Seasonal feeding on giant cuttlefish (Sepia apama) by Indo-Pacific bottlenose dolphins (Tursiops aduncus) in south-western Australia
H. C. Smith A B C and K. R. Sprogis AA Cetacean Research Unit, Murdoch University, Perth, WA 6150, Australia.
B Marine Science Program, Department of Parks and Wildlife, Perth, WA 6151, Australia.
C Corresponding author. Email: holly.raudino@dpaw.wa.gov.au
Australian Journal of Zoology 64(1) 8-13 https://doi.org/10.1071/ZO15075
Submitted: 11 November 2015 Accepted: 24 February 2016 Published: 18 March 2016
Abstract
We report on observations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) feeding on giant cuttlefish (Sepia apama) from March 2007 to April 2013 in the temperate waters off Bunbury, south-western Australia. Seventeen feeding events were observed during the cooler months between July and September in relatively shallow coastal waters, with 12 dolphins identified as adult females. We observed behavioural sequences of complex prey-handling of cuttlefish where dolphins’ used multiple steps to remove the cuttlefish head, ink and cuttlebone before consuming the flesh of the cuttlefish mantle. Our study provides valuable information to the limited knowledge on the complex prey-handling by T. aduncus on cuttlefish in Australia, and is complementary to other known specialised foraging behaviours of bottlenose dolphins. This study also details a different behavioural sequence of cuttlefish prey-handling to that of the bottlenose dolphins in the Sado estuary, Portugal, where only the head is consumed, and to the Spencer Gulf, Australia, in that the dolphins in Bunbury carry the cuttlefish mantle over their rostrum before removing the cuttlebone. Information on S. apama in Bunbury is scarce, therefore studies on abundance, distribution and egg-laying sites are recommended in order to enable informed decision making and to understand the importance of S. apama to the diet of T. aduncus.
References
Allen, S. J., Bejder, L., and Krützen, M. (2011). Why do Indo-Pacific bottlenose dolphins (Tursiops sp.) carry conch shells (Turbinella sp.) in Shark Bay, Western Australia? Marine Mammal Science 27, 449–454.| Why do Indo-Pacific bottlenose dolphins (Tursiops sp.) carry conch shells (Turbinella sp.) in Shark Bay, Western Australia?Crossref | GoogleScholarGoogle Scholar |
Amir, O. A., Berggren, P., Ndaro, S. G. M., and Jiddawi, N. S. (2005). Feeding ecology of the Indo-Pacific bottlenose dolphin (Tursiops aduncus) incidentally caught in the gillnet fisheries off Zanzibar, Tanzania. Estuarine, Coastal and Shelf Science 63, 429–437.
| Feeding ecology of the Indo-Pacific bottlenose dolphin (Tursiops aduncus) incidentally caught in the gillnet fisheries off Zanzibar, Tanzania.Crossref | GoogleScholarGoogle Scholar |
Barratt, I., and Allcock, L. (2012). Sepia apama. In ‘The IUCN Red List of Threatened Species’. (Version 2015.2) Available at: http://www.iucnredlist.org/ [accessed 6 August 2015].
Barros, N. B., Parsons, E. C. M., and Jefferson, T. A. (2000). Prey of offshore bottlenose dolphins from the South China Sea. Aquatic Mammals 26, 2–6.
Battam, H., Richardson, M., Watson, A. W. T., and Buttemer, W. A. (2010). Chemical composition and tissue energy density of the cuttlefish (Sepia apama) and its assimilation efficiency by Diomedea albatrosses. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 180, 1247–1255.
| Chemical composition and tissue energy density of the cuttlefish (Sepia apama) and its assimilation efficiency by Diomedea albatrosses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12qu7bK&md5=fb09f32b868f0adbe8ee25e479cfab04CAS | 20640855PubMed |
Bernard, H. J., and Hohn, A. A. (1989). Differences in feeding habits between pregnant and lactating spotted dolphins (Stenella attenuata). Journal of Mammalogy 70, 211–215.
| Differences in feeding habits between pregnant and lactating spotted dolphins (Stenella attenuata).Crossref | GoogleScholarGoogle Scholar |
Cockcroft, V. G., and Ross, G. J. B. (1990). Food and feeding of the Indian Ocean bottlenose dolphin off southern Natal, South Africa. In ‘The Bottlenose Dolphin’. (Ed. S. R. Leatherwood.) pp. 295–328. (Academic Press, Inc.: San Diego, CA.)
