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.

  • Letter
  • Published:

Unexpected changes in community size structure in a natural warming experiment

Abstract

Natural ecosystems typically consist of many small and few large organisms1,2,3,4. The scaling of this negative relationship between body mass and abundance has important implications for resource partitioning and energy usage5,6,7. Global warming over the next century is predicted to favour smaller organisms8,9,10,11,12, producing steeper mass–abundance scaling13 and a less efficient transfer of biomass through the food web5. Here, we show that the opposite effect occurs in a natural warming experiment involving 13 whole-stream ecosystems within the same catchment, which span a temperature gradient of 5–25 °C. We introduce a mechanistic model that shows how the temperature dependence of basal resource carrying capacity can account for these previously unexpected results. If nutrient supply increases with temperature to offset the rising metabolic demand of primary producers, there will be sufficient resources to sustain larger consumers at higher trophic levels. These new data and the model that explains them highlight important exceptions to some commonly assumed ‘rules’ about responses to warming in natural ecosystems.

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

Figure 1: Map of the geothermal streams and effects of temperature on mass–abundance (MN) scaling.
Figure 2: A mechanistic model helps reveal the underlying processes of the stream ecosystems.

Similar content being viewed by others

References

  1. Jonsson, T., Cohen, J. E. & Carpenter, S. R. Food webs, body size, and species abundance in ecological community description. Adv. Ecol. Res. 36, 1–84 (2005).

    Article  Google Scholar 

  2. Marquet, P. A., Navarrete, S. A. & Castilla, J. C. Scaling population-density to body size in rocky intertidal communities. Science 250, 1125–1127 (1990).

    Article  CAS  Google Scholar 

  3. O’Gorman, E. J. & Emmerson, M. C. Body mass-abundance relationships are robust to cascading effects in marine food webs. Oikos 120, 520–528 (2011).

    Article  Google Scholar 

  4. Reuman, D. C., Mulder, C., Raffaelli, D. & Cohen, J. E. Three allometric relations of population density to body mass: theoretical integration and empirical tests in 149 food webs. Ecol. Lett. 11, 1216–1228 (2008).

    Article  Google Scholar 

  5. Jennings, S. & Blanchard, J. L. Fish abundance with no fishing: predictions based on macroecological theory. J. Anim. Ecol. 73, 632–642 (2004).

    Article  Google Scholar 

  6. White, E. P., Ernest, S. K. M., Kerkhoff, A. J. & Enquist, B. J. Relationships between body size and abundance in ecology. Trends Ecol. Evol. 22, 323–330 (2007).

    Article  Google Scholar 

  7. Woodward, G. et al. Body size in ecological networks. Trends Ecol. Evol. 20, 402–409 (2005).

    Article  Google Scholar 

  8. Daufresne, M., Lengfellner, K. & Sommer, U. Global warming benefits the small in aquatic ecosystems. Proc. Natl Acad. Sci. USA 106, 12788–12793 (2009).

    Article  CAS  Google Scholar 

  9. Moran, X. A. G., Lopez-Urrutia, A., Calvo-Diaz, A. & Li, W. K. W. Increasing importance of small phytoplankton in a warmer ocean. Glob. Change Biol. 16, 1137–1144 (2010).

    Article  Google Scholar 

  10. Sheridan, J. A. & Bickford, D. Shrinking body size as an ecological response to climate change. Nat. Clim. Change 1, 401–406 (2011).

    Article  Google Scholar 

  11. Petchey, O. L., McPhearson, P. T., Casey, T. M. & Morin, P. J. Environmental warming alters food-web structure and ecosystem function. Nature 402, 69–72 (1999).

    Article  CAS  Google Scholar 

  12. Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).

    Article  Google Scholar 

  13. Yvon-Durocher, G., Montoya, J. M., Trimmer, M. & Woodward, G. Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Glob. Change Biol. 17, 1681–1694 (2011).

    Article  Google Scholar 

  14. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article  Google Scholar 

  15. Rice, J. & Gislason, H. Patterns of change in the size spectra of numbers and diversity of the North Sea fish assemblage, as reflected in surveys and models. ICES J. Mar. Sci. 53, 1214–1225 (1996).

