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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Olfactory responses of coral-reef fishes to coral degradation and crown-of-thorns (Acanthaster planci)

Amy G. Coppock A B C , Naomi M. Gardiner A and Geoffrey P. Jones A B
+ Author Affiliations
- Author Affiliations

A College of Marine and Environmental Sciences, James Cook University, Townsville, Qld 4811, Australia.

B ARC Centre of Excellence James Cook University, Townsville, Qld 4811, Australia.

C Corresponding author. Email: amy.coppock@my.jcu.edu.au

Marine and Freshwater Research 67(5) 605-611 https://doi.org/10.1071/MF14424
Submitted: 24 December 2014  Accepted: 8 April 2015   Published: 6 August 2015

Abstract

Coral degradation is a major threat towards the biodiversity of coral-reef ecosystems, either through the physical effects of environmental change, or biological agents such as crown-of-thorns (Acanthaster planci). Coral loss is leading to significant declines in reef-fish assemblages, particularly those dependent on live coral as settlement sites. Most reef fishes use olfactory stimuli at settlement; however, their ability to detect chemical stimuli from degraded corals or A. planci is unknown. Here, olfactory responses of juvenile reef fishes to the presence of stressed corals and A. planci were tested. Juveniles of eight common coral-associated species were subjected to a series of pair-wise choice tests, where the period of time spent in two differing water sources was noted. All species demonstrated a significant attraction towards healthy coral (≥76%), avoiding cues emitted by stressed coral colonies. When given the choice between a control water (untreated reef water) and water containing chemical cues from A. planci, most species elicited no response. Finally, when given the choice between chemical cues derived from feeding A. planci or the control, all species avoided A. planci (≥70%). Our results indicated that juvenile reef fish are capable of distinguishing the state of coral health, but not directly from disturbance agents.

Additional keywords: Chaetodontidae, chemosensory cues, coral degradation, habitat selection, Labridae, olfaction, Pomacentridae.


References

Atema, J., Kingsford, M. J., and Gerlach, G. (2002). Larval reef fish could use odour for detection, retention and orientation to reefs. Marine Ecology Progress Series 241, 151–160.
Larval reef fish could use odour for detection, retention and orientation to reefs.Crossref | GoogleScholarGoogle Scholar |

Baird, A. H., Pratchett, M. S., Hoey, A. S., Herdiana, Y., and Campbell, S. J. (2013). Acanthaster planci is a major cause of coral mortality in Indonesia. Coral Reefs 32, 803–812.
Acanthaster planci is a major cause of coral mortality in Indonesia.Crossref | GoogleScholarGoogle Scholar |

Bellwood, D. R., Hughes, T. P., Folke, C., and Nyström, M. (2004). Confronting the coral reef crisis. Nature 429, 827–833.
Confronting the coral reef crisis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVKltb8%3D&md5=312df4541085ce63d2f6bc34ba79c831CAS | 15215854PubMed |

Berumen, M. L., Pratchett, M. S., and McCormick, M. I. (2005). Within-reef differences in diet and body condition of coral feeding butterfly fishes (Chaetodontidae). Marine Ecology Progress Series 287, 217–227.
Within-reef differences in diet and body condition of coral feeding butterfly fishes (Chaetodontidae).Crossref | GoogleScholarGoogle Scholar |

Blondel, J., Thomas, D. W., Charmantier, A., Perret, P., Bourgault, P., and Lambrects, M. M. (2006). A thrity year study of phenotypic and genetic variation of blue tits in Mediterranean habitat mosaics. BioScience 56, 661–673.
A thrity year study of phenotypic and genetic variation of blue tits in Mediterranean habitat mosaics.Crossref | GoogleScholarGoogle Scholar |

Booth, D. J. (1992). Larval settlement patterns and preferences by domino damselfish Dascyllus albisella Gill. Journal of Experimental Marine Biology and Ecology 155, 85–104.
Larval settlement patterns and preferences by domino damselfish Dascyllus albisella Gill.Crossref | GoogleScholarGoogle Scholar |

