Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Range extensions in anemonefishes and host sea anemones in eastern Australia: potential constraints to tropicalisation

Hamish Malcolm A C and Anna Scott B
+ Author Affiliations
- Author Affiliations

A Fisheries Research, Marine Ecosystems, NSW Department of Primary Industries, Department of Primary Industries, Locked Bag 800, Nelson Bay, NSW 2315, Australia.

B National Marine Science Centre and Marine Ecology Research Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia.

C Corresponding author. Email: hamish.malcolm@dpi.nsw.gov.au

Marine and Freshwater Research 68(7) 1224-1232 https://doi.org/10.1071/MF15420
Submitted: 9 November 2015  Accepted: 5 October 2016   Published: 6 December 2016

Abstract

Species distributions at range edges show complex shifts with climate change. The present study examined anemonefish and host sea anemone abundance at their southern distribution limits on the eastern coast of Australia, to identify factors influencing the geographic responses of the symbiosis. Roaming surveys (30 min) were conducted at 21 sites (~30.01–30.95°S) on rocky reefs in a tropical–temperate transition zone. Two species of host anemones (Entacmaea quadricolor and Heteractis crispa) and anemonefishes (Amphiprion akindynos and A. latezonatus) were found, along with Dascyllus trimaculatus. Nearly all anemones and anemonefishes (>99.5%) were associated with vegetated islands and rocky islets, and abundance was influenced by seawater temperature. Greater numbers of H. crispa and A. akindynos than E. quadricolor and A. latezonatus were found; however, most A. akindynos were juveniles. H. crispa provided nursery habitat for both fishes, whereas adult fishes utilised only E. quadricolor. A southern range extension was found for E. quadricolor, and overwintering of A. latezonatus had extended poleward since the mid-1990s. The paucity of islands and rocky islets south of our surveys, and host-usage patterns, could constrain future range extensions. These findings showed climate-driven latitudinal shifts are complex and are likely to be variably constrained for different species.

Additional keywords: biogeography, climate change, fish.


References

Allen, G. R., Drew, J., and Kaufman, L. (2008). Amphiprion barberi, a new species of anemonefish (Pomacentridae) from Fiji, Tonga, and Samoa. Aqua – International Journal of Ichthyology 14, 105–114.

Allen, G. R., Drew, J., and Fenner, D. (2010). Amphiprion pacificus, a new species of anemonefish (Pomacentridae) from Fiji, Tonga, Samoa, and Wallis Island. Aquaculture 16, 129–138.

Baird, A. H., Sommer, B., and Madin, J. S. (2012). Pole-ward range expansion of Acropora spp. along the east coast of Australia. Coral Reefs 31, 1063.
Pole-ward range expansion of Acropora spp. along the east coast of Australia.Crossref | GoogleScholarGoogle Scholar |

Bates, A. E., Peci, G. T., Frusher, S., Hobday, A. J., Wernberg, T., Smale, D. A., Sunday, J. M., Hill, N. A., Dulvy, N. K., Colwell, R. K., Holbrook, N. J., Fulton, E. A., Slawinski, D., Feng, M., Edgar, G. J., Radford, B. T., Thompson, P. A., and Watson, R. A. (2014). Defining and observing stages of climate-mediated range shifts in marine systems. Global Environmental Change 26, 27–38.
Defining and observing stages of climate-mediated range shifts in marine systems.Crossref | GoogleScholarGoogle Scholar |

Beck, H. J., Feary, D. A., Figueira, W. F., and Booth, D. J. (2014). Assessing range shifts of tropical reef fishes: a comparison of belt transect and roaming underwater visual census methods. Bulletin of Marine Science 90, 705–721.
Assessing range shifts of tropical reef fishes: a comparison of belt transect and roaming underwater visual census methods.Crossref | GoogleScholarGoogle Scholar |

Booth, D., Figueira, W., Gregson, M., Brown, L., and Beretta, G. (2007). Occurrence of tropical fishes in temperate southeastern Australia: role of the East Australian Current. Estuarine, Coastal and Shelf Science 72, 102–114.
Occurrence of tropical fishes in temperate southeastern Australia: role of the East Australian Current.Crossref | GoogleScholarGoogle Scholar |

Booth, D. J., Bond, N., and Macreadie, P. (2011). Detecting range shifts among Australian fishes in response to climate change. Marine and Freshwater Research 62, 1027–1042.
Detecting range shifts among Australian fishes in response to climate change.Crossref | GoogleScholarGoogle Scholar |

Chadwick, N. E., and Arvedlund, M. (2005). Abundance of giant sea anemones and patterns of association with anemone¢sh in the northern Red Sea. Journal of the Marine Biological Association of the United Kingdom 85, 1287–1292.
Abundance of giant sea anemones and patterns of association with anemone¢sh in the northern Red Sea.Crossref | GoogleScholarGoogle Scholar |

