Coral Reefs

, Volume 38, Issue 3, pp 527–537 | Cite as

Changes in sociality of butterflyfishes linked to population declines and coral loss

  • Cassandra A. Thompson
  • Samuel Matthews
  • Andrew S. Hoey
  • Morgan S. PratchettEmail author


Degradation and loss of reef habitat is one of the foremost threats to coral reef fishes, especially for highly specialised species with specific reliance on live corals. Aside from affecting the carrying capacity of local environments, declines in the quality and quantity of critical reef habitats may lead to changes in behaviour, condition and fitness of individual fishes. This study explores changes in the sociality (specifically, the proportion of individuals observed in pairs) for coral reef butterflyfishes over a 15-yr period, in the northern Great Barrier Reef. During the study period where there were significant disturbances that reduced coral cover, there were also sustained declines in abundance of many butterflyfishes. Across five species of pairing butterflyfishes (Chaetodon baronessa, C. lunulatus, C. citrinellus, C. auriga and C. vagabundus), the overall proportion of individuals in pairs varied among the three surveys (2002, 2009, and 2017) and was positively correlated with live coral cover. This pattern was most apparent for, and largely driven by changes in sociality of, C. baronessa. Declines in incidence of pairing may suggest that pairing is untenable as prey becomes limiting, or elevated rates of adult mortality increasingly disrupt patterns of sociality. Disruptions to sociality, and thereby reproductive systems, may add to population declines and greatly constrain subsequent recovery and resilience of populations. For other more generalist or non-coral feeders, the relative incidence of pairing actually increased due to disproportionate declines in abundance of solitary individuals.


Chaetodontidae Coral reefs Coral loss Disturbance Sociality 



Annual surveys of butterflyfishes and corals were undertaken with assistance from ML Berumen, A Cole, R Lawton and DJ Pratchett. This research was supported by the ARC Centre of Excellence for Coral Reef Studies, as well as the Lizard Island Research Station. On behalf of all authors, the corresponding author states that there is no conflict of interest.