    Article  Google Scholar 

  16. Binzer, A., Guill, C., Brose, U. & Rall, B. C. The dynamics of food chains under climate change and nutrient enrichment. Phil. Trans. R. Soc. B 367, 2935–2944 (2012).

    Article  Google Scholar 

  17. Fussmann, K. E., Schwarzmüller, F., Brose, U., Jousset, A. & Rall, B. C. Ecological stability in response to warming. Nat. Clim. Change 4, 206–210 (2014).

    Article  Google Scholar 

  18. DeLong, J. P. Experimental demonstration of a ‘rate–size’ trade-off governing body size optimization. Evol. Ecol. Res. 14, 343–352 (2012).

    Google Scholar 

  19. Reuman, D. C., Holt, R. D. & Yvon-Durocher, G. A metabolic perspective on competition and body size reductions with warming. J. Anim. Ecol. 83, 59–69 (2014).

    Article  Google Scholar 

  20. Adams, G. et al. Diatoms can be an important exception to temperature-size rules at species and community levels of organization. Glob. Change Biol. 19, 3540–3552 (2013).

    Google Scholar 

  21. Friberg, N. et al. Relationships between structure and function in streams contrasting in temperature. Freshwat. Biol. 54, 2051–2068 (2009).

    Article  CAS  Google Scholar 

  22. O’Gorman, E. J. et al. Impacts of warming on the structure and function of aquatic communities: individual- to ecosystem-level responses. Adv. Ecol. Res. 47, 81–176 (2012).

    Article  Google Scholar 

  23. Woodward, G. et al. Sentinel systems on the razor’s edge: effects of warming on Arctic geothermal stream ecosystems. Glob. Change Biol. 16, 1979–1991 (2010).

    Article  Google Scholar 

  24. Demars, B. O. L. et al. Temperature and the metabolic balance of streams. Freshwat. Biol. 56, 1106–1121 (2011).

    Article  Google Scholar 

  25. O’Gorman, E. J. et al. Climate change and geothermal ecosystems: natural laboratories, sentinel systems, and future refugia. Glob. Change Biol. 20, 3291–3299 (2014).

    Article  Google Scholar 

  26. Gilbert, B. et al. A bioenergetic framework for the temperature dependence of trophic interactions. Ecol. Lett. 17, 902–914 (2014).

    Article  Google Scholar 

  27. Welter, J. R. et al. Does N2-fixation amplify the temperature dependence of ecosystem metabolism? Ecology 96, 603–610 (2015).

    Article  Google Scholar 

  28. Battin, T. J. et al. Biophysical controls on organic carbon fluxes in fluvial networks. Nat. Geosci. 1, 95–100 (2008).

    Article  CAS  Google Scholar 

  29. Brookshire, E., Valett, H. & Gerber, S. Maintenance of terrestrial nutrient loss signatures during in-stream transport. Ecology 90, 293–299 (2009).

    Article  CAS  Google Scholar 

  30. Elliott, J. & Elliott, J. Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change. J. Fish Biol. 77, 1793–1817 (2010).

    Article  CAS  Google Scholar 

  31. O’Gorman, E. J. et al. Temperature effects on fish production across a natural thermal gradient. Glob. Change Biol. 22, 3206–3220 (2016).

    Article  Google Scholar 

  32. Kratina, P., Greig, H. S., Thompson, P. L., Carvalho-Pereira, T. S. & Shurin, J. B. Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology 93, 1421–1430 (2012).

    Article  Google Scholar 

  33. IPCC Climate Change 2013: The Physical Sciences Basis (eds Stocker, T. F. et al.) 36 (Cambridge Univ. Press, 2013).

  34. Stewart, B. A., Close, P. G., Cook, P. A. & Davies, P. M. Upper thermal tolerances of key taxonomic groups of stream invertebrates. Hydrobiologia 718, 131–140 (2013).

