Abstract
The effects of disturbances on coral reef fishes have been extensively documented but most studies have relied on opportunistic sampling following single events. Few studies have the spatial and temporal extent to directly compare the effects of multiple disturbances over a large geographic scale. Here, benthic communities and butterflyfishes on 47 reefs of the Great Barrier Reef were surveyed annually to examine their responses to physical disturbances (cyclones and storms) and/or biological disturbances (bleaching, outbreaks of crown-of-thorns starfish and white syndrome disease). The effects on benthic and butterflyfish communities varied among reefs depending on the structure and geographical setting of each community, on the size and type of disturbance, and on the disturbance history of that reef. There was considerable variability in the response of butterflyfishes to different disturbances: physical disturbances (occurring with or without biological disturbances) produced substantial declines in abundance, whilst biological disturbances occurring on their own did not. Butterflyfishes with the narrowest feeding preferences, such as obligate corallivores, were always the species most affected. The response of generalist feeders varied with the extent of damage. Wholesale changes to the butterflyfish community were only recorded where structural complexity of reefs was drastically reduced. The observed effects of disturbances on butterflyfishes coupled with predictions of increased frequency and intensity of disturbances sound a dire warning for the future of butterflyfish communities in particular and reef fish communities in general.
References
Adjeroud M, Augustin D, Galzin R, Salvat B (2002) Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Mar Ecol Prog Ser 237:121–131
Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y, Lison de Loma T, Penin L, Thibaut L, Vidal-Dupiol J, Salvat B, Galzin R (2009) Recurrent disturbances, recovery trajectories and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28:775–780
Allen GR, Steene R, Allen M (1998) A guide to angelfishes and butterflyfishes. Vanguard Press, Perth, Australia
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141
Bell JD, Galzin R (1984) Influence of live coral cover on coral-reef fish communities. Mar Ecol Prog Ser 15:265–274
Bell JD, Harmelin-Vivien M, Galzin R (1985) Large scale spatial variation of abundance in butterflyfishes (Chaetodontidae) on Polynesian reefs. Proc 5th Int Coral Reef Symp 5:633–641
Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–832
Booth DJ, Beretta GA (2002) Changes in a fish assemblage after a coral bleaching event. Mar Ecol Prog Ser 245:205–212
Bouchon-Navaro Y, Bouchon C, Harmelin-Vivien ML (1985) Impact of coral degradation on a chaetodontid fish assemblage (Moorea, French Polynesia) Proc 5th Int Coral Reef Symp 5:427–432
Bozec YM, Doledec S, Kulbicki M (2005) An analysis of fish-habitat associations on disturbed coral reefs: chaetodontid fishes in New Caledonia. J Fish Biol 66:966–982
Cheal AJ, Wilson SK, Emslie MJ, Dolman AM, Sweatman H (2008) Response of reef fish communities to coral declines on the Great Barrier Reef. Mar Ecol Prog Ser 372:211–223
Cole AJ, Pratchett MS, Jones GP (2008) Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish Fish 9:286–307
Done TJ (1982) Patterns in the distribution in coral communities across the central Great Barrier Reef. Coral Reefs 1:95–107
Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132
Emslie MJ, Pratchett MS, Cheal AJ, Osborne K (2010) Great Barrier Reef butterflyfish community structure: the role of shelf position and benthic habitat type. Coral Reefs 29:705–715
Findley JS, Findley MT (1985) A search for pattern in butterflyfish communities. Am Nat 126:800–816
Garpe KC, Yahya SAS, Lindahl U, Öhman MC (2006) Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Mar Ecol Prog Ser 315:237–247
Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103:8425–8429
Graham NAJ, McClannahan TR, MacNeil MA, Wilson SK, Polunin NVC, Jennings S, Chabanet P, Clark S, Spalding MD, Letourner Y, Bigot L, Galzin R, Ohman MC, Garpe KC, Edwards AJ, Sheppard CRC (2008) Climate warming, marine protected areas and the ocean scale integrity of coral reef ecosystems. PLoS one 3:1–9
Graham NAJ, Wilson SK, Pratchett MS, Polunin NVC, Spalding MD (2009) Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline. Biodivers Conserv 18:3325–3336