Cheung, W. W., Lam, V. W., Sarmiento, J. L., Kearney, K., Watson, R., and Pauly, D. (2009). Projecting global marine biodiversity impacts under climate change scenarios. Fish and Fisheries 10, 235–251.
Projecting global marine biodiversity impacts under climate change scenarios.Crossref | GoogleScholarGoogle Scholar |

Cheung, W. W. L., Meeuwig, J. J., Feng, M., Harvey, E., Lam, V. W. H., Langlois, T., Slawinski, D., Sun, C., and Pauly, D. (2012). Climate-change induced tropicalisation of marine communities in Western Australia. Marine and Freshwater Research 63, 415–427.
Climate-change induced tropicalisation of marine communities in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Dunn, D. F. (1981). The clownfish sea anemones. Stichodactylidae (Coelenterata: Actinaria) and other sea anemones symbiotic with pomacentrid fishes. Transactions of the American Philosophical Society 71, 3–115.
The clownfish sea anemones. Stichodactylidae (Coelenterata: Actinaria) and other sea anemones symbiotic with pomacentrid fishes.Crossref | GoogleScholarGoogle Scholar |

Fautin, D. G., and Allen, G. R. (1997). ‘Anemonefishes and their Host Sea Anemones: a Guide for Aquarists and Divers.’ (Western Australian Museum: Perth, WA, Australia.)

Feary, D. A., Pratchett, M. S. J., Emslie, M., Fowler, A. M., Figueira, W. F., Luiz, O. J., Nakamura, Y., and Booth, D. J. (2014). Latitudinal shifts in coral reef fishes: why some species do and others do not shift. Fish and Fisheries 15, 593–615.
Latitudinal shifts in coral reef fishes: why some species do and others do not shift.Crossref | GoogleScholarGoogle Scholar |

Figueira, W. F., and Booth, D. J. (2010). Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Global Change Biology 16, 506–516.
Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters.Crossref | GoogleScholarGoogle Scholar |

Figueira, W. F., Biro, P., Booth, D. J., and Valenzuela, V. C. (2009). Performance of tropical fish recruiting to temperate habitats: role of ambient temperature and implications of climate change. Marine Ecology Progress Series 384, 231–239.
Performance of tropical fish recruiting to temperate habitats: role of ambient temperature and implications of climate change.Crossref | GoogleScholarGoogle Scholar |

Floeter, S. R., Krohling, W., Gasparini, J. L., Ferreira, C. E. L., and Zalmon, I. R. (2007). Reef fish community structure on coastal islands of the southeatern Brazil: the influence of exposure and benthic cover. Environmental Biology of Fishes 78, 147–160.
Reef fish community structure on coastal islands of the southeatern Brazil: the influence of exposure and benthic cover.Crossref | GoogleScholarGoogle Scholar |

Greenstein, B. J., and Pandolfi, J. M. (2008). Escaping the heat: range shifts of reef coral taxa in coastal Western Australia. Global Change Biology 14, 513–528.
Escaping the heat: range shifts of reef coral taxa in coastal Western Australia.Crossref | GoogleScholarGoogle Scholar |

Hobday, A. J., and Lough, J. M. (2011). Projected climate change in Australian marine and freshwater environments. Marine and Freshwater Research 62, 1000–1014.
Projected climate change in Australian marine and freshwater environments.Crossref | GoogleScholarGoogle Scholar |

Hurst, T. P. (2007). Causes and consequences of winter mortality in fishes. Journal of Fish Biology 71, 315–345.
Causes and consequences of winter mortality in fishes.Crossref | GoogleScholarGoogle Scholar |

Hurst, T. P., and Conover, D. O. (2002). Effects of temperature and salinity on survival of young-of-the-year Hudson River striped bass (Morone saxatilis): implications for optimal overwintering habitats. Canadian Journal of Fisheries and Aquatic Sciences 59, 787–795.
Effects of temperature and salinity on survival of young-of-the-year Hudson River striped bass (Morone saxatilis): implications for optimal overwintering habitats.Crossref | GoogleScholarGoogle Scholar |

Lambers, J. (2015). Extinction risks from climate change: how will climate change affect global biodiversity. Science 348, 501–502.
Extinction risks from climate change: how will climate change affect global biodiversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptlWisLs%3D&md5=80417e7e1fb03d7a064a821142acfbf0CAS |

Ling, S. D., Johnson, C. R., Ridgeway, K. R., Hobday, A. J., and Haddon, M. (2009). Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Global Change Biology 15, 719–731.
Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics.Crossref | GoogleScholarGoogle Scholar |

Malcolm, H. A., Smith, S. D. A., and Jordan, A. (2010a). Using patterns of reef fish assemblages to refine a habitat classification system for marine parks in NSW, Australia. Aquatic Conservation: Marine and Freshwater Ecosystems 20, 83–92.