    Article  CAS  Google Scholar 

  35. Nelson, D. et al. Experimental whole-stream warming alters community size structure. Glob. Change Biol. 23, 2618–2628 (2017).

    Article  Google Scholar 

  36. Gudmundsdottir, R. et al. Effects of temperature regime on primary producers in Icelandic geothermal streams. Aquat. Bot. 95, 278–286 (2011).

    Article  Google Scholar 

  37. Hannesdóttir, E. R., Gíslason, G. M., Ólafsson, J. S., Ólafsson, Ó. P. & O’Gorman, E. J. Increased stream productivity with warming supports higher trophic levels. Adv. Ecol. Res. 48, 283–340 (2013).

    Google Scholar 

  38. Arnason, B., Theodorsson, P., Björnsson, S. & Saemundsson, K. Hengill, a high temperature thermal area in Iceland. Bull. Volcanol. 33, 245–259 (1969).

    Article  CAS  Google Scholar 

  39. Abramoff, M. D., Magalhaes, P. J. & Ram, S. J. Image processing with ImageJ. Biophotonics Int. 11, 36–42 (2004).

    Google Scholar 

  40. Sun, J. & Liu, D. Geometric models for calculating cell biovolume and surface area for phytoplankton. J. Plankton Res. 25, 1331–1346 (2003).

    Article  Google Scholar 

  41. Rocha, O. & Duncan, A. The relationship between cell carbon and cell volume in freshwater algal species used in zooplanktonic studies. J. Plankton Res. 7, 279–294 (1985).

    Article  Google Scholar 

  42. Sicko-Goad, L. M., Schelske, C. L. & Stoermer, E. F. Estimation of intracellular carbon and silica content of diatoms from natural assemblages using morphometric techniques. Limnol. Oceanogr. 29, 1170–1178 (1984).

    Article  Google Scholar 

  43. Seber, G. A. F. & Le Cren, E. D. Estimating population parameters from catches large relative to the population. J. Anim. Ecol. 36, 631–643 (1967).

    Article  Google Scholar 

  44. Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R 101–142 (Springer, 2009).

    Book  Google Scholar 

  45. Damuth, J. Population-density and body size in mammals. Nature 290, 699–700 (1981).

    Article  Google Scholar 

  46. Jennings, S. & Mackinson, S. Abundance–body mass relationships in size-structured food webs. Ecol. Lett. 6, 971–974 (2003).

    Article  Google Scholar 

  47. Yodzis, P. & Innes, S. Body size and consumer-resource dynamics. Am. Nat. 139, 1151–1175 (1992).

    Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. Reiss for meiofauna and protist data, N. Craig for laboratory work, A. Moustakas for advice on data analysis, G. M. Gíslason and J. S. Ólafsson for providing research support and facilities, and G. Yvon-Durocher, S. Pawar, M. Trimmer and B. Kordas for helpful comments on earlier drafts. We acknowledge funding from NERC (NE/I009280/2, NE/F013124/1, NE/L011840/1, NE/M020843/1), the Royal Society (RG140601), the British Ecological Society (4009-4884), the National Special Water Program (No. 2009ZX07210-009), the China Scholarship Council (No. 201206730022), the Department of Environmental Protection of Shandong Province (SDHBPJ-ZB-08), the German Research Foundation (FZT 118), the James S. McDonnell Foundation, and NSF (1442595).

Author information

Authors and Affiliations

Authors

Contributions

G.W., N.F. and D.C.R. were responsible for funding application, research design, and planning. E.J.O’G., D.E.P., G.A. and A.S. collected the data. E.J.O’G., B.C.R. and L.Z. analysed the data. L.Z., D.C.R. and H.Z. did the modelling. All authors wrote the paper.

Corresponding authors

Correspondence to Eoin J. O’Gorman, Daniel C. Reuman or Guy Woodward.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 2417 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

O’Gorman, E., Zhao, L., Pichler, D. et al. Unexpected changes in community size structure in a natural warming experiment. Nature Clim Change 7, 659–663 (2017). https://doi.org/10.1038/nclimate3368

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate3368

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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