Behaviour and survivorship of a dasyurid predator (Antechinus flavipes) in response to encounters with the toxic and invasive cane toad (Rhinella marina)
Wiebke Kämper A B D , Jonathan K. Webb A C , Mathew S. Crowther A , Matthew J. Greenlees A and Richard Shine A
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, University of Sydney, NSW 2006, Australia.
B Behavioural Biology, University of Leiden, 2300 RA Leiden, The Netherlands.
C School of the Environment, University of Technology Sydney, Broadway, NSW 2007, Australia.
D Corresponding author. Email: Wiebkekaemper@gmail.com
Australian Mammalogy 35(2) 136-143 https://doi.org/10.1071/AM12025
Submitted: 14 May 2012 Accepted: 6 September 2012 Published: 21 December 2012
Abstract
Australia’s biogeographical isolation has rendered many endemic species vulnerable to invaders. The recent spread of the cane toad (Rhinella marina) has caused serious population declines for some predatory reptile and mammal species. To determine a priori whether or not cane toad poisoning endangers native species, we can test the fates of predators in laboratory trials. We investigated whether an Australian marsupial whose range is increasingly being occupied by cane toads (the yellow-footed antechinus, Antechinus flavipes) is at risk of toad poisoning by testing (1) whether yellow-footed antechinuses approach or attack cane toads and, if so, whether they die as a result; and (2) if they survive, whether they then learn to avoid toads in subsequent encounters. We also investigated the effects of sympatry with toads on the feeding response. In all, 58% of antechinuses from eastern New South Wales approached or attacked a toad (over 4 or 5 opportunities to do so, on successive nights), and none showed ill effects after doing so. Antechinuses that attacked (killed or ingested) toads rapidly learnt to avoid them. Antechinuses from toad-exposed populations ingested more toad flesh, but otherwise reacted in the same ways as did conspecifics from toad-free areas. Hence, the yellow-footed antechinus is unlikely to face population declines via toad poisoning.
Additional keywords: invasive species, predator learning, taste aversion, toxic prey.
References
Aldridge, V., Dovey, T. M., and Halford, J. C. G. (2009). The role of familiarity in dietary development. Developmental Review 29, 32–44.| The role of familiarity in dietary development.Crossref | GoogleScholarGoogle Scholar |
Burbidge, A., and McKenzie, N. (1989). Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications. Biological Conservation 50, 143–198.
| Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications.Crossref | GoogleScholarGoogle Scholar |
Burnett, S. (1997). Colonizing cane toads cause population declines in native predators: reliable anecdotal information and management implications. Pacific Conservation Biology 3, 65–72.
Chisholm, R. A., and Taylor, R. (2010). Body size and extinction risk in Australian mammals: an information-theoretic approach. Austral Ecology 35, 616–623.
| Body size and extinction risk in Australian mammals: an information-theoretic approach.Crossref | GoogleScholarGoogle Scholar |
Covacevich, J., and Archer, M. (1975). The distribution of the cane toad, Bufo marinus, in Australia and its effects on indigenous vertebrates. Memoirs of the Queensland Museum 17, 305–310.
Crowther, M. S. (2008). Yellow-footed antechinus Antechinus flavipes. In ‘Mammals of Australia’. (Eds S. Van Dyck and R. Strahan.) pp. 86–88. (New Holland: Sydney.)
Dickman, C. R., Pressey, R. L., Lim, L., and Parnaby, H. E. (1993). Mammals of particular conservation concern in the western division of New South Wales. Biological Conservation 65, 219–248.
| Mammals of particular conservation concern in the western division of New South Wales.Crossref | GoogleScholarGoogle Scholar |
Doody, J. S., Green, B., Rhind, D., Castellano, C. M., Sims, R., and Robinson, T. (2009). Population-level declines in Australian predators caused by an invasive species. Animal Conservation 12, 46–53.
| Population-level declines in Australian predators caused by an invasive species.Crossref | GoogleScholarGoogle Scholar |
Greenlees, M. J., Phillips, B. L., and Shine, R. (2010). Adjusting to a toxic invader: native Australian frogs learn not to prey on cane toads. Behavioral Ecology 21, 966–971.
