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:

Fish body sizes change with temperature but not all species shrink with warming

Nature Ecology & Evolution volume 4, pages 809–814 (2020)Cite this article

Subjects

Abstract

Ectotherms generally shrink under experimental warming, but whether this pattern extends to wild populations is uncertain. We analysed ten million visual survey records, spanning the Australian continent and multiple decades and comprising the most common coastal reef fishes (335 species). We found that temperature indeed drives spatial and temporal changes in fish body size, but not consistently in the negative fashion expected. Around 55% of species were smaller in warmer waters (especially among small-bodied species), while 45% were bigger. The direction of a species’ response to temperature through space was generally consistent with its response to temperature increase through time at any given location, suggesting that spatial trends could help forecast fish responses to long-term warming. However, temporal changes were about ten times faster than spatial trends (~4% versus ~40% body size change per 1 °C change through space and time, respectively). The rapid and variable responses of fish size to warming may herald unexpected impacts on ecosystem restructuring, with potentially greater consequences than if all species were shrinking.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Fig. 1: Relative change in mean body length of 335 coastal marine fish species per 1 °C change in SST observed across their geographic distributions.
Fig. 2: Long-term annual relative change in mean body length of 71 species at eight warming locations.

Similar content being viewed by others

Data availability

Underwater visual survey datasets are available through the Reef Life Survey site www.reeflifesurvey.com. The final datasets used in this analysis are available through the code depository at https://github.com/astaaudzi/RLSfishSize and as Supplementary datasets linked to this article.

Code availability

All codes used in this analysis are available at https://github.com/astaaudzi/RLSfishSize.

References

  1. 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 

  2. Blanchard, J. L., Heneghan, R. F., Everett, J. D., Trebilco, R. & Richardson, A. J. From bacteria to whales: using functional size spectra to model marine ecosystems. Trends Ecol. Evol. 32, 174–186 (2017).

    Article  Google Scholar 

  3. Fisher, J. A., Frank, K. T. & Leggett, W. C. Breaking Bergmann’s rule: truncation of Northwest Atlantic marine fish body sizes. Ecology 91, 2499–2505 (2010).

    Article  Google Scholar 

  4. Shackell, N. L., Frank, K. T., Fisher, J. A., Petrie, B. & Leggett, W. C. Decline in top predator body size and changing climate alter trophic structure in an oceanic ecosystem. Proc. R. Soc. Lond. B 277, 1353–1360 (2009).

    Article  Google Scholar 

  5. Rouyer, T., Sadykov, A., Ohlberger, J. & Stenseth, N. C. Does increasing mortality change the response of fish populations to environmental fluctuations? Ecol. Lett. 15, 658–665 (2012).

  6. 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 

  7. Cheung, W. W. et al. Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat. Clim. Change 3, 254–258 (2013).

    Article  Google Scholar 

  8. Pauly, D. & Cheung, W. W. L. Sound physiological knowledge and principles in modeling shrinking of fishes under climate change. Glob. Change Biol. 24, e15–e26 (2018).

    Article  Google Scholar 

  9. Lefevre, S., McKenzie, D. J. & Nilsson, G. E. In modelling effects of global warming, invalid assumptions lead to unrealistic projections. Glob. Change Biol. 24, 553–556 (2018).

    Article  Google Scholar 

  10. Morrongiello, J. R., Sweetman, P. C. & Thresher, R. E. Fishing constrains phenotypic responses of marine fish to climate variability. J. Anim. Ecol. 88, 1645–1656 (2019).

    Article  Google Scholar 

  11. Angilletta, M. J. Jr, Steury, T. D. & Sears, M. W. Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr. Comp. Biol. 44, 498–509 (2004).

    Article  Google Scholar 

  12. Bergman, C. Uber die Verhaltnisse der Warmeokonomie der Thiere zu ihrer Grosse. Gottinger Stud. 3, 595–708 (1847).

    Google Scholar 

  13. Audzijonyte, A. et al. Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? Glob. Ecol. Biogeogr. 28, 64–77 (2019).

    Article  Google Scholar 

  14. Forster, J., Hirst, A. G. & Atkinson, D. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc. Natl Acad. Sci. USA 109, 19310–19314 (2012).

    Article  CAS  Google Scholar 

  15. Lefevre, S., McKenzie, D. J. & Nilsson, G. E. Models projecting the fate of fish populations under climate change need to be based on valid physiological mechanisms. Glob. Change Biol. 23, 3449–3459 (2017).

