Abstract
Successive, extensive bleaching events have reduced coral cover and altered species assemblages significantly in the Montebello and Barrow Islands in north-western Australia. In particular, acroporid and pocilloporid populations were dramatically reduced, while poritid and faviid corals were less impacted and now dominate coral assemblages. Subsequent to this perturbation, there have been changes in the abundance and distribution of the coral eating crown-of-thorns starfish, Acanthaster cf. solaris (to densities of up to 320 ha−1) that have had a further impact on coral communities selectively targeting the coral taxa most susceptible to bleaching, often referred to as climate change “losers”. The feeding selectivity of A. cf. solaris under post-bleaching conditions was studied to determine its likely impact on coral communities and coral recovery. We found that even when Acropora and Pocillopora were extremely rare, A. cf. solaris demonstrated a high level of selectivity for these genera, although they consumed non-preferred taxa such as poritid, faviid, and merulinid corals in greater numbers. The consumption of non-preferred genera and families of corals differed between sites and was influenced by their local abundance. This study demonstrates that where crown-of-thorns starfish populations greatly exceed outbreak threshold densities of 10–15 ha−1, they are likely to impact recovery of coral communities from bleaching events and exacerbate bleaching induced changes in assemblage structure.
Similar content being viewed by others
References
Arrigoni R, Stefani F, Pichon M, Galli P, Benzoni F (2012) Molecular phylogeny of the robust clade (Faviidae, Mussidae, Merulinidae, and Pectiniidae): an Indian Ocean perspective. Mol Phylogenet Evol 65:183–193
Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2008.09.003
Birkeland C, Lucas JS (1990) Acanthaster planci Major management problem of coral reefs. CRC Press, Boca Raton, p 257
Branham JM, Reed SA, Bailey JH, Caperon J (1971) Coral eating sea stars Acanthaster planci in Hawaii. Science (Wash DC) 172:1155–1157
Brauer RW, Jordan MR, Barnes DJ (1970) Triggering of the stomach aversion reflex of Acanthaster planci by coral extracts. Nature (Lond) 228:344–346
Brodie J, Fabricius K, De’ath G, Okaji K (2005) Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence. Mar Pollut Bull 51:266–278
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:129–138
Chesher RH (1969) Destruction of Pacific corals by sea star Acanthaster planci. Science (Wash DC) 165:280–283
Chesson J (1978) Measuring preference in selective predation. Ecology 59:211–215
Collins AR (1975) Biochemical investigation of two responses involved in the feeding behaviour of Acanthaster planci (L.). III. Food preferences. J Exp Mar Biol Ecol 17(1):87–94
De’ath G, Moran PJ (1998a) Factors affecting the behaviour of crown-of-thorns starfish (Acanthaster planci L.) on the Great Barrier Reef: 2: feeding preferences. J Exp Mar Biol Ecol 220:107–126
De’ath G, Moran PJ (1998b) Factors affecting the behaviour of crown-of-thorns starfish (Acanthaster planci L.) on the Great Barrier Reef: 1: patterns of activity. J Exp Mar Biol Ecol 220:83–106
Depczynski M, Gilmour JP, Ridgway T, Barnes H, Heyward AJ, Holmes TH, Moore JAY, Radford BT, Thomson DP, Tinkler P, Wilson SK (2013) Bleaching, coral mortality and subsequent survivorship on a West Australian fringing reef. Coral Reefs 32:233–238
Done TT (1985) Effects of two Acanthaster outbreaks on coral community structure-the meaning of devastation. Proc 5th Int Coral Reef Congr 5:315–320
DPIRD (2017) North coast demersal scalefish resource harvest strategy 2017 – 2021. Fisheries Management Paper No. 285. Department of Primary Industries and Regional Development (DPIRD), Government of Western Australia, Perth, Australia, pp vi + 35
Fabricius KE (2013) Acanthaster planci. In: Lawrence JM (ed) Starfish: biology and ecology of the Asteroidea. John Hopkins University Press, Baltimore, pp 132–141
Fabricius KE, Okaji K, De’ath G (2010) Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation. Coral Reefs 29:593–605
Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169
Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340(6128):69–71
Glynn PW (1976) Some physical and biological determinants of coral community structure in the eastern Pacific. Ecol Monogr 46:431–456
Glynn PW (1980) Defence by symbiotic crustacea of host corals elicited by chemical cues from predator. Oecologia 47:287–290
Glynn PW, Ault JS (2000) A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs 19:1–23
Haszprunar G, Spies M (2014) An integrative approach to the taxonomy of the crown-of-thorns starfish species group (Asteroidea: Acanthaster): a review of names and comparison to recent molecular data. Zootaxa 3841(2):271–284
Haszprunar G, Vogler C, Wörheide G (2017) Persistent gaps of knowledge for naming and distinguishing multiple species of crown-of-thorns seastar in the Acanthaster planci species complex. Diversity 9(2):22
Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ (2018) Global warming transforms coral reef assemblages. Nature 556(7702):492
Ivlev VS (1961) Experimental ecology of the feeding of fishes. Translated from Russian by D Scott. Yale University Press, New Haven, Connecticut, USA
Jacobs J (1974) Quantitative measurement of food selection. Oecologia 14:413–417
Johansson CL, Francis DS, Uthicke S (2016) Food preferences of juvenile corallivorous crown-of-thorns (Acanthaster planci) sea stars. Mar Biol 163:49
Johnson DB, Stoddart JA (1988) Report on surveys of the distribution, abundance and impact of Acanthaster planci on reefs within the Dampier Archipelago (Western Australia), April 1987. The Crown of Thorns Study. Australian Institute of Marine Science (AIMS), Townsville, Queensland, Australia
Jones GP, Norman MD (1986) Feeding selectivity in relation to territory size in a herbivorous reef fish. Oecologia 68:549–556
Jonker M, Johns K, Osborne K (2008) Surveys of benthic reef communities using underwater digital photography and counts of juvenile corals. Long-term monitoring of the Great Barrier Reef. Standard Operational Procedure Number 10/2008. Australian Institute of Marine Science (AIMS), Townsville, Queensland, Australia, pp vi +75
Keesing JK (1990) Feeding biology of the crown of thorns starfish, Acanthaster planci (Linnaeus). PhD thesis. James Cook University of North Queensland, Townsville, Australia
Keesing JK (1993) Influence of persistent sub-infestation density Acanthaster planci (L.) and high density Echinometra mathaei (de Blainville) populations on coral reef community structure in Okinawa, Japan. In: Proceedings of 7th International Coral Reef Symposium 2:769–779
Keesing JK (1995) Temporal patterns in the feeding and emergence behaviour of the crown-of-thorns starfish Acanthaster planci. Mar Behav Physiol 25:209–232
Keesing JK, Lucas JS (1992) Field measurement of feeding and movement rates in the crown-of-thorns starfish, Acanthaster planci (L.). J Exp Mar Biol Ecol 156:89–104
Lechowicz MJ (1982) The sampling characteristics of electivity indices. Oecologia 52:22–30
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131
Lozano-Montes HM, Keesing JK, Grol MG, Haywood MD, Vanderklift MA, Babcock RC, Bancroft K (2017) Limited effects of an extreme flood event on corals at Ningaloo Reef. Estuar Coast Shelf Sci 191:234–238
Lucas JS (1982) Quantitative studies of feeding and nutrition during larval development of the coral reef asteroid Acanthaster planci (L.). J Exp Mar Biol Ecol 65:173–193
Manly BF, McDonald LL, Thomas DL, McDonald TL, Erickson WP (2002) Resource selection by animals: statistical analysis and design for field studies. Kluwer Academic Publishers, Nordrecht, p 221
Marsh LM (2000a) Echinoderms of the Montebello Islands. Rec West Aust Mus Suppl 59:21–27
Marsh LM (2000b) Scleractinian corals of the Montebello Islands. Rec West Aust Mus Suppl 59:15–19
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
Moore JAY, Bellchambers LM, Depczynski MR, Evans RD, Evans SN, Field SN, Friedman KJ, Gilmour JP, Holmes TH, Middlebrook R, Radford BT, Ridgway T, Shedrawi G, Taylor H, Thomson DP, Wilson SK (2012) Unprecedented mass bleaching and loss of coral across 12° of latitude in Western Australia in 2010–11. PLoS One 7(12):e51807
Moran PJ (1986) The Acanthaster phenomenon. Oceanogr Mar Biol Ann Rev 24:379–480
Moran PJ, De’ath G (1992) Estimates of the abundance of the crown-of-thorns starfish (Acanthaster planci L.) in outbreaking and non-outbreaking populations on reefs with the Great Barrier Reef. Mar Biol 113:509–515
Nakamura M, Okaji K, Higa Y, Yamakawa E, Mitarai S (2014) Spatial and temporal population dynamics of the crown-of-thorns starfish, Acanthaster planci, over a 24-year period along the central west coast of Okinawa Island, Japan. Mar Biol 161:2521–2530
Oliver EC, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Gupta AS, Hobday AJ, Holbrook NJ (2018) Longer and more frequent marine heatwaves over the past century. Nat Comm 9(1):1324
Ormond RFG, Hanscomb NJ, Beach DH (1976) Food selection in the crown of thorns starfish, Acanthaster planci (L.). Mar Behav Physiol 4:93–105
Page C, Coleman G, Ninio R, Osborne K (2001) Surveys of benthic reef communities using underwater video. In: Long-term monitoring of the great barrier reef standard operating procedure. Number 7. Australian Institute of Marine Science, Townsville
Pearson RG (1981) Recovery and recolonization of coral reefs. Mar Ecol Prog Ser 4(1):105–122
Pearson RG, Endean R (1969) A preliminary study of the coral predator Acanthaster planci (L.) (Asteroidea) on the Great Barrier Reef. Qld Dept Harb Mar Fish Notes 3(1):27–55
Pickrell J (2015) New threat to Western Australian reefs. Aust Geogr 2015:37
Pratchett MS (2001) Influence of coral symbionts on feeding preferences of crown-of-thorns starfish Acanthaster planci in the western Pacific. Mar Ecol Prog Ser 214:111–119
Pratchett MS (2007) Feeding Preferences of Acanthaster planci (Echinodermata: Asteroidea) under controlled conditions of food availability. Pacific Sci 61(1):113–120
Pratchett MS, Schenk TJ, Baine M, Syms C, Baird AH (2009) Selective coral mortality associated with outbreaks of Acanthaster planci L. in Bootless Bay, Papua New Guinea. Mar Environ Res 67(4–5):230–236
Pratchett MS, Caballes CF, Rivera-Posada JA, Sweatman HP (2014) Limits to understanding and managing outbreaks of crown-of-thorns starfish (Acanthaster spp.). Oceanogr Mar Biol Ann Rev 52:133–200
Richards Z, Rosser N (2012) Abundance, distribution and new records of scleractinian corals at Barrow Island and Southern Montebello Islands, Pilbara (offshore) bioregion. J Roy Soc West Aust 95:155–165
Ridgway T, Inostroza K, Synnot L, Trapon M, Twomey L, Westera M (2016) Temporal patterns of coral cover in the offshore Pilbara, Western Australia. Mar Biol 163:182
Smith LD, Gilmour JP, Heyward AJ, Rees M (2006) Mass-bleaching, mortality and slow recovery of three common groups of scleractinian corals at an isolated reef. In: Proceedings of the 10th International Coral Reef Symposium, vol 1, pp 651–656
Sweatman H (2008) No-take reserves protect coral reefs from predatory starfish. Curr Biol 18(14):R598–R599
van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76
Vanderploeg HA, Scavia D (1979) Calculation and use of selectivity coefficients of feeding: zooplankton grazing. Ecol Modell 7:135–149
Veron JEN (1986) Corals of Australia and the Indo-Pacific. Angus and Robertson, Sydney, p 644
von Prahl H, Mejía A (1985) Primer informe de un coral acropórido, Acropora valida (Dana, 1984) (Scleractinia: Astrocoeniida: Acroporidae) para el Pacífico americano. Rev Biol Trop 33:39–43 (Spanish with English abstract)
Veron JEN, Marsh LM (1988) Hermatypic corals of Western Australia: records and annotated species list. Rec West Aust Mus Suppl 29:1–136
Wahab MA, Fromont J, Gomez O, Fisher R, Jones R (2017) Comparisons of benthic filter feeder communities before and after a large-scale capital dredging program. Mar Poll Bull 122:176–193
Wilson BR (1972). Western Australian coral reefs, with preliminary notes on a study at Kendrew Island, Dampier Archipelago. In: Paper presented at Crown of Thorns Starfish Seminar, University of Queensland, Brisbane, 25 August 1972, pp 47–58
Wilson BR, Marsh LM (1974) Wilson BR, Marsh LM. Acanthaster studies on a Western Australian coral reef. In: Proceedings of 2nd International Coral Reef Symposium, vol 1, pp 621–630
Wilson BR, Marsh LM (1975) Seasonal behaviour of a ‘normal’ population of Acanthaster in Western Australia. In: Crown of Thorns Starfish Seminar Proc Brisb 6 September 1974, pp. 167–179, Aust Govt Publ Serv, Canberra
Wilson BR, Stoddart J (1987) A thorny problem: crown of thorns starfish in Western Australia. Landscope 3:35–39
Yamaguchi M (1986) Acanthaster planci infestations of reefs and coral assemblages in Japan: a retrospective analysis of control efforts. Coral Reefs 5:23–30
Yasuda N (2018) Distribution expansion and historical population outbreak patterns of Crown-of-thorns starfish, Acanthaster planci sensu lato, in Japan from 1912 to 2015. In: Iguchi A, Hongo C (eds) Coral Reef Studies of Japan. Coral Reefs of the World, vol 13. Springer, Singapore, pp 125–148
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, Upper Saddle River
Acknowledgements
This research was undertaken as part of the Pilbara Marine Conservation Partnership between CSIRO and the University of Western Australia, funded by the Gorgon Barrow Island Net Conservation Benefits Fund which is administered by the Western Australian Department of Biodiversity Conservation and Attractions (DBCA). We thank Joanna Strzelecki (CSIRO) for reviewing the manuscript, Richard Pillans and Chris Doropoulos (CSIRO) and Rachel Marshall of DBCA for assistance with the fieldwork. DBCA also provided the imagery for Fig. 2. Data on rainfall levels and cyclone frequency were obtained from the Australian Bureau of Meteorology (http://www.bom.gov.au/jsp/ncc/climate_averages/rainfall/index.jsp?period=an&area=wa#maps and http://www.bom.gov.au/climate/maps/averages/tropical-cyclones/).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
All necessary permits to access field sites and conduct the research described in this paper were obtained.
Additional information
Responsible Editor: M. Byrne.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by K. Wolfe and N. Yasuda.
Rights and permissions
About this article
Cite this article
Keesing, J.K., Thomson, D.P., Haywood, M.D.E. et al. Two time losers: selective feeding by crown-of-thorns starfish on corals most affected by successive coral-bleaching episodes on western Australian coral reefs. Mar Biol 166, 72 (2019). https://doi.org/10.1007/s00227-019-3515-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-019-3515-3