Halford A, Thompson AA (1994) Standard Operating Procedure No. 3: Visual Census Surveys of Reef Fish. Australian Institute of Marine Science, Townsville, Australia
Halford AR, Cheal AJ, Ryan D, DMcB Williams (2004) Resilience to large-scale disturbance in coral and fish assemblages on the Great Barrier Reef, Australia. Ecology 85:1892–1905
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hoey AS, Bellwood DR (2008) Cross shelf variation in the role of parrotfishes on the Great Barrier Reef. Coral Reefs 27:37–47
Hughes TP (1994) Catastrophes, phase shifts and large scale degradation of a Caribbean coral reef. Science 265:1547–1551
Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: A long-term perspective. Limnol Oceanogr 44:932–940
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
Jones GP, Syms C (1998) Disturbance, habitat structure and the ecology of fishes on coral reefs. Aust J Ecol 23:287–297
Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral declines threaten fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251–8253
Lewis AR (1997) Effects of experimental coral disturbance on the structure of fish communities on large patch reefs. Mar Ecol Prog Ser 161:37–50
Lindahl U, Ohman MC, Schelten CK (2001) The 1997/1998 mass mortality of corals: effects on fish communities. Mar Pollut Bull 42:127–131
Macgeachy JK, Stearn CW (1976) Boring by macro-organisms in the coral Montastrea annularis on Barbados reefs. Int Rev Gesamten Hydrobiol 61:715–745
Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Global Change Biol 10:1642–1647
Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306
Nyström M, Graham NAJ, Lokrantz J, Norström AV (2008) Capturing the cornerstones of coral reef resilience: linking theory to practice. Coral Reefs 27:795–809
Pratchett MS (2001) Influences of coral symbionts on feeding preferences of crown-of-thorns starfish. Mar Ecol Prog Ser 214:111–119
Pratchett MS (2005) Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar Biol 148:373–382
Pratchett MS (2010) Changes in coral assemblages during an outbreak of Acanthaster planci at Lizard Island, northern Great Barrier Reef (1995–1999). Coral Reefs. doi:10.1007/s00338-010-0602-9
Pratchett MS, Berumen ML (2008) Inter-specific variation in distributions and diets of coral reef butterflyfishes (Teleostei: Chaetodontidae). J Fish Biol 73:1730–1747
Pratchett MS, Wilson SK, Berumen ML, McCormick MI (2004) Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23:352–356
Pratchett MS, Pradjakusuma OA, Jones GP (2006a) Is there a reproductive basis to solitary living versus pair formation in coral reef fishes? Coral Reefs 25:85–92
Pratchett MS, Wilson SK, Baird AH (2006b) Declines in abundance of Chaetodon butterflyfishes following extensive coral depletion. J Fish Biol 69:1269–1280
Pratchett MS, Marnane MJ, Berumen ML, Eagle JE, Pratchett DJ (2008a) Habitat associations of juvenile versus adult butterflyfishes. Coral Reefs 27:541–551
Pratchett MS, Munday PL, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008b) Effects of climate-induced coral bleaching on coral-reef fishes: ecological and economic consequences. Oceanogr Mar Biol Annu Rev 46:251–296
Ralston S (1980) Aspects of the reproductive biology and feeding ecology of Chaetodon miliaris, a Hawaiian endemic butterflyfish. Environ Biol Fish 6:167–176
Reese ES (1975) A comparative field study of the social behaviour and related ecology of reef fishes of the family Chaetodontidae. Z Tierpsychol 37:37–61
Reese ES (1981) Predation on corals by fishes of the family Chaetodontidae: implications for conservation and management of coral reef systems. Bull Mar Sci 31:594–604
Russ GR (1984) Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef. I. levels of variability across the entire continental shelf. Mar Ecol Prog Ser 20:23–34
Sano M (2004) Short-term effects of a mass coral bleaching event on a reef fish assemblage at Iriomote Island, Japan. Fish Sci 70:41–46
Sano M, Shimizu M, Nose Y (1984) Changes in the structure of coral reef fish communities by destruction of hermatypic corals: observations and experimental views. Pac Sci 38:51–79
Sano M, Shimizu M, Nose Y (1987) Long-term effects of destruction of hermatypic corals by Acanthaster planci infestation of reef fish communities at Iriomote Island, Japan. Mar Ecol Prog Ser 37:191–199
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596