    Article  Google Scholar 

  16. Pauly, D. The relationships between gill surface area and growth performance in fish: a generalization of von Bertalanffy’s theory of growth. Meeresforschung 28, 251–282 (1981).

    Google Scholar 

  17. Donelson, J. M., Munday, P. L., McCormick, M. I. & Pitcher, C. R. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change 2, 30–32 (2011).

    Article  Google Scholar 

  18. Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, eaai9214 (2017).

    Article  Google Scholar 

  19. Edgar, G. J. & Barrett, N. S. An assessment of population responses of common inshore fishes and invertebrates following declaration of five Australian marine protected areas. Environ. Conserv. 39, 271–281 (2012).

    Article  Google Scholar 

  20. Edgar, G. J. & Stuart-Smith, R. D. Systematic global assessment of reef fish communities by the Reef Life Survey program. Sci. Data 1, 140007 (2014).

    Article  Google Scholar 

  21. Stuart-Smith, R. D., Edgar, G. J., Barrett, N. S., Kininmonth, S. J. & Bates, A. E. Thermal biases and vulnerability to warming in the world’s marine fauna. Nature 528, 88–92 (2015).

    Article  CAS  Google Scholar 

  22. Edgar, G. J., Barrett, N. S. & Morton, A. J. Biases associated with the use of underwater visual census techniques to quantify the density and size-structure of fish populations. J. Exp. Mar. Biol. Ecol. 308, 269–290 (2004).

    Article  Google Scholar 

  23. Waldock, C., Stuart‐Smith, R. D., Edgar, G. J., Bird, T. J. & Bates, A. E. The shape of abundance distributions across temperature gradients in reef fishes. Ecol. Lett. 22, 685–696 (2019).

    Article  Google Scholar 

  24. Bennett, S., Wernberg, T., Joy, B. A., De Bettignies, T. & Campbell, A. H. Central and rear-edge populations can be equally vulnerable to warming. Nat. Commun. 6, 10280 (2015).

    Article  CAS  Google Scholar 

  25. Conover, D. O., Duffy, T. A. & Hice, L. A. The covariance between genetic and environmental influences across ecological gradients: reassessing the evolutionary significance of countergradient and cogradient variation. Ann. N. Y. Acad. Sci. 1168, 100–129 (2009).

    Article  Google Scholar 

  26. Audzijonyte, A., Kuparinen, A. & Fulton, E. A. How fast is fisheries‐induced evolution? Quantitative analysis of modelling and empirical studies. Evol. Appl. 6, 585–595 (2013).

    Article  Google Scholar 

  27. Audzijonyte, A. et al. Trends and management implications of human‐influenced life‐history changes in marine ectotherms. Fish Fish. 17, 1005–1028 (2016).

    Article  Google Scholar 

  28. Fritschie, K. J. & Olden, J. D. Disentangling the influences of mean body size and size structure on ecosystem functioning: an example of nutrient recycling by a non‐native crayfish. Ecol. Evol. 6, 159–169 (2016).

    Article  Google Scholar 

  29. AudzijonyteA., KuparinenA., GortonR. & FultonE. A . Ecological consequences of body size decline in harvested fish species: positive feedback loops in trophic interactions amplify human impact. Biol. Lett. 9, 20121103 (2013).

    Article  Google Scholar 

  30. Jørgensen, C. & Fiksen, Ø. Modelling fishing-induced adaptations and consequences for natural mortality. Can. J. Fish. Aquat. Sci. 67, 1086–1097 (2010).

    Article  Google Scholar 

  31. Edgar, G. J. & Stuart-Smith, R. D. Ecological effects of marine protected areas on rocky reef communities—a continental-scale analysis. Mar. Ecol. Prog. Ser. 388, 51–62 (2009).

    Article  Google Scholar 

  32. Reynolds, R. & Banzon, V. NOAA Optimum Interpolation 1/4 Degree Daily Sea Surface Temperature (OISST) Analysis, Version 2 (NOAA National Centers for Environmental Information, 2008); https://go.nature.com/2WtURVO

  33. Stuart-Smith, R. D., Edgar, G. J. & Bates, A. E. Thermal limits to the geographic distributions of shallow-water marine species. Nat. Ecol. Evol. 1, 1846 (2017).