Malcolm, H. A., Jordan, A., and Smith, S. D. A. (2010b). Biogeographical and cross-shelf patterns of reef fish assemblages in a transition zone. Marine Biodiversity 40, 181–193.
Biogeographical and cross-shelf patterns of reef fish assemblages in a transition zone.Crossref | GoogleScholarGoogle Scholar |

Malcolm, H. A., Davies, P., Jordan, A., and Smith, S. D. A. (2011). Variation in sea temperature and the East Australian Current in the Solitary Islands region between 2001 to 2008. Deep-sea Research – II. Topical Studies in Oceanography 58, 616–627.
Variation in sea temperature and the East Australian Current in the Solitary Islands region between 2001 to 2008.Crossref | GoogleScholarGoogle Scholar |

Moyer, J. T. (1980). Influence of temperate waters on the behaviour of the tropical anemonefish Amphiprion clarkii at Miyake-jima, Japan. Bulletin of Marine Science 30, 261–272.

Nakamura, Y., Feary, D. A., Kanda, M., and Yamaoka, K. (2013). Tropical fishes dominate temperate reef fish communities within western Japan. PLoS One 8, e81107.
Tropical fishes dominate temperate reef fish communities within western Japan.Crossref | GoogleScholarGoogle Scholar |

Ollerton, J., McCollin, D., Fautin, D. G., and Allen, G. R. (2007). Finding NEMO: nestedness engendered by mutualistic organization in anemonefish and their hosts. Proceedings of the Royal Society of London – B. Biological Sciences 274, 591–598.
Finding NEMO: nestedness engendered by mutualistic organization in anemonefish and their hosts.Crossref | GoogleScholarGoogle Scholar |

Perry, A. L., Low, P. J., Ellis, J. R., and Reynolds, J. D. (2005). Climate change and distribution shifts in marine fishes. Science 308, 1912–1915.
Climate change and distribution shifts in marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsVWmtbg%3D&md5=e9dc4319ee57f15c99620032a581c12eCAS |

Poloczanska, E. S., Babcock, R. C., Butler, A., Hobday, A. J., Hoegh-Guldberg, O., Kunz, T. J., Matear, R., Milton, D. A., Okey, T. A., and Richardson, A. J. (2007). Climate change and Australian marine life. Oceanography and Marine Biology – an Annual Review 45, 407–478.

Poloczanska, E. S., Brown, C. J., Sydeman, W. J., Kiessling, W., Schoeman, D. S., Moore, P. J., Brander, K., Bruno, J. F., Buckley, L. B., Burrows, M. T., Duarte, C. M., Halpern, B. S., Holding, J., Kappel, C. V., O’Connor, M. I., Pandolfi, J. M., Permesan, C., Schwing, F., Thompson, S. A., and Richardson, A. J. (2013). Global imprint of climate change on marine life. Nature Climate Change 3, 919–925.
Global imprint of climate change on marine life.Crossref | GoogleScholarGoogle Scholar |

Precht, W. F., and Aronson, R. B. (2004). Climate flickers and range shifts of reef corals. Frontiers in Ecology and the Environment 2, 307–314.
Climate flickers and range shifts of reef corals.Crossref | GoogleScholarGoogle Scholar |

Richardson, D. L. (1996). Factors influencing the ecology of anemonefishes (Pomacetridae: Amphiprion) and giant anemones (Actinaria) within sub-tropical eastern Australian waters. Ph.D. Thesis, Southern Cross University, Lismore, NSW, Australia.

Ridgway, K. R. (2007). Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophysical Research Letters 34, L13613.
Long-term trend and decadal variability of the southward penetration of the East Australian Current.Crossref | GoogleScholarGoogle Scholar |

Roughan, M., and Middleton, J. H. (2004). On the East Australian Current: variability, encroachment, and upwelling. Journal of Geophysical Research 109, C07003.
On the East Australian Current: variability, encroachment, and upwelling.Crossref | GoogleScholarGoogle Scholar |

Scott, A., and Harrison, P. (2007). Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis cripsa, that host anemone fish. Invertebrate Reproduction & Development 50, 163–171.
Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis cripsa, that host anemone fish.Crossref | GoogleScholarGoogle Scholar |

Scott, A., and Harrison, P. L. (2008). Larval settlement and juvenile development of sea anemones that provide habitat for anemonefish. Marine Biology 154, 833–839.
Larval settlement and juvenile development of sea anemones that provide habitat for anemonefish.Crossref | GoogleScholarGoogle Scholar |