Connor, R. C., Heithaus, M. R., Berggren, P., and Miksis, J. L. (2000). Kerplunking: surface fluke-splashes during shallow-water bottom foraging by bottlenose dolphins. Marine Mammal Science 16, 646–653.
| Kerplunking: surface fluke-splashes during shallow-water bottom foraging by bottlenose dolphins.Crossref | GoogleScholarGoogle Scholar |
de Waal, F. B. M., and Tyack, P. L. (2003). ‘Animal Social Complexity: Intelligence, Culture, and Individualized Societies.’ (Harvard University Press: Cambridge, MA.)
dos Santos, M. E., and Lacerda, M. (1987). Preliminary observations of the bottlenose dolphin (Tursiops truncatus) in the Sado Estuary (Portugal). Aquatic Mammals 13, 65–80.
dos Santos, M. E., Coniglione, C., and Louro, S. (2007). Feeding behaviour of the bottlenose dolphin, Tursiops truncatus (montagu, 1821) in the Sado Estuary, Portugal, and a review of its prey species. Zoociências 9, 31–39.
Dupavillon, J. L., and Gillanders, B. M. (2009). Impacts of seawater desalination on the giant Australian cuttlefish Sepia apama in the upper Spencer Gulf, South Australia. Marine Environmental Research 67, 207–218.
| Impacts of seawater desalination on the giant Australian cuttlefish Sepia apama in the upper Spencer Gulf, South Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlslajsLc%3D&md5=9449b73fa83d403df8a60852f0cdb1a1CAS | 19332355PubMed |
Fernández, R., Santos, M. B., Carrillo, M., Tejedor, M., and Pierce, G. J. (2009). Stomach contents of cetaceans stranded in the Canary Islands 1996–2006. Journal of the Marine Biological Association of the United Kingdom 89, 873–883.
| Stomach contents of cetaceans stranded in the Canary Islands 1996–2006.Crossref | GoogleScholarGoogle Scholar |
Finn, J., Tregenza, T., and Norman, M. (2009). Preparing the perfect cuttlefish meal: complex prey handling by dolphins. PLoS One 4, e4217.
| Preparing the perfect cuttlefish meal: complex prey handling by dolphins.Crossref | GoogleScholarGoogle Scholar | 19156212PubMed |
Fiorito, G., and Gherardi, F. (1999). Prey-handling behaviour of Octopus vulgaris (Mollusca, Cephalopoda) on bivalve preys. Behavioural Processes 46, 75–88.
| Prey-handling behaviour of Octopus vulgaris (Mollusca, Cephalopoda) on bivalve preys.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cfitlSmsQ%3D%3D&md5=9be8c0985998f9dda528479fb0062cf6CAS | 24925500PubMed |
Gannon, D. P., and Waples, D. M. (2004). Diets of coastal bottlenose dolphins from the U.S. mid-Atlantic coast differ by habitat. Marine Mammal Science 20, 527–545.
| Diets of coastal bottlenose dolphins from the U.S. mid-Atlantic coast differ by habitat.Crossref | GoogleScholarGoogle Scholar |
Gibbs, S. E., Harcourt, R. G., and Kemper, C. M. (2011). Niche differentiation of bottlenose dolphin species in South Australia revealed by stable isotopes and stomach contents. Wildlife Research 38, 261–270.
| Niche differentiation of bottlenose dolphin species in South Australia revealed by stable isotopes and stomach contents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFeks7bE&md5=21dba7ac2e9e0367b472ce4478f4e631CAS |
Gowlett-Holmes, K. (2008). ‘A Field Guide to the Marine Invertebrates of South Australia.’ (Notomares: Hobart.)