Trapon M, Pratchett MS, Penin L (2010) Change in coral cover and composition following 30 years of disturbances at Moorea, French Polynesia. J Mar Biol. doi:10.1155/2011/807625
Vasquez DP, Simberloff D (2002) Ecological specialisation and susceptibility to disturbance: conjectures and refutations. Am Nat 159:606–623
Walsh WJ (1983) Stability of a coral reef fish community following a catastrophic storm. Coral Reefs 2:49–63
Webster PJ, Holland GJ, Curry JA, Chang HR (2005) Changes in tropical cyclone number, duration and intensity in a warming environment. Science 309:1844–1846
Williams DMcB (1983) Longitudinal and latitudinal variation in the structure of reef fish communities. In: Baker JT, Carter RM, Sammarco PW, Stark KP (eds) Proceedings of the Great Barrier Reef Conference. JCU Press, Townsville, pp 265–270
Williams DMcB, Hatcher AI (1983) Structure of fish communities on outer slopes of inshore, mid-shelf and outer shelf reefs of the Great Barrier Reef. Mar Ecol Prog Ser 10:239–250
Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Global Change Biol 12:2220–2234
Wilson SK, Fisher R, Pratchett MS, Graham NAJ, Dulvy NK, Turner RA, Cakacaka A, Polunin NVC, Rushton SP (2008) Exploitation and habitat degradation as agents of change within coral reef fish communities. Global Change Biol 12:2796–2809
Wilson SK, Dolman AM, Cheal AJ, Emslie MJ, Pratchett MS, Sweatman HPA (2009) Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 28:3–14
Woodley JD, Chornesky EA, Clifford PA (1981) Hurricane Allen’s impact on Jamaican coral reefs. Science 214:749–755
Acknowledgments
We thank the crews of the RVs Sirius, Harry Messel, Cape Ferguson and Lady Basten for support in the field and all members past and present of the AIMS long-term monitoring program who assisted with data collection. Comments from Terry Done, Nick Graham and four anonymous reviewers greatly improved earlier versions of the manuscript.
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Electronic supplementary material
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338_2011_730_MOESM1_ESM.eps
Temporal trends in average hard coral cover on 47 reefs surveyed by the Long Term Monitoring Program. Error bars are 95% Confidence Intervals. Graphs are arranged down the page by latitudinal sector running from north to south: CL = Cooktown-Lizard Island, CA = Cairns, TO = Townsville, WH = Whitsunday, SW = Swains, CB = Capricorn-Bunker. Graphs are then arranged across the page to represent position across the continental shelf: inner-shelf, mid-shelf, outer-shelf. Supplementary material 1 (EPS 5709 kb)
338_2011_730_MOESM2_ESM.eps
Temporal trends in total butterflyfish abundance on 47 reefs surveyed by the Long Term Monitoring Program. Graphs are arranged down the page by latitudinal sector running from north to south: CL = Cooktown-Lizard Island, CA = Cairns, TO = Townsville, WH = Whitsunday, SW = Swains, CB = Capricorn-Bunker. Graphs are then arranged across the page to represent position across the continental shelf: inner-shelf, mid-shelf, outer-shelf. Supplementary material 2 (EPS 6274 kb)
338_2011_730_MOESM3_ESM.eps
Temporal trends in butterflyfish species richness on 47 reefs surveyed by the Long Term Monitoring Program. Graphs are arranged down the page by latitudinal sector running from north to south: CL = Cooktown-Lizard Island, CA = Cairns, TO = Townsville, WH = Whitsunday, SW = Swains, CB = Capricorn-Bunker. Graphs are then arranged across the page to represent position across the continental shelf: inner-shelf, mid-shelf, outer-shelf. Supplementary material 3 (EPS 5698 kb)
Appendix—Species list
Appendix—Species list
Obligate corallivores—Chaetodon aureofasciatus, C. bennetti, C. baronessa, C. lunulatus, C. ornatissimus, C. pelewensis, C. plebeius, C. rainfordi, C. reticulatus, C. trifascialis
Facultative corallivores—C. auriga, C. citrinellus, C. ephippium, C. flavirostris, C. kleinii, C. lineolatus, C. lunula, C. meyeri, C. punctatofasciatus, C. rafflesi, C. speculum, C. vagabundus
Generalist feeders—C. melannotus, C. mertensii, C. ulietensis, C. unimaculatus, Chelmon rostratus, Forcipiger flavissimus, F. longirostris
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Emslie, M.J., Pratchett, M.S. & Cheal, A.J. Effects of different disturbance types on butterflyfish communities of Australia’s Great Barrier Reef. Coral Reefs 30, 461–471 (2011). https://doi.org/10.1007/s00338-011-0730-x
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DOI: https://doi.org/10.1007/s00338-011-0730-x