Booth, D. J., and Wellington, G. (1998). Settlement preferences in coral -reef fishes: Effects on patterns of adult and juvenile distributions, individual fitness and population structure. Australian Journal of Ecology 23, 274–279.
Settlement preferences in coral -reef fishes: Effects on patterns of adult and juvenile distributions, individual fitness and population structure.Crossref | GoogleScholarGoogle Scholar |

Booth, D. J., and Beretta, G. A. (2002). Changes in a fish assemblage after a coral bleaching event. Marine Ecology Progress Series 245, 205–212.
Changes in a fish assemblage after a coral bleaching event.Crossref | GoogleScholarGoogle Scholar |

Byrnes, J., Stachowicz, J. J., Hultgren, K. M., Hughes, A. R., Olyanik, S. V., and Thornber, C. S. (2006). Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecology Letters 9, 61–71.
| 16958869PubMed |

Conradt, L., Clutton-Brock, T. H., and Guinness, F. E. (1999). The relationship between habitat choice and lifetime reproductive success in female red deer. Oecologica 120, 218–224.
The relationship between habitat choice and lifetime reproductive success in female red deer.Crossref | GoogleScholarGoogle Scholar |

Coppock, A. G., Gardiner, N. M., and Jones, G. P. (2013). Olfactory discrimination in juvenile coral reef fishes: response to conspecifics and corals. Journal of Experimental Marine Biology and Ecology 443, 21–26.
Olfactory discrimination in juvenile coral reef fishes: response to conspecifics and corals.Crossref | GoogleScholarGoogle Scholar |

Danilowicz, B. S. (1996). Choice of coral species by naive and field-caught damselfish. Copeia 1996, 735–739.
Choice of coral species by naive and field-caught damselfish.Crossref | GoogleScholarGoogle Scholar |

Dixson, D. L., Jones, G. P., Munday, P. L., Planes, S., Pratchett, M. S., Srinivasan, M., Syms, C., and Thorrold, S. R. (2008). Coral reef fish smell leaves to find island homes. Proceedings of the Royal Society of London – B. Biological Sciences 275, 2831–2839.
Coral reef fish smell leaves to find island homes.Crossref | GoogleScholarGoogle Scholar |

Dixson, D. L., Munday, P. L., and Jones, G. P. (2010). Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters 13, 68–75.
Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues.Crossref | GoogleScholarGoogle Scholar | 19917053PubMed |

Dixson, D. L., Munday, P. L., Pratchett, M. S., and Jones, G. P. (2011). Ontogenetic changes in responses to settlement cues by Anenomefish. Coral Reefs 30, 903–910.
Ontogenetic changes in responses to settlement cues by Anenomefish.Crossref | GoogleScholarGoogle Scholar |

Dixson, D. L., Pratchett, M. S., and Munday, P. L. (2012). Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species. Animal Behaviour 84, 45–51.
Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species.Crossref | GoogleScholarGoogle Scholar |

Dixson, D. L., Abrego, D., and Hay, M. E. (2014). Chemically mediated behaviour of recruiting corals and fishes: a tipping point that may limit recovery. Science 345, 892–897.
Chemically mediated behaviour of recruiting corals and fishes: a tipping point that may limit recovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlOmsr%2FE&md5=24120d8e87a730dd08bcf0985c357b97CAS | 25146281PubMed |

Feary, D. A., Almany, G. R., Jones, G. P., and McCormick, M. I. (2007a). Coral degradation and the structure of tropical reef fish communities. Marine Ecology Progress Series 333, 243–248.
Coral degradation and the structure of tropical reef fish communities.Crossref | GoogleScholarGoogle Scholar |

Feary, D. A., Almany, G. R., McCormick, M. I., and Jones, G. P. (2007b). Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153, 727–737.
Habitat choice, recruitment and the response of coral reef fishes to coral degradation.Crossref | GoogleScholarGoogle Scholar | 17566781PubMed |