Hall, K. C., and Hanlon, R. T. (2002). Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Marine Biology 140, 533–545.
| Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda).Crossref | GoogleScholarGoogle Scholar |
Kopps, A. M., Ackermann, C. Y., Sherwin, W. B., Allen, S. J., Bejder, L., and Krutzen, M. (2014). Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins. Proceedings of the Royal Society B: Biological Sciences 281, 20133245.
| Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins.Crossref | GoogleScholarGoogle Scholar | 24648223PubMed |
Lipinski, M. R., and Jackson, S. (1989). Surface-feeding on cephalopods by procellariiform seabirds in the southern Benguela region. South African Journal of Zoology 218, 549–563.
Lu, C. C. (1998). A synopsis of Sepiidae in Australian waters (Cephalopods: Sepioidea). In ‘Systematics and Biogeography of Cephalopods’. (Eds N. A. Voss, M. Vecchione, R. B. Toll and M. J. Sweeney.) pp. 159–190. (Smithsonian Institution Press: Washington.)
Mann, J., and Patterson, E. (2013). Tool use by aquatic animals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 368, 20120424.
| Tool use by aquatic animals.Crossref | GoogleScholarGoogle Scholar | 24101631PubMed |
Mann, J., and Sargeant, B. (2003). Like mother, like calf: the ontogeny of foraging traditions in wild Indian Ocean bottlenose dolphins (Tursiops sp.). Chapter 9. In ‘The Biology of Traditions: Models and Evidence’. (Eds D. M. Fragaszy and S. Perry.) pp. 236–266. (Cambridge University Press: Cambridge.)
McCluskey, S. M., Bejder, L., and Loneragan, N. R. (2016). Dolphin prey availability and calorific value in an estuarine and coastal environment. Frontiers in Marine Science 3, .
| Dolphin prey availability and calorific value in an estuarine and coastal environment.Crossref | GoogleScholarGoogle Scholar |
Norman, M., and Reid, A. (2000). ‘A Guide to Squid, Cuttlefish and Octopuses of Australasia.’ (CSIRO Publishing: Melbourne.)
O’Brien, E. L., Burger, A. E., and Dawson, R. D. (2005). Foraging decision rules and prey species preferences of northwestern crows (Corvus caurinus). Ethology 111, 77–87.
| Foraging decision rules and prey species preferences of northwestern crows (Corvus caurinus).Crossref | GoogleScholarGoogle Scholar |
Patterson, E. M., and Mann, J. (2015). Cetacean innovation. Chapter 4. In ‘Animal Creativity and Innovation’. (Eds A. B. Kaufman, and J. C. Kaufman.) pp. 73–120. (Elsevier: London)
Ponnampalam, L. S., Collins, T. J. Q., Minton, G., Schulz, I., Gray, H., Ormond, R. F. G., and Baldwin, R. M. (2012). Stomach contents of small cetaceans stranded along the Sea of Oman and Arabian Sea coasts of the Sultanate of Oman. Journal of the Marine Biological Association of the United Kingdom 92, 1699–1710.
| Stomach contents of small cetaceans stranded along the Sea of Oman and Arabian Sea coasts of the Sultanate of Oman.Crossref | GoogleScholarGoogle Scholar |
Riedman, M. L., and Estes, J. A. (1988). A review of the history, distribution and foraging ecology of sea otters. In ‘The Community Ecology of Sea Otters.’ (Eds G. VanBlaricom and J. Estes.) pp. 4–21. (Springer: Berlin and Heidelberg.)
Santos, M. B., Fernandez, R., Lopez, A., Martinez, J. A., and Pierce, G. J. (2007). Variability in the diet of bottlenose dolphin, Tursiops truncatus, in Galician waters, north-western Spain, 1990–2005. Journal of the Marine Biological Association of the United Kingdom 87, 231–241.
| Variability in the diet of bottlenose dolphin, Tursiops truncatus, in Galician waters, north-western Spain, 1990–2005.Crossref | GoogleScholarGoogle Scholar |
Sargeant, B., and Mann, J. (2009). Developmental evidence for foraging traditions in wild bottlenose dolphins. Animal Behaviour 78, 715–721.
| Developmental evidence for foraging traditions in wild bottlenose dolphins.Crossref | GoogleScholarGoogle Scholar |
Sargeant, B. L., Mann, J., Berggren, P., and Krützen, M. (2005). Specialization and development of beach hunting, a rare foraging behavior, by wild bottlenose dolphins (Tursiops sp.). Canadian Journal of Zoology 83, 1400–1410.
| Specialization and development of beach hunting, a rare foraging behavior, by wild bottlenose dolphins (Tursiops sp.).Crossref | GoogleScholarGoogle Scholar |
Schulz, M. (1988). Dolphins and the giant cuttlefish Sepia apama. Victorian Naturalist 105, 48–49.
