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RESEARCH ARTICLE
Contents Vol 37(2)

Predation on toxic cane toads (Bufo marinus) may imperil bluetongue lizards (Tiliqua scincoides intermedia, Scincidae) in tropical Australia

Samantha J. Price-Rees A , Gregory P. Brown A and Richard Shine A B
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- Author Affiliations

A School of Biological Sciences A08, University of Sydney, NSW 2006, Australia.

B Corresponding author. Email: rick.shine@sydney.edu.au

Wildlife Research 37(2) 166-173 https://doi.org/10.1071/WR09170
Submitted: 4 December 2009  Accepted: 8 February 2010   Published: 16 April 2010

Abstract

Context. Detecting ecological impacts of invasive species can be extremely difficult. Even major population declines may be undetectable without extensive long-term data if the affected taxon is rare and/or difficult to census, and exhibits stochastic variation in abundance as a result of other factors. Our data suggest such a situation in an iconic Australian reptile species, the bluetongue lizard. Originally restricted to Central and South America, cane toads (Bufo marinus) are rapidly spreading through tropical Australia. Most native predators have no evolutionary history of exposure to the toads’ distinctive chemical defences (bufadienolides), and many varanid lizards, elapid snakes, crocodiles and marsupials have been killed when they have attempted to consume toads.

Aims. Scincid lizards have not been considered vulnerable to toad invasion; however, one lineage (the bluetongues, genus Tiliqua) consists of large omnivores that may be affected. Our field and laboratory research aimed to elucidate this concern.

Methods. Nightly surveys for bluetongue lizards (Tiliqua scincoides intermedia) and cane toads were conducted along two adjacent roadways on the Adelaide River floodplain of the Northern Territory. Scent discrimination trials in the laboratory assessed lizard responses to chemical cues from three food types (native frogs, cane toads and ‘preferred foods’) by counting tongue-flicks and biting elicited by cotton swabs. A subset of lizards was presented with live toads.

Key results. Numbers of bluetongues encountered during standardised field surveys in the Darwin region declined soon after toads arrived, and we have not recorded a single lizard for the last 20 months. In the laboratory, foraging responses of bluetongues were as intense to cane-toad scent as to the scent of native frogs, and many of the lizards we tested attempted to consume toads, and were poisoned as a result.

Conclusions and implications. The population decline of bluetongues in this region appears to have been the direct result of fatal ingestion of toxic cane toads. Our studies thus add a scincid lizard species to the list of native Australian predators imperilled by cane-toad invasion, and point to the difficulty of detecting invader impact even for an iconic species in a system subject to detailed survey work.

Additional keywords: ecological impact, invasive species, Rhinella marina, Tiliqua intermedia, toxicity.


Acknowledgements

We thank Michelle Franklin and Nilusha Somaweera for assistance with animal husbandry and carrying out experimental procedures, Matthew Greenlees for advice on experimental design, Melanie Elphick and Christa Beckmann for assistance with preparing figures, John Weigel and Robert Coward (Exotic Pets, Darwin) for lizards. David Pearson and Jonathan Webb kindly allowed us to cite unpublished results of other studies. The work was funded by the Australian Research Council.


References

Box, G. E. P. , and Tiao, G. C. (1975). Intervention analysis with application to economic and environmental problems. Journal of the American Statistical Association 70, 70–92.
| Crossref | GoogleScholarGoogle Scholar | Burghardt G. M. (1970). Chemical perception in reptiles. In ‘Communication by Chemical Signals’. (Eds J. W. Johnston, D. G. Moulton and A. Turk.) pp. 241–308. (Appleton-Century-Crofts: New York.)

Burnett, S. (1997). Colonising cane toads cause population declines in native predators: reliable anecdotal information and management implications. Pacific Conservation Biology 3, 65–72.
Caldow R. W. G. , Stillman R. A. , le V. dit Durell S. E. A. , West A. D. , McGrorty S. , Goss-Custard J. D. , Wood P. J. , and Humphreys J. (2007). Benefits to shorebirds from invasion of a non-native shellfish. Proceedings of the Royal Society B 274 1449 1455

Carpenter, C. C. , and Murphy, J. B. (1978). Tongue display by the common bluetongue (Tiliqua scincoides) Reptilia, Lacertilia, Scincidae. Journal of Herpetology 12, 428–429.
| Crossref | GoogleScholarGoogle Scholar | Cogger H. G. (2000). ‘Reptiles and Amphibians of Australia.’ 6th edn. (Reed New Holland: Sydney.)