Fitt, W. K., Brown, B. E., Warner, M. E., and Dunne, R. P. (2001). Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65.
Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals.Crossref | GoogleScholarGoogle Scholar |

Gardner, T. A., Cote, I. M., Gill, J. A., Grant, A., and Watkinson, A. R. (2003). Long-term region-wide declines in Caribbean corals. Science 301, 958–960.
Long-term region-wide declines in Caribbean corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1elsL0%3D&md5=3531c45e2ce4f3674c531d267417c025CAS | 12869698PubMed |

Goldberg, J., and Wilkinson, C. (2004). Global threats to coral reefs: coral bleaching, global climate change, disease, predator plagues, and invasive species. In ‘Status of Coral Reefs of the World’. (Ed. C Wilkinson) pp. 67–92. (Australian Institute of Marine Science: Townsville, Qld)

Hay, M. E. (2009). Marine chemical ecology: chemical signals and cues structure marine populations, communities and ecosystems. Annual Review of Marine Science 1, 193–212.
Marine chemical ecology: chemical signals and cues structure marine populations, communities and ecosystems.Crossref | GoogleScholarGoogle Scholar | 21141035PubMed |

Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C. M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R. H., Dubi, A., and Hatziolos, M. E. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742.
Coral reefs under rapid climate change and ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWhu7fN&md5=e3ee8b6f43e3553ff7e23b2196c4f671CAS | 18079392PubMed |

Holbrook, S. J., and Schmitt, R. J. (2002). Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83, 2855–2868.
Competition for shelter space causes density-dependent predation mortality in damselfishes.Crossref | GoogleScholarGoogle Scholar |

Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., Lough, J. M., Marshall, P., Nystrom, M., Palumbi, S. R., Pandolfi, J. M., Rosen, B., and Roughgarden, J. (2003). Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933.
Climate change, human impacts, and the resilience of coral reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1elsb4%3D&md5=49096c324f4ef3066d55b164ac2e9913CAS | 12920289PubMed |

Jackson, B. C., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., Bradbury, R. H., Cooke, R., Erlandson, J., Estes, J. A., Hughes, T. P., Kidwell, S., Lange, C. B., Lenihan, H. S., Pandolfi, J. M., Peterson, C. H., Steneck, R. S., Tegner, M. J., and Warner, R. R. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637.
Historical overfishing and the recent collapse of coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1Khu7o%3D&md5=1697cc02fae25b68935990cbe6bd5c34CAS |

Jones, G. P., McCormick, M. I., Srinivasan, M., and Eagle, J. V. (2004). Coral decline threatens biodiversity in marine reserves. Proceedings of the National Academy of Sciences of the United States of America 101, 8251–8253.
Coral decline threatens biodiversity in marine reserves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslCitbw%3D&md5=789adaddc47ad838bc021e00ce97a901CAS | 15150414PubMed |

Kenchington, R., and Kelleher, G. (1992). Crown-of-thorns starfish management conundrums. Coral Reefs 11, 53–56.
Crown-of-thorns starfish management conundrums.Crossref | GoogleScholarGoogle Scholar |

Kingsford, M. J., Leis, J. M., Shanks, A., Lindeman, K. C., Morgan, S. G., and Pineda, J. (2002). Sensory environments, larval abilities and local self recruitment. Bulletin of Marine Science 70, 309–340.

Lecchini, D., Planes, S., and Galzin, R. (2005a). Experimental assessment of sensory modalities of coral reef fish larvae in the recognition of their settlement habitat. Behavioral Ecology and Sociobiology 58, 18–26.
Experimental assessment of sensory modalities of coral reef fish larvae in the recognition of their settlement habitat.Crossref | GoogleScholarGoogle Scholar |

Lecchini, D., Shima, J., Banaigs, B., and Galzin, R. (2005b). Larval sensory abilities and mechanisms of habitat selection of a coral-reef fish during settlement. Oecologia 143, 326–334.
Larval sensory abilities and mechanisms of habitat selection of a coral-reef fish during settlement.Crossref | GoogleScholarGoogle Scholar | 15647903PubMed |