Sherrard, K. M. (2000). Cuttlebone morphology limits habitat depth in eleven species of Sepia (Cephalopoda: Sepiidae). The Biological Bulletin 198, 404–414.
| Cuttlebone morphology limits habitat depth in eleven species of Sepia (Cephalopoda: Sepiidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FgvFKjtw%3D%3D&md5=4279447d4dbb15b9048e22aa2d292cf7CAS | 10897454PubMed |
Smith, H. C. (2012). Population dynamics and habitat use of bottlenose dolphins (Tursiops aduncus), Bunbury, Western Australia. Ph.D. Thesis, Murdoch University, Perth.
Smith, H. C., Pollock, K., Waples, K., Bradley, S., and Bejder, L. (2013). Use of the robust design to estimate seasonal abundance and demographic parameters of a coastal bottlenose dolphin (Tursiops aduncus) population. PLoS One 8, e76574.
| Use of the robust design to estimate seasonal abundance and demographic parameters of a coastal bottlenose dolphin (Tursiops aduncus) population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1egs7%2FO&md5=6cf3c63c42bc9e33015be7b04dfa9d16CAS | 24130781PubMed |
Smith, H., Frère, C., Kobryn, H., and Bejder, L. (2016). Dolphin sociality, distribution and calving as important behavioural patterns informing management. Animal Conservation , .
| Dolphin sociality, distribution and calving as important behavioural patterns informing management.Crossref | GoogleScholarGoogle Scholar |
Smolker, R. A., Richards, A. F., Connor, R. C., Mann, J., and Berggren, P. (1997). Sponge-carrying by Indian Ocean bottlenose dolphins: possible tool-use by a delphinid. Ethology 103, 454–465.
| Sponge-carrying by Indian Ocean bottlenose dolphins: possible tool-use by a delphinid.Crossref | GoogleScholarGoogle Scholar |
Sprogis, K. R. (2015). Sex-specific patterns in abundance, home ranges and habitat use of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in south-western Australia. Ph.D. Thesis, Murdoch University, Perth.
Sprogis, K. R., Pollock, K. H., Raudino, H. C., Allen, S. J., Kopps, A. M., Manlik, O., Tyne, J. A., and Bejder, L. (2016a). Sex-specific patterns in abundance, temporary emigration and survival of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in coastal and estuarine waters. Frontiers in Marine Science 3, 12.
| Sex-specific patterns in abundance, temporary emigration and survival of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in coastal and estuarine waters.Crossref | GoogleScholarGoogle Scholar |
Sprogis, K. R., Raudino, H. C., Rankin, R., MacLeod, C. D., and Bejder, L. (2016b). Home range size of adult Indo-Pacific bottlenose dolphins (Tursiops aduncus) in a coastal and estuarine system is habitat and sex-specific. Marine Mammal Science 32, 287–308.
| Home range size of adult Indo-Pacific bottlenose dolphins (Tursiops aduncus) in a coastal and estuarine system is habitat and sex-specific.Crossref | GoogleScholarGoogle Scholar |
Tinker, M. T., Bentall, G., and Estes, J. A. (2008). Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proceedings of the National Academy of Sciences of the United States of America 105, 560–565.
| Food limitation leads to behavioral diversification and dietary specialization in sea otters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvV2ksw%3D%3D&md5=f3a655a0490fb8a58064744b1a9463e5CAS | 18195370PubMed |
Torres, L. G., and Read, A. J. (2009). Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida. Marine Mammal Science 25, 797–815.
| Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida.Crossref | GoogleScholarGoogle Scholar |