| Adjusting to a toxic invader: native Australian frogs learn not to prey on cane toads.Crossref | GoogleScholarGoogle Scholar |
Hayes, R. A., Crossland, M. R., Hagman, M., Capon, R. J., and Shine, R. (2009). Ontogenetic variation in the chemical defenses of cane toads (Bufo marinus): toxin profiles and effects on predators. Journal of Chemical Ecology 35, 391–399.
| Ontogenetic variation in the chemical defenses of cane toads (Bufo marinus): toxin profiles and effects on predators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlt1Kis74%3D&md5=6608ccec57bbfb615102c55e279ff87dCAS |
Johnson, C. N. (2006). ‘Australia’s Mammal Extinctions – A 50 000 year history.’ (Cambridge University Press: New York.)
Johnson, C. N., and Isaac, J. L. (2009). Body mass and extinction risk in Australian marsupials: the ‘Critical Weight Range’ revisited. Austral Ecology 34, 35–40.
| Body mass and extinction risk in Australian marsupials: the ‘Critical Weight Range’ revisited.Crossref | GoogleScholarGoogle Scholar |
Johnson, C. N., Delean, S., and Balmford, A. (2002). Phylogeny and the selectivity of extinction in Australian marsupials. Animal Conservation 5, 135–142.
| Phylogeny and the selectivity of extinction in Australian marsupials.Crossref | GoogleScholarGoogle Scholar |
Johnson, K. A., Burbidge, A. A., and McKenzie, N. L. (1989). Australian Macropodoidea: status, causes of delcine and future research and management. In ‘Kangaroos, Wallabies and Rat-Kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 641–657. (Surrey Beatty: Sydney)
Letnic, M., Webb, J. K., and Shine, R. (2008). Invasive cane toads (Bufo marinus) cause mass mortality of freshwater crocodiles (Crocodylus johnstoni) in tropical Australia. Biological Conservation 141, 1773–1782.
| Invasive cane toads (Bufo marinus) cause mass mortality of freshwater crocodiles (Crocodylus johnstoni) in tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Llewelyn, J., Webb, J. K., Schwarzkopf, L., Alford, R., and Shine, R. (2010). Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus). Austral Ecology 35, 560–567.
| Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus).Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., Burbidge, A. A., Baynes, A., Brereton, R. N., Dickman, C. R., Gordon, G., Gibson, L. A., Menkhorst, P. W., Robinson, A. C., Williams, M. R., and Woinarski, J. C. Z. (2007). Analysis of factors implicated in the recent decline of Australia’s mammal fauna. Journal of Biogeography 34, 597–611.
| Analysis of factors implicated in the recent decline of Australia’s mammal fauna.Crossref | GoogleScholarGoogle Scholar |
Morton, S. R. (1990). The impact of European settlement on the vertebrate animals of arid Australia: a conceptual model. In ‘Australian Ecosystems: 200 years of Utilization, Degradation and Reconstruction’. (Eds D. A. Saunders, A. J. M. Hopkins and R. A. How.) pp. 201–213. (Ecological Society of Australia: Sydney.)
Newell, D. (2011). Recent invasions of World Heritage rainforests in north-east New South Wales by the cane toad Bufo marinus. Australian Zoologist 35, 876–883.
O’Donnell, S., Webb, J. K., and Shine, R. (2010). Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader. Journal of Applied Ecology 47, 558–565.
| Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader.Crossref | GoogleScholarGoogle Scholar |
Pearl, C. A., Adams, M. J., Schuytema, G. S., and Nebeker, A. V. (2003). Behavioral responses of anuran larvae to chemical cues of native and introduced predators in the Pacific northwestern United States. Journal of Herpetology 37, 572–576.
| Behavioral responses of anuran larvae to chemical cues of native and introduced predators in the Pacific northwestern United States.Crossref | GoogleScholarGoogle Scholar |
Phillips, B. L., and Shine, R. (2006). An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proceedings. Biological Sciences 273, 1545–1550.
| An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia.Crossref | GoogleScholarGoogle Scholar |
Phillips, B. L., Brown, G. P., and Shine, R. (2003). Assessing the potential impact of cane toads on Australian snakes. Conservation Biology 17, 1738–1747.