Lecchini, D., and Nakamura, Y. (2013). Use of chemical cues by coral reef animal larvae for habitat selection. Aquatic Biology 19, 231–238.
Use of chemical cues by coral reef animal larvae for habitat selection.Crossref | GoogleScholarGoogle Scholar |

Lecchini, D., Waqalevu, V. P., Parmentier, E., Radford, C. A., and Banaigs, B. (2013). Fish larvae prefer coral over algal water cues: implications of coral reef degradation. Marine Ecology Progress Series 475, 303–307.
Fish larvae prefer coral over algal water cues: implications of coral reef degradation.Crossref | GoogleScholarGoogle Scholar |

Leis, J. M., and Yerman, M. (2012). Behaviour of larval butterflyfishes (Teleostei: Chaetodontidae) at settlement on coral reefs. Copeia , 211–221.
Behaviour of larval butterflyfishes (Teleostei: Chaetodontidae) at settlement on coral reefs.Crossref | GoogleScholarGoogle Scholar |

Long, J. D., Smalley, G. W., Barsby, T., Anderson, J. T., and Hay, M. E. (2007). Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton. Proceedings of the National Academy of Sciences of the United States of America 104, 10512–10517.
Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1KktLs%3D&md5=34886f6d553ef437ed39b158955efd72CAS | 17563379PubMed |

Lough, J. M., and van Oppen, M. J. H., (Eds) (2009). Chapter 1. Introduction: coral bleaching – pattern, processes, causes and consequences. In ‘Coral Bleaching. Ecological Studies, vol. 205’. pp. 1–5. (Springer-Verlag: Berlin)

McCormick, M. I. (2009). Behaviourally mediated phenotypic selection in a disturbed coral reef environment. PLoS One 4, e7096.
Behaviourally mediated phenotypic selection in a disturbed coral reef environment.Crossref | GoogleScholarGoogle Scholar | 19763262PubMed |

McCormick, M. I., Moore, J. A. Y., and Munday, P. L. (2010). Influence of habitat degradation on fish replenishment. Coral Reefs 29, 537–546.
Influence of habitat degradation on fish replenishment.Crossref | GoogleScholarGoogle Scholar |

Moran, P. J. (1986). The Acanthaster phenomenon. Oceanography and Marine Biology: an Annual Review 24, 379–480.

Morris, D. W., and Davidson, D. L. (2000). Optimally foraging mice match patch use with habitat differences in fitness. Ecology 81, 2061–2066.
Optimally foraging mice match patch use with habitat differences in fitness.Crossref | GoogleScholarGoogle Scholar |

Mumby, P. J., and Steneck, R. S. (2008). Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends in Ecology & Evolution 23, 555–563.
Coral reef management and conservation in light of rapidly evolving ecological paradigms.Crossref | GoogleScholarGoogle Scholar |

Munday, P. L. (2001). Fitness consequences of habitat selection and competition among coral dwelling fish. Oecologia 128, 585–593.
Fitness consequences of habitat selection and competition among coral dwelling fish.Crossref | GoogleScholarGoogle Scholar |

Munday, P. L. (2004). Habitat loss, resource specialisation, and extinction on coral reefs. Global Change Biology 10, 1642–1647.
Habitat loss, resource specialisation, and extinction on coral reefs.Crossref | GoogleScholarGoogle Scholar |

Munday, P. L., Dixson, D. L., Donelson, J. M., Jones, G. P., Pratchett, M. S., Devitsina, G. V., and Døving, K. B. (2009). Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proceedings of the National Academy of Sciences of the United States of America 106, 1848–1852.
Ocean acidification impairs olfactory discrimination and homing ability of a marine fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitV2isrg%3D&md5=8c3b79f54a0cc3db91cc3b067faf4748CAS | 19188596PubMed |

Öhman, M. C., Munday, P. L., Jones, G. P., and Caley, M. J. (1998). Settlement strategies and distribution patterns of coral reef fishes. Journal of Experimental Marine Biology and Ecology 225, 219–238.
Settlement strategies and distribution patterns of coral reef fishes.Crossref | GoogleScholarGoogle Scholar |

Peacor, S. D., and Werner, E. E. (2001). The contribution of trait-mediated indirect effects to net effects of a predator. Proceedings of the National Academy of Sciences of the United States of America 98, 3904–3908.
The contribution of trait-mediated indirect effects to net effects of a predator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1KhsL8%3D&md5=c482aade90d9a44bcfc749bf7a7267bcCAS | 11259674PubMed |

Pratchett, M. S., and Berumen, M. L. (2008). Interspecific variation in distributions and diets of coral reef butterfly fishes (Teleosti: Chaetodontidae). Journal of Fish Biology 73, 1730–1747.
Interspecific variation in distributions and diets of coral reef butterfly fishes (Teleosti: Chaetodontidae).Crossref | GoogleScholarGoogle Scholar |

Pratchett, M. S., Schenk, T. J., Baine, M., Syms, C., and Baird, A. H. (2009). Selective coral mortality associated with outbreaks of Acanthaster planci L. in Bootless Bay, Papua New Guinea. Marine Environmental Research 67, 230–236.
Selective coral mortality associated with outbreaks of Acanthaster planci L. in Bootless Bay, Papua New Guinea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlslajsb8%3D&md5=b9c71fbb48cb31500f738a5d820ceb2bCAS | 19327821PubMed |

Rasher, D. B., Hoey, A. S., and Hay, M. E. (2013). Consumer diversity interacts with prey defences to drive ecosystem function. Ecology 94, 1347–1358.
Consumer diversity interacts with prey defences to drive ecosystem function.Crossref | GoogleScholarGoogle Scholar | 23923498PubMed |

Schlaepfer, M. A., Runge, M. C., and Sherman, P. W. (2002). Ecological and evolutionary traps. Trends in Ecology & Evolution 17, 474–480.
Ecological and evolutionary traps.Crossref | GoogleScholarGoogle Scholar |

Sweatman, H. P. A. (1988). Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. Journal of Experimental Marine Biology and Ecology 124, 163–174.
Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues.Crossref | GoogleScholarGoogle Scholar |

Tolimieri, N. (1995). Effects of microhabitat characteristics on the settlement and recruitment of a coral reef fish at two spatial scales. Oecologia 102, 52–63.
Effects of microhabitat characteristics on the settlement and recruitment of a coral reef fish at two spatial scales.Crossref | GoogleScholarGoogle Scholar |

Trussell, G. C., Ewanchuk, P. J., Bertness, M. D., and Siliman, B. R. (2004). Trophic cascades in rocky shore tide pools: distinguishing lethal and non-lethal effects. Oecologia 139, 427–432.
Trophic cascades in rocky shore tide pools: distinguishing lethal and non-lethal effects.Crossref | GoogleScholarGoogle Scholar | 14872337PubMed |

Vail, A. L., and McCormick, M. I. (2011). Metamorphosing reef fishes avoid predator scent when choosing a home. Biology Letters 7, 921–924.
Metamorphosing reef fishes avoid predator scent when choosing a home.Crossref | GoogleScholarGoogle Scholar | 21653563PubMed |

Wenger, A. S., Johansen, J. L., and Jones, G. P. (2012). Increasing suspended sediment reduces foraging, growth, and condition of a planktivorous damselfish. Journal of Experimental Marine Biology and Ecology 428, 43–48.
Increasing suspended sediment reduces foraging, growth, and condition of a planktivorous damselfish.Crossref | GoogleScholarGoogle Scholar |

Yamaguchi, M., and Braham, J. M. (1974). The crown-of-thorns starfish. BioScience 24, 134.
The crown-of-thorns starfish.Crossref | GoogleScholarGoogle Scholar |