Synchronous behavioural shifts in reef fishes linked to mass coral bleaching


Mass coral bleaching causes population declines and mortality of coral reef species1 yet its impacts on behaviour are largely unknown. Here, we unite behavioural theory with community ecology to test whether bleaching-induced mass mortality of corals can cause consistent changes in the behaviour of coral-feeding fishes. We documented 5,259 encounters between individuals of 38 Chaetodon (butterflyfish) species on 17 reefs within the central Indo-Pacific, of which 3,828 were repeated on 10 reefs both before and after the global coral bleaching event in 2016. Aggression between butterflyfishes decreased by two-thirds following large-scale coral mortality, despite no significant change in fish abundance or community composition. Pairwise encounters were most likely to be aggressive between obligate corallivores and on reefs with high coral cover. After bleaching, the proportion of preferred Acropora corals in the diet decreased significantly (up to 85% fewer bites), with no increase in overall bite rate to compensate for the loss of these nutritionally rich corals. The observed reduced aggression at low resource levels due to nutritional deficit follows the predictions of the economic theory of aggressive behaviour2,3. Our results reveal synchronous changes in behaviour in response to coral mortality. Such changes could potentially disrupt territories4, leading to reorganization of ecological communities.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Change in coral cover before and after the 2016 coral bleaching events at each field region across replicate point intercept transects at depths 1–5 m.
Fig. 2: Probability of encounters resulting aggression before and after bleaching.
Fig. 3: Influence of biotic and abiotic factors on the probability of aggression following encounters.
Fig. 4: Change in Acropora spp. cover against change in the proportion of bites on Acropora spp. for obligate and facultative corallivores.
Fig. 5: Mean bite rate (all coral genera) before and after bleaching for each species at each region, and overall for each region.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.


  1. 1.

    Pratchett, M. S. et al. in Oceanography and Marine Biology: An Annual Review Vol. 46 (eds Gibson, R. N. et al.) 251–296 (CRC, Boca Raton, 2008).

  2. 2.

    Peiman, K. S. & Robinson, B. W. Ecology and evolution of resource-related heterospecific aggression. Q. Rev. Biol. 85, 133–158 (2010).

    Article  Google Scholar 

  3. 3.

    Maher, C. R. & Lott, D. F. A review of ecological determinants of territoriality within vertebrate species. Am. Midl. Nat. 143, 1–29 (2000).

    Article  Google Scholar 

  4. 4.

    Samways, M. J. Breakdown of butterflyfish (Chaetodontidae) territories associated with the onset of a mass coral bleaching event. Aquat. Conser. Mar. Freshw. Ecosyst. 15, S101–S107 (2005).

    Article  Google Scholar 

  5. 5.

    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    CAS  Article  Google Scholar 

  6. 6.

    Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D. & Wilson, S. K. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94–97 (2015).

    CAS  Article  Google Scholar 

  7. 7.

    McClanahan, T. R., Weil, E., Cortés, J., Baird, A. H. & Ateweberhan, M. in Coral Bleaching: Patterns, Processes, Causes and Consequences (eds van Oppen, M. J. H. & Lough, J. M.) 121–138 (Springer, Berlin, 2009).

  8. 8.

    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    CAS  Article  Google Scholar 

  9. 9.

    Nagelkerken, I. & Munday, P. L. Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Glob. Change Biol. 22, 974–989 (2016).

    Article  Google Scholar 

  10. 10.

    Keith, S. A. & Bull, J. W. Animal culture impacts species’ capacity to realise climate-driven range shifts. Ecography 40, 296–304 (2017).

    Article  Google Scholar 

  11. 11.

    Grether, G. F., Peiman, K. S., Tobias, J. A. & Robinson, B. W. Causes and consequences of behavioral interference between species. Trends Ecol. Evol. 32, 760–772 (2017).

    Article  Google Scholar 

  12. 12.