| Assessing the potential impact of cane toads on Australian snakes.Crossref | GoogleScholarGoogle Scholar |
Phillips, B. L., Greenlees, M. J., Brown, G. P., and Shine, R. (2010). Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia. Animal Conservation 13, 53–59.
| Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia.Crossref | GoogleScholarGoogle Scholar |
Pliner, P., and Salvy, S.J. (2006). ‘The Psychology of Food Choice.’ (University of Surrey: UK)
Price-Rees, S. J., Brown, G. P., and Shine, R. (2010). Predation on toxic cane toads (Bufo marinus) may imperil bluetongue lizards (Tiliqua scincoides intermedia, Scincidae) in tropical Australia. Wildlife Research 37, 166–173.
| Predation on toxic cane toads (Bufo marinus) may imperil bluetongue lizards (Tiliqua scincoides intermedia, Scincidae) in tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Semeniuk, M., Lemckert, F., and Shine, R. (2007). Breeding-site selection by cane toads (Bufo marinus) and native frogs in northern New South Wales, Australia. Wildlife Research 34, 59–66.
| Breeding-site selection by cane toads (Bufo marinus) and native frogs in northern New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Somaweera, R., Webb, J. K., Brown, G. P., and Shine, R. (2011). Hatchling Australian freshwater crocodiles rapidly learn to avoid toxic invasive cane toads. Behaviour 148, 501–517.
| Hatchling Australian freshwater crocodiles rapidly learn to avoid toxic invasive cane toads.Crossref | GoogleScholarGoogle Scholar |
Strauss, S. Y., Lau, J. A., and Carroll, S. P. (2006). Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecology Letters 9, 357–374.
| Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities?Crossref | GoogleScholarGoogle Scholar |
Urban, M. C., Phillips, B. L., Skelly, D. K., and Shine, R. (2008). A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia. American Naturalist 171, E134–E148.
| A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia.Crossref | GoogleScholarGoogle Scholar |
Watson, M., and Woinarski, J. C. Z. (2004). Vertebrate monitoring and resampling in Kakadu National Park Year 3, 2003–2004. Tropical Savannas Cooperative Research Centre, Darwin.
Webb, J. K., Brown, G. P., Child, T., Greenlees, M. J., Phillips, B. L., and Shine, R. (2008). A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader. Austral Ecology 33, 821–829.
| A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader.Crossref | GoogleScholarGoogle Scholar |
Webb, J. K., Pearson, D., and Shine, R. (2011). A small dasyurid predator (Sminthopsis virginiae) rapidly learns to avoid a toxic invader. Wildlife Research 38, 726–731.
| A small dasyurid predator (Sminthopsis virginiae) rapidly learns to avoid a toxic invader.Crossref | GoogleScholarGoogle Scholar |
Woinarski, J. C. Z., Milne, D. J., and Wanganeen, G. (2001). Changes in mammal populations in relatively intact landscapes of Kakadu National Park, Northern Territory, Australia. Austral Ecology 26, 360–370.
| Changes in mammal populations in relatively intact landscapes of Kakadu National Park, Northern Territory, Australia.Crossref | GoogleScholarGoogle Scholar |
Woinarski, J. C. Z., Watson, M., and Gambold, N. (2003). Vertebrate monitoring and re-sampling in Kakadu National Park, 2002. Tropical Savannas Cooperative Research Centre, Darwin.
Woinarski, J. C. Z., Oakwood, M., Winter, J., Burnett, S., Milne, D., Foster, P., Myles, H., and Holmes, B. (2008). Surviving the toads: patterns of persistence of the northern quoll Dasyurus hallucatus in Queensland. Report to The Australian Government’s Natural Heritage Trust.
Woinarski, J. C. Z., Armstrong, M., Brennan, K., Fisher, A., Griffiths, A. D., Hill, B., Milne, D. J., Palmer, C., Ward, S., Watson, M., Winderlich, S., and Young, S. (2010). Monitoring indicates rapid and severe decline of native small mammals in Kakadu National Park, northern Australia. Wildlife Research 37, 116–126.
| Monitoring indicates rapid and severe decline of native small mammals in Kakadu National Park, northern Australia.Crossref | GoogleScholarGoogle Scholar |