    Article  Google Scholar 

  34. Stan Development Team RStan: the R interface to Stan. R package version 2.19.2 http://mc-stan.org/ (2019).

Download references

Acknowledgements

We acknowledge all divers and support personnel who contributed to the data collection and repository, especially A. Cooper, J. Berkhout, E. Oh, J. Stuart-Smith, J. Hulls and E. Clausius. We also thank M. Sumner for help with the SST data, F. Heather for help with figures, J. Berkhout for help with parallel computing, and A. Bates and C. Waldock for thermal distribution information. This research used the NCRIS-enabled Integrated Marine Observing System (IMOS) infrastructure for database support and storage. This study was supported by the ARC Discovery grant DP170104240 (to J.L.B., G.P. and R.D.S.-S.), UTAS visiting scholars fellowship (to A.A. for N.P. visit to IMAS), ARC Future Fellowship to G.P., and the Marine Biodiversity Hub, a collaborative partnership supported through the Australian Government’s National Environmental Science Programme (NESP).

Author information

Authors and Affiliations

  1. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia

    Asta Audzijonyte, Rick D. Stuart-Smith, Gretta Pecl, Graham J. Edgar, Neville S. Barrett & Julia L. Blanchard

  2. Centre for Marine Socioecology, University of Tasmania, Hobart, Tasmania, Australia

    Asta Audzijonyte, Gretta Pecl & Julia L. Blanchard

  3. School of Natural Sciences, University of Tasmania, Hobart, Tasmania, Australia

    Shane A. Richards

  4. School of Natural Sciences, Trinity College Dublin, Dublin, Ireland

    Nicholas Payne

Authors
  1. Asta Audzijonyte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shane A. Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rick D. Stuart-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gretta Pecl
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Graham J. Edgar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Neville S. Barrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nicholas Payne
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Julia L. Blanchard
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.A. designed the study and led the writing. A.A. and S.A.R. designed and conducted the statistical analyses. R.D.S.-S., G.J.E. and N.S.B. led field surveys and data collection. G.P., N.P. and J.L.B. contributed critically to the development of the study. All authors contributed to the manuscript writing and gave final approval for publication.

Corresponding author

Correspondence to Asta Audzijonyte.

Ethics declarations

Competing interests

The authors declare no competing interests.

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 Spatial distribution of Australian fish survey data used, coloured according to the mean annual sea surface temperature.

All sites are grouped onto 0.5 degree grid cells. Colours represent mean annual SST over the entire sampling period in that cell (ranging from 12 °C for yellow to 29 °C for red) and circle size is proportional to the total number of species used for the analyses in the cell (determined by species richness and number of surveys in the cell). Black stars indicate the nine long-term monitoring locations. The Australian coastline shapefile was downloaded from the Australian Natural Resources Data Library website (Commonwealth of Australia).

Extended Data Fig. 2 Correlation between species body size – SST slopes and abundance – SST slopes from literature.

Species-specific slopes between body size and mean annual SST through space (β1, on y axis) are compared with the species specific abundance and mean annual SST slopes estimated in Waldock et al. (2019). Data on both slopes was available for 300 species. If abundance was a major driver of average body size, we could expect an overall negative correlation between size-temperature and abundance-temperature slopes, such as mean body size is smaller at sites with higher abundances. Alternatively, larger average body sizes might have positive effects on abundance through e.g. improved recruitment or inter-specific effects. In this case we could expect a positive correlation between size-temperature and abundance-temperature slopes. The correlation between body size slopes and abundances was close to zero (r = 0.09, P = 0.14), suggesting that abundance is unlikely to be a major driver of body sizes and vice versa.

Extended Data Fig. 3 Species-specific body length changes at nine long-term monitored and warming locations.

Location and species specific temporal responses, represented by slopes of body length change in 105 coastal fish species in nine warming and long-term monitored locations. Each dot represents a species, arranged according to the temperature at the centre of their distribution area (temperature midpoint). Blue and red colours indicate species for which 90% of the posterior probability density range for the slope of the annual body length change (on y axis) was above or below zero, respectively. For the map of the nine locations see Extended Data Fig. 1.

Supplementary information

Supplementary Information

Supplementary Tables 2 and 3, and Figs. 1–4.

Reporting Summary

Supplementary Tables 1 and 4

List of Bayesian estimates of body size–SST slopes through space for each of the 335 individual species used in the analyses (Supplementary Table 1) and Bayesian estimates of annual changes in body lengths (slopes of size versus year) in nine long-term locations (Supplementary Table 4).

Supplementary Data

Filtered and final datasets used in the analyses.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Audzijonyte, A., Richards, S.A., Stuart-Smith, R.D. et al. Fish body sizes change with temperature but not all species shrink with warming. Nat Ecol Evol 4, 809–814 (2020). https://doi.org/10.1038/s41559-020-1171-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-1171-0

This article is cited by

Search

Advanced 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