    Gause, G. F. The Struggle for Existence (Williams and Wilkins, Baltimore, 1934).

  13. 13.

    Allan, B. J. M., Domenici, P., Watson, S. A., Munday, P. L. & McCormick, M. I. Warming has a greater effect than elevated CO2 on predator-prey interactions in coral reef fish. Proc. R. Soc. B 284, 20170784 (2017).

    Article  Google Scholar 

  14. 14.

    Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).

    CAS  Article  Google Scholar 

  15. 15.

    Browman, H. I. Applying organized scepticism to ocean acidification research. ICES J. Mar. Sci. 73, 529–536 (2016).

    Article  Google Scholar 

  16. 16.

    Sundin, J. et al. Long-term exposure to elevated carbon dioxide does not alter activity levels of a coral reef fish in response to predator chemical cues. Behav. Ecol. Sociobiol. 71, 108 (2017).

    Article  Google Scholar 

  17. 17.

    Connell, J. H. in Experimental Marine Biology (ed. Mariscal, R.) 21–54 (Academic, New York, 1974).

  18. 18.

    Maynard Smith, J. Evolutionary Game Theory (Cambridge Univ. Press, Cambridge, 1982).

  19. 19.

    Blowes, S. A., Pratchett, M. S. & Connolly, S. R. Heterospecific aggression and dominance in a guild of coral-feeding fishes: the roles of dietry ecology and phylogeny. Am. Nat. 182, 157–168 (2013).

    Article  Google Scholar 

  20. 20.

    Yabuta, S. & Berumen, M. L. in Biology of Butterflyfishes (eds Pratchett, M. S. et al.) 200–225 (CRC, Boca Raton, 2014).

  21. 21.

    Stamps, J. A. The relationship between resource competition, risk, and aggression in a tropical territorial lizard. Ecology 58, 349–358 (1977).

    Article  Google Scholar 

  22. 22.

    Toms, J. D. Linking behavior and community ecology: interspecific aggression provides evidence for competition between a migrant and resident warbler. Ethology 119, 1057–1066 (2013).

    Article  Google Scholar 

  23. 23.

    Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, London, 1859).

  24. 24.

    Biro, P. A., Beckmann, C. & Stamps, J. A. Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc. R. Soc. B 277, 71–77 (2010).

    Article  Google Scholar 

  25. 25.

    Pratchett, M. S. in Biology of Butterflyfishes (eds Pratchett, M. S. et al.) 140–179 (CRC, Boca Raton, 2014).

  26. 26.

    Marshall, P. A. & Baird, A. H. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155–163 (2000).

    Article  Google Scholar 

  27. 27.

    Vahl, W. K., Lok, T., van der Meer, J., Piersma, T. & Weissing, F. J. Spatial clumping of food and social dominance affect interference competition among ruddy turnstones. Behav. Ecol. 16, 834–844 (2005).

    Article  Google Scholar 

  28. 28.

    Pratchett, M. S., Wilson, S. K. & Baird, A. H. Long-term monitoring of the Great Barrier Reef. J. Fish. Biol. 69, 1269–1280 (2006).

    Article  Google Scholar 

  29. 29.

    Pratchett, M. S., Wilson, S. K., Berumen, M. L. & McCormick, M. I. Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23, 352–356 (2004).

    Article  Google Scholar 

  30. 30.

    Bonin, M. C., Boström-Einarsson, L., Munday, P. L. & Jones, G. P. The prevalence and importance of competition among coral reef fishes. Annu. Rev. Ecol. Evol. Syst. 46, 169–190 (2015).

    Article  Google Scholar 

  31. 31.

    Chandler, J. F., Burn, D., Berggren, P. & Sweet, M. J. Influence of resource availability on the foraging strategies of the triangle butterflyfish Chaetodon triangulum in the Maldives. PLoS One 11, e0151923 (2016).

    Article  Google Scholar 

  32. 32.