Scott, A., Malcolm, H. A., Damiano, C., and Richardson, D. L. (2011). Long-term increases in abundance of anemonefish and their host sea anemones in an Australian marine protected area. Marine and Freshwater Research 62, 187–196.
Long-term increases in abundance of anemonefish and their host sea anemones in an Australian marine protected area.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitlejtrc%3D&md5=7602ac5803ff54999db3e465b032d59eCAS |

Scott, A., Harasti, D., Davis, T., and Smith, S. D. A. (2015). Southernmost records of the host sea anemone, Stichodactyla haddoni, and associated commensal shrimps in a climate change hotspot. Marine Biodiversity 45, 145–146.
Southernmost records of the host sea anemone, Stichodactyla haddoni, and associated commensal shrimps in a climate change hotspot.Crossref | GoogleScholarGoogle Scholar |

Scott, A., Rushworth, K., Dalton, S., and Smith, S. (2016). Subtropical anemonefish Amphiprion latezonatus recorded in two additional species of host sea anemone. Marine Biodiversity 46, 327.
Subtropical anemonefish Amphiprion latezonatus recorded in two additional species of host sea anemone.Crossref | GoogleScholarGoogle Scholar |

Sommer, B., Harrison, P. L., Beger, M., and Pandolfi, J. M. (2014). Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95, 1000–1009.
Trait-mediated environmental filtering drives assembly at biogeographic transition zones.Crossref | GoogleScholarGoogle Scholar |

Sorte, C. J., Williams, S. L., and Carlton, J. T. (2010). Marine range shifts and species introductions: comparative spread rates and community impacts. Global Ecology and Biogeography 19, 303–316.
Marine range shifts and species introductions: comparative spread rates and community impacts.Crossref | GoogleScholarGoogle Scholar |

Sunday, J. M., Peci, G. T., Frusher, S., Hobday, A. J., Hill, N., Holbrook, N. J., Edgar, G. J., Stuart-Smith, R., Barrett, N., Wernberg, T., Watson, R. A., Smale, D. A., Fulton, E. A., Slawinski, D., Feng, M., Radford, B. T., Thompson, P. A., and Bates, A. E. (2015). Species traits and climate velocity explain geographic range shifts in an ocean warming hotspot. Ecology Letters 18, 944–953.
Species traits and climate velocity explain geographic range shifts in an ocean warming hotspot.Crossref | GoogleScholarGoogle Scholar |

Suthers, I. M., Young, J. W., Baird, M. E., Roughan, M., Everett, J. D., Brassington, G. B., Byrne, M., Condie, S. A., Hartog, J. R., Hassler, C. S., Hobday, A. J., Holbrook, N. J., Malcolm, H. A., Oke, P. R., Thompson, P. A., and Ridgway, K. R. (2011). The strengthening East Australian Current, its eddies and biological effects: an introduction and overview. Deep-sea Research – II. Topical Studies in Oceanography 58, 538–546.
The strengthening East Australian Current, its eddies and biological effects: an introduction and overview.Crossref | GoogleScholarGoogle Scholar |

Vergés, A., Steinberg, P. D., Hay, M. E., Poore, A. G., Campbell, A. H., Ballesteros, E., Heck, K. L., Booth, D. J., Coleman, M. A., and Feary, D. A. (2014). The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20140846.
The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts.Crossref | GoogleScholarGoogle Scholar |

Vergés, A., Doropoulos, C., Malcolm, H. A., Skye, M., Garcia-Piza, M., Marzinelli, E. M., Campbell, A. H., Ballesteros, E., Hoey, A. S., Vila-Concejo, A., Bozec, Y.-M., and Steinberg, P. D. (2016). Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proceedings of the National Academy of Science 113, 13791–13796.
Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp.Crossref | GoogleScholarGoogle Scholar |

Wernberg, T., Bennett, S., Babcock, R. C., de Bettignies, T., Cure, K., Depczynski, M., Dufois, F., Fromont, J., Fulton, C. J., Hovey, R. K., Harvey, E. S., Holmes, T. H., Kendrick, G. A., Radford, B., Santana-Garcon, J., Saunders, B. J., Smale, D. A., Thomsen, M. S., Tuckett, C. A., Tuya, F., Vanderklift, M. A., and Wilson, S. (2016). Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172.
Climate-driven regime shift of a temperate marine ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFSisrjJ&md5=39fd59d4acc576d1cd7780f007b7285dCAS |

Yamano, H., Sugihara, K., and Nomura, K. (2011). Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophysical Research Letters 38, L04601.
Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures.Crossref | GoogleScholarGoogle Scholar |