  1. Almany GR (2004) Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141:105–113CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1(7):1–23Google Scholar
  3. Bellwood DR, Goatley CHR, Cowman PF, Bellwood O (2015) The evolution of fishes on coral reefs: fossils, phylogenies and functions. In: Mora C (ed) Ecology of Fishes on Coral Reefs. Cambridge University Press, Cambridge, pp 55–63CrossRefGoogle Scholar
  4. Berumen ML, Pratchett MS (2006) Effects of resource availability on the competitive behaviour of butterflyfishes (Chaetodontidae). Proc 10th Int Coral Reef Symp 1:644-650Google Scholar
  5. Berumen ML, Pratchett MS, McCormick MI (2005) Within-reef differences in diet and body condition of coral-feeding butterflyfishes (Chaetodontidae). Marine Ecology Progress Series 287:217–227. CrossRefGoogle Scholar
  6. Berumen ML, Trip EDL, Pratchett MS, Choat JH (2012) Differences in demographic traits of four butterflyfish species between two reefs of the Great Barrier Reef separated by 1,200 km. Coral Reefs 31:169–177CrossRefGoogle Scholar
  7. Blowes SA, Pratchett MS, Connolly SR (2013) Heterospecific aggression and dominance in a guild of coral-feeding fishes: the roles of dietary ecology and phylogeny. Am Nat 182:157–168CrossRefGoogle Scholar
  8. Bouchon-Navaro Y (1981) Quantitative distribution of the Chaetodontidae on a reef of Moorea Island (French Polynesia). J Exp Mar Biol Ecol 55:145–157CrossRefGoogle Scholar
  9. Bouchon-Navaro Y, Bouchon C, Harmelin-Vivien ML (1985) Impact of coral degradation on a chaetodontid fish assemblage (Moorea, French Polynesia). Proc 5th Coral Reef Symp 5:427-432Google Scholar
  10. Brandl SJ, Bellwood DR (2014) Pair-formation in coral reef fishes: an ecological perspective. Oceanogr Mar Biol Ann Rev 52:1–80Google Scholar
  11. Brandl SJ, Bellwood DR (2015) Coordinated vigilance provides evidence for direct reciprocity in coral reef fishes. Sci Rep 5:14556CrossRefGoogle Scholar
  12. Brooker RM, Jones GP, Munday PL (2013) Prey selectivity affects reproductive success of a corallivorous reef fish. Oecologia 172:409–416CrossRefGoogle Scholar
  13. Bruno JF, Selig ER (2007) Regional decline of coral cover in the indo-pacific: Timing, extent, and subregional comparisons. PLoS ONE 2:e711CrossRefGoogle Scholar
  14. Ceccarelli DM, Emslie MJ, Richards ZT (2016) Post-disturbance stability of fish assemblages measured at coarse taxonomic resolution masks change at finer scales. PloS ONE 11:e0156232CrossRefGoogle Scholar
  15. Cheal AJ, MacNeil MA, Emslie MJ, Sweatman H (2017) The threat to coral reefs from more intense cyclones under climate change. Global Change Biol 23:1511–1524CrossRefGoogle Scholar
  16. Chivers DP, McCormick MI, Allan BJ, Ferrari MC (2016) Risk assessment and predator learning in a changing world: understanding the impacts of coral reef degradation. Sci Rep 6:32542CrossRefGoogle Scholar
  17. Cole AJ, Pratchett MS (2014) Diversity in diet and feeding behaviour of butterflyfishes: reliance on reef corals versus reef habitats. In: Pratchett MS, Berumen ML, Kapoor BG (eds) Biology of Butterflyfishes. CRC Press, Boca Raton, pp 107–139Google Scholar
  18. Cole AJ, Pratchett MS, Jones GP (2008) Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish and Fisheries 9:286–307CrossRefGoogle Scholar
  19. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci 109:17995–17999CrossRefGoogle Scholar
  20. Dixson DL, Abrego D, Hay ME (2014) Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345:892–897CrossRefGoogle Scholar
  21. Dunbar RI, Shultz S (2010) Bondedness and sociality. Behav 147:775–803Google Scholar
  22. Emslie MJ, Pratchett MS, Cheal AJ (2011) Effects of different disturbance types on butterflyfish communities of Australia’s Great Barrier Reef. Coral Reefs 30:461–471CrossRefGoogle Scholar
  23. Feary DA, Almany GR, McCormick MI, Jones GP (2007) Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153:727–737CrossRefGoogle Scholar
  24. Fricke HW (1986) Pair swimming and mutual partner guarding in monagomous butterflyfish (Pisces, Chaetodontidae): a joint advertisement for territory. Ethol 73:307–333CrossRefGoogle Scholar
  25. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci 103:8425–8429CrossRefGoogle Scholar
  26. Halford A, Cheal AJ, Ryan D, Williams DM (2004) Resilience to large scale disturbance in coral and fish assemblages on the great barrier reef. Ecol 85:1892–1905CrossRefGoogle Scholar
  27. Hing ML, Klanten OS, Dowton M, Brown KR, Wong MYL (2018) Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes. PLoS ONE 13:e0202407CrossRefGoogle Scholar
  28. Hoey AS, Howells E, Johansen JL, Hobbs J-PA, Messmer V, McCowan DM, Wilson SK, Pratchett MS (2016) Recent advances in understanding the effects of climate change on coral reefs. Diversity 8:d8020012CrossRefGoogle Scholar
  29. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C-Y, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefGoogle Scholar
  30. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83CrossRefGoogle Scholar
  31. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proceedings of the National Academy of Science 101(21):8251–8253. CrossRefGoogle Scholar
  32. Keith SA, Baird AH, Hobbs J-PA, Woolsey ES, Hoey AS, Fadli N, Sanders NJ (2018) Synchronous behavioural shifts in reef fishes linked to mass coral bleaching. Nature Climate Change 8:986–991CrossRefGoogle Scholar
  33. Khan JA, Goatley CH, Brandl SJ, Tebbett SB, Bellwood DR (2017) Shelter use by large reef fishes: long-term occupancy and the impacts of disturbance. Coral Reefs 36:1123–1132CrossRefGoogle Scholar
  34. Kokita T, Nakazono A (2001) Rapid response of an obligately corallivorous filefish Oxymonocanthus longirostris (Monacanthidae) to a mass coral bleaching event. Coral Reefs 20:155–158CrossRefGoogle Scholar
  35. Madin JS, Baird AH, Bridge TC, Connolly SR, Zawada KJ, Dornelas M (2018) Cumulative effects of cyclones and bleaching on coral cover and species richness at Lizard Island. Marine Ecology Progress Series 604:263–268CrossRefGoogle Scholar
  36. Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Global Change Biol 10:1642–1647CrossRefGoogle Scholar
  37. Nagelkerken I, van der Velde G, Wartenbergh SLJ, Nugues MM, Pratchett MS (2009) Cryptic dietary components reduce dietary overlap among sympatric butterflyfishes (Chaetdontidae). J Fish Biol 75:1123–1143CrossRefGoogle Scholar
  38. Nowicki JP, Walker SPW, Coker DJ, Hoey AS, Nicolet KJ, Pratchett MS (2018a) Pair bond endurance promotes cooperative food defense and inhibits conflict in coral reef butterflyfish. Sci Rep 8:6295CrossRefGoogle Scholar
  39. Nowicki JP, O’Connell LA, Cowman PF, Walker SPW, Coker DJ, Pratchett MS (2018b) Variation in social systems within Chaetodon butterflyfishes, with special reference to pair bonding. PloS ONE 13:e0194465CrossRefGoogle Scholar
  40. Pratchett MS (2005) Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar Biol 148:373–382CrossRefGoogle Scholar
  41. Pratchett MS (2007) Dietary selection by coral-feeding butterflyfishes (Chaetodontidae) on the Great Barrier Reef, Australia. Raffles Bull Zool S14:155–160Google Scholar
  42. Pratchett MS, Wilson SK, Berumen ML, McCormick MI (2004) Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23:352–356CrossRefGoogle Scholar
  43. Pratchett MS, Wilson SK, Baird AH (2006a) Declines in abundance of Chaetodon butterflyfishes following extensive coral depletion. J Fish Biol 69:1269–1280CrossRefGoogle Scholar
  44. Pratchett MS, Pradjakusuma OA, Jones GP (2006b) Is there a reproductive basis to solitary living versus pair-formation in coral reef fishes? Coral Reefs 25:85–92CrossRefGoogle Scholar
  45. Pratchett MS, Munday PL, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes: ecological and economic consequences. Oceanogr Mar Biol Ann Rev 46:251–296Google Scholar
  46. Pratchett MS, Blowes SA, Coker D, Kubacki E, Nowiki J, Hoey AS (2015) Indirect benefits of high coral cover for non-corallivorous butterflyfishes. Coral Reefs 34:665–672CrossRefGoogle Scholar
  47. Pratchett MS, Thompson CA, Hoey AS, Cowman PF, Wilson SK (2018) Effects of coral bleaching and coral loss on the structure and function of reef fish assemblages. In: van Oppen M, Lough J (eds) Coral bleaching: Patterns, processes, causes and consequences -, 2nd edn. Springer, Cham, pp 265–293CrossRefGoogle Scholar
  48. Reese ES (1975) A comparative field study of the social behavior and related ecology of reef fishes of the family Chaetodontidae. Ethol 37:37–61Google Scholar
  49. Reese ES (1977) Coevolution of corals and coral feeding fishes of the family Chaetodontidae. Proc 3rd Int Coral Reef Symp 1:267-274Google Scholar
  50. Reese ES (1981) Predation on corals by fishes of the family Chaetodontidae: implications for the conservation and management of coral reef ecosystems. Bull Mar Sci 31:594–604Google Scholar
  51. Richardson LE, Graham NAJ, Pratchett MS, Eurich JG, Hoey AS (2018) Mass coral bleaching causes biotic homogenization of reef fish assemblages. Global Change Biol 24:3117–3129CrossRefGoogle Scholar
  52. Righton D (1998) Modelling the effect of resource renewal on the social dynamics of butterflyfishes. Mar FW Behav Physiol 31:215–229CrossRefGoogle Scholar
  53. Sano M, Shimizu M, Nose Y (1984) Changes in structure of coral reef fish communities by destruction of hermatypic corals: observational and experimental views. Pac Sci 38:51–79Google Scholar
  54. Sano M, Shimizu M, Nose Y (1987) Long-term effects of destruction of hermatypic corals by Acanthaster planci infestation on reef fish communities at Iriomote Island, Japan. Mar Ecol Prog Ser 37:191–199CrossRefGoogle Scholar
  55. Tricas TC (1989) Determinants of feeding territory size in the corallivorous butterflyfish, Chaetodon multicinctus. An Behav 37:830–841CrossRefGoogle Scholar
  56. Uthicke S, Doyle J, Duggan S, Yasuda N, McKinnon AD (2015) Outbreak of coral-eating crown-of-thorns creates continuous cloud of larvae over 320 km of the Great Barrier Reef. Sci Rep 5:16885CrossRefGoogle Scholar
  57. Whiteman EA, Côté IM (2004) Monogamy in marine fishes. Biol Rev 79:351–375CrossRefGoogle Scholar
  58. Williams DM (1986) Temporal variation in the structure of reef slope fish communities (central Great Barrier Reef): short-term effects of Acanthaster planci infestation. Mar Ecol Prog Ser 28:157–164CrossRefGoogle Scholar
  59. Williams AH, Sale PF (1981) Spatial and temporal patterns of recruitment of juvenile coral reef fishes to coral habitats within “One Tree Lagoon”, Great Barrier Reef. Mar Biol 65:245–253CrossRefGoogle Scholar
  60. Wilson EO (2000) Sociobiology: the new synthesis. Harvard University Press, USAGoogle Scholar
  61. Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Pulunin N (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Global Change Biol 12:1–15CrossRefGoogle Scholar
  62. Wilson SK, Graham NAJ, Pratchett MS (2014) Susceptibility of butterflyfish to habitat disturbance: Do ‘chaets’ ever prosper? In: Pratchett MS, Berumen ML, Kapoor B (eds) Biology of butterflyfishes. CRC, Boca Raton, pp 226–245Google Scholar
  63. Wolff NH, Wong A, Vitolo R, Stolberg K, Anthony KRN, Mumby PJ (2016) Temporal clustering of tropical cyclones on the Great Barrier Reef and its ecological importance. Coral Reefs 35:613–623CrossRefGoogle Scholar
  64. Yabuta S (2002) Uncertainty in partner recognition and the tail-up display in a monogamous butterflyfish. An Behav 63:165–173CrossRefGoogle Scholar
  65. Yabuta S (2007) Social groupings in 18 species of butterflyfish and pair bond weakening during the nonreproductive season. Ichthyol Res 54:207–210CrossRefGoogle Scholar
  66. Yabuta S (1997) Spawning migrations in the monogamous butterflyfish, Chaetodon trifasciatus. Ichthyol Res 44:177–182CrossRefGoogle Scholar
  67. Yabuta S, Berumen ML (2014) Social structure and spawning behavior of Chaetodon butterflyfishes. In: Pratchett MS, Berumen ML, Kapoor BG (eds) Biology of Butterflyfishes. CRC Press, Boca Raton, pp 200–225Google Scholar
  68. Yabuta S, Kawahima M (1997) Spawning behaviour and haremic mating system in the corallivorous butterflyfish, Chatodon trifascialis, at Kuroshima Island, Okinawa. Ichthyol Res 44:183–188CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia

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