    Tricas, T. C. Determinants of feeding territory size in the corallivorous butterflyfish, Chaetodon multicinctus. Anim. Behav. 37, 830–841 (1989).

    Article  Google Scholar 

  33. 33.

    Nash Suding, K. & Goldberg, D. Do disturbances alter competitive hierarchies? Mechanisms of change following gap creation. Ecology 82, 2133–2149 (2001).

    Article  Google Scholar 

  34. 34.

    Tinbergen, N. The functions of territory. Bird Study 4, 14–27 (1957).

    Article  Google Scholar 

  35. 35.

    Berumen, M. L. & Pratchett, M. S. Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25, 647–653 (2006).

    Article  Google Scholar 

  36. 36.

    Berumen, M. L. & Pratchett, M. S. Effects of resource availability on the competitive behaviour of butterflyfishes (Chaetodontidae). In Proc. 10th International Coral Reef Symposium (ed. Suzuki, Y.) 644–650 (Japanese Coral Reef Society, 2006).

  37. 37.

    Pink, J. R. & Fulton, C. J. Fin spotting: efficacy of manual and video-based visual assessments of reef fish swimming behaviour. J. Exp. Mar. Bio. Ecol. 465, 92–98 (2015).

    Article  Google Scholar 

  38. 38.

    Kulbicki, M. How the acquired behaviour of commercial reef fishes may influence the results obtained from visual censuses. J. Exp. Mar. Bio. Ecol. 222, 11–30 (1998).

    Article  Google Scholar 

  39. 39.

    Pratchett, M. S. Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar. Biol. 148, 373–382 (2005).

    Article  Google Scholar 

  40. 40.

    vegan: Community Ecology Package v.1. 17-6 (R Foundation, 2011);

  41. 41.

    Hodge, J. R., van Herwerden, L. & Bellwood, D. R. Temporal evolution of coral reef fishes: global patterns and disparity in isolated locations. J. Biogeogr. 41, 2115–2127 (2014).

    Article  Google Scholar 

  42. 42.

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    CAS  Article  Google Scholar 

  43. 43.

    rstanarm: Bayesian applied regression modeling via Stan (Stan Development Team, 2016);

  44. 44.

    Monnahan, C. C., Thorson, J. T. & Branch, T. A. Faster estimation of Bayesian models in ecology using Hamiltonian Monte Carlo. Methods Ecol. Evol. 8, 339–348 (2017).

    Article  Google Scholar 

Download references


We are grateful for funding support from VILLUM FONDEN (S.A.K., grant number 10114), the Danish National Research Foundation for support of the Center for Macroecology, Evolution and Climate (grant number DNRF96), and the Australian Research Council Centre of Excellence for Coral Reef Studies (AHB grant number CE140100020). For field assistance and logistical support, we thank N. Maginnis, L. Corner, T. Quimpo, V. Horigue and A. Roan; T. Naruse and R. Yoshida, the University of the Ryukyus Iriomote Field Station; Parks Australia and Christmas Island Divers Association; and R. Trono, A. Trono and staff of the Bontoc Seaview Guesthouse and Mabini Municipal Tourism Office, Batangas, Philippines. We also thank A. MacNeil for statistical advice and N. Graham and I. Hartley for constructive feedback on this manuscript.

Author information




S.A.K. designed the study with input from J-P.A.H., A.H.B. and N.J.S.; S.A.K., J-P.A.H., A.H.B., E.S.W. and A.S.H. collected the data; N.F. provided fieldwork support; S.A.K. analysed the data and wrote the manuscript with contributions from all authors.

Corresponding author

Correspondence to Sally A. Keith.

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.

Supplementary information

Supplementary Information

Supplementary figures 1–6, Supplementary table 1

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Keith, S.A., Baird, A.H., Hobbs, J.A. et al. Synchronous behavioural shifts in reef fishes linked to mass coral bleaching. Nature Clim Change 8, 986–991 (2018).

Download citation

Further reading


Quick links

Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.
Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing