23.

    Lang, B., Rall, B. C. & Brose, U. Warming effects on consumption and intraspecific interference competition depend on predator metabolism. J. Anim. Ecol. 81, 516–523 (2012).

  24. 24.

    A’Bear, A. D., Boddy, L. & Hefin Jones, T. Impacts of elevated temperature on the growth and functioning of decomposer fungi are influenced by grazing collembola. Glob. Change Biol. 18, 1823–1832 (2012).

  25. 25.

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

  26. 26.

    Conant, R. T. et al. Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob. Change Biol. 17, 3392–3404 (2011).

  27. 27.

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

  28. 28.

    Allison, S. D. & Treseder, K. K. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob. Change Biol. 14, 2898–2909 (2008).

  29. 29.

    IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team et al.) (IPCC, 2014). 

  30. 30.

    Schindlbacher, A. et al. Soil respiration under climate change: prolonged summer drought offsets soil warming effects. Glob. Change Biol. 18, 2270–2279 (2012).

  31. 31.

    IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2014).

  32. 32.

    Rich, R. et al. Design and performance of combined infrared canopy and belowground warming in the B4WarmED (Boreal Forest Warming at an Ecotone in Danger) experiment. Glob. Change Biol. 21, 2334–2348 (2015).

  33. 33.

    Von Torne, E. Assessing feeding activities of soil-living animals. I. Bait-lamina-tests. Pedobiologia 34, 89–101 (1990).

  34. 34.

    Rall, B. C. et al. Universal temperature and body-mass scaling of feeding rates. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 2923–2934 (2012).

  35. 35.

    Lindberg, N., Engtsson, J. B. & Persson, T. Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. J. Appl. Ecol. 39, 924–936 (2002).

  36. 36.

    Staley, J. T. et al. Effects of summer rainfall manipulations on the abundance and vertical distribution of herbivorous soil macro-invertebrates. Eur. J. Soil Biol. 43, 189–198 (2007).

  37. 37.

    Eisenhauer, N. et al. Warming shifts ‘worming’: effects of experimental warming on invasive earthworms in northern North America. Sci. Rep. 4, 6890 (2014).

  38. 38.

    Vasseur, D. A. & McCann, K. S. A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. Am. Nat. 166, 184–198 (2005).

  39. 39.

    Brown, J., Gillooly, J., Allen, A. & Savage, V. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

  40. 40.

    Lang, B., Rall, B. C., Scheu, S. & Brose, U. Effects of environmental warming and drought on size-structured soil food webs. Oikos 123, 1224–1233 (2013).

  41. 41.

    Gongalsky, K. B., Persson, T. & Pokarzhevskii, A. D. Effects of soil temperature and moisture on the feeding activity of soil animals as determined by the bait-lamina test. Appl. Soil Ecol. 39, 84–90 (2008).

  42. 42.

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

  43. 43.

    Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).

  44. 44.

    Gauthier, S., Bernier, P., Kuuluvainen, T., Shvidenko, A. Z. & Schepaschenko, D. G. Boreal forest health and global change. Science 349, 819–822 (2015).

  45. 45.

    Schindlbacher, A., Jandl, R. & Schindlbacher, S. Natural variations in snow cover do not affect the annual soil CO2 efflux from a mid-elevation temperate forest. Glob. Change Biol. 20, 622–632 (2014).

  46. 46.

    Gelman, A. & Yu-Sung, S. arm: Data Analysis Using Regression and Multilevel/Hierarchical Models. R Package v.1.8-6 (2015).

  47. 47.

    Reich, P. B. et al. Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species. Nat. Clim. Change 5, 148–152 (2015).

  48. 48.

    Eisenhauer, N. et al. Organic textile dye improves the visual assessment of the bait-lamina test. Appl. Soil Ecol. 82, 78–81 (2014).

  49. 49.

    Riutta, T., Clack, H., Crockatt, M. & Slade, E. M. Landscape-scale implications of the edge effect on soil fauna activity in a temperate forest. Ecosystems 19, 534–544 (2016).

  50. 50.

    Simpson, J. E., Slade, E., Riutta, T. & Taylor, M. E. Factors affecting soil fauna feeding activity in a fragmented lowland temperate deciduous woodland. PLoS ONE 7, e29616 (2012).

  51. 51.

    Birkhofer, K. et al. Soil fauna feeding activity in temperate grassland soils increases with legume and grass species richness. Soil Biol. Biochem. 43, 2200–2207 (2011).

  52. 52.

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

  53. 53.

    Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest: Tests in Linear Mixed Effects Models. R Package v.2.0-33 (2016).

  54. 54.

    Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008).

  55. 55.

    Wood, S. N. Generalized Additive Models: an Introduction with R (Chapman and Hall, Boca Raton, USA, CRC, 2006).

  56. 56.

    Wood, S. & Scheipl, F. gamm4: Generalized Additive Mixed Models Using ‘mgcv’ and ‘lme4’. R Package v.0.2-3 (2014).

  57. 57.

    Van Rij, J. & Wieling, M. itsadug: Interpreting Time Series and Autocorrelated Data Using GAMMs. R Package v.2.2 (2016).

  58. 58.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).

Download references


We gratefully acknowledge several interns who spent innumerable hours in the field assessing bait lamina strips. We are thankful to S. Zieger and J. Siebert for providing the images of detritivores and bait lamina strips, respectively. M.P.T. and N.E. acknowledge funding by the Deutsche Forschungsgemeinschaft in the frame of the Emmy Noether research group (Ei 862/2). This project also received support from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement number 677232). Further support came from the German Centre for Integrative Biodiversity Research Halle–Jena–Leipzig, funded by the German Research Foundation (FZT 118). The B4WarmED project is funded by the US Department of Energy (Grant number DE-FG02-07ER64456) and the College of Food, Agricultural and Natural Resource Sciences at the University of Minnesota.

Author information

P.B.R. and S.E.H. conceived the B4WarmED experiment. N.E. conceived the study of soil detritivore feeding activity. A.S., R.R., K.E.R. and W.C.E. collected the data. M.P.T. developed the ideas for this manuscript, analysed the data and wrote the manuscript with substantial input from N.E. and P.B.R. All authors contributed to revisions.

Correspondence to Madhav P. Thakur.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Figures 1–12 and Supplementary Table 1.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Thakur, M.P., Reich, P.B., Hobbie, S.E. et al. Reduced feeding activity of soil detritivores under warmer and drier conditions. Nature Clim Change 8, 75–78 (2018).

Download citation

Further reading