Cooper, W. E. (1994). Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. Journal of Chemical Ecology 20, 439–487.
| Crossref | GoogleScholarGoogle Scholar | CAS | Evans S. (1999). Fisheries issues in the Borroloola region. In ‘Wise Use of Wetlands in Northern Australia: Indigenous Use’. (Eds P. Whitehead, M. Storrs, M. McKaige, R. Kennett and M. Douglas.) p. 16. (Centre for Tropical Wetlands Management and Centre for Indigenous Natural and Cultural Resource Management, Northern Territory University: Darwin.)

Fenner, A. L. , and Bull, C. M. (2009). Tiliqua adelaidensis (pygmy bluetongue lizard) mating behaviour. Herpetological Review 40, 91–92.
Greer A. E. (1989). ‘Biology and Evolution of Australian Lizards.’ (Surrey Beatty: Sydney.)

Griffiths, A. D. , and McKay, J. L. (2007). Cane toads reduce the abundance and site occupancy of freshwater goannas Varanus mertensi. Wildlife Research 34, 609–615.
Lever C. (2001). ‘The Cane Toad. The History and Ecology of a Successful Colonist.’ (Westbury Academic Publishing: Otley, West Yorkshire.)

Mack, R. N. , Simberloff, D. , Lonsdale, W. M. , Evans, H. , Clout, M. , and Bazzaz, E. (2000). Biotic invasions: causes, epidemiology, global consequences and control. Issues in Ecology 5, 1–20.
O’Donnell S. (2009). Alien versus predator: taste aversion learning as a way of enhancing survival in northern quolls (Dasyurus hallucatus). B.Sc.(Honours) Thesis, University of Sydney.

Oakwood, M. (2004a). Case of the disappearing spots. Nature Australia 28, 26–35.
Oakwood M. (2004 b). The effect of cane toads on a marsupial carnivore, the northern quoll, Dasyurus hallucatus. Unpublished Report to Parks Australia North, Darwin.

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.
| Crossref | GoogleScholarGoogle Scholar | Rasmussen P. W. , Heisey D. M. , Nordheim E. V. , and Frost T. M. (2001). Time-series analysis: unreplicated large-scale experiments. In ‘Design and Analysis of Ecological Experiments’. (Eds S. M. Scheiner and J. Gurevitch.) pp. 138–158. (Oxford University Press: New York.)

Shardell, M. , Harris, A. D. , El-Kamary, S. S. , Furuno, J. P. , Miller, R. R. , and Perencevich, E. N. (2007). Statistical analysis and application of quasi-experiments to antimicrobial resistance intervention studies. Clinical Infectious Diseases 45, 901–907.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Shea G. (1992). The systematics and reproduction of bluetongue lizards of the genus Tiliqua (Squamata: Scincidae). Ph.D. Thesis, University of Sydney.

Shea, G. (1998). Australian bluetongues. Nature Australia 26, 31–39.
Tabachnick B. G. , and Fidell L. S. (2007). ‘Using Multivariate Statistics.’ 5th edn. (Allyn and Bacon: Boston, MA.)

Taylor R. , and Edwards G. (2005). A review of the impact and control of cane toads in Australia with recommendations for future research and management approaches. A Report to the Vertebrate Pests Committee from the National Cane Toad Taskforce. Pest Animal Control CRC, Canberra.

Townsend, C. R. (2003). Individual, population, community, and ecosystem consequences of a fish invader in New Zealand streams. Conservation Biology 17, 38–47.
| Crossref | GoogleScholarGoogle Scholar | Turner G. (2001). ‘Keeping Bluetongue Lizards.’ (Australian Reptile Keeper Publications: Melbourne.)

Ujvari, B. , and Madsen, T. (2009). Increased mortality of naïve varanid lizards after the invasion of non-native cane toads (Bufo marinus). Herpetological Conservation Biology 4, 248–251.
van Dam R. A. , Walden D. J. , and Begg G. W. (2002). A preliminary risk assessment for cane toads in Kakadu National Park. Environmental Research Institute of the Supervising Scientist, Jabiru, NT.

Watson M. , and Woinarski J. (2003). A preliminary assessment of impacts of cane toads on terrestrial vertebrate fauna in Kakadu National Park. Unpublished Report February 2003. Kakadu Research Advisory Committee, Jabiru, NT.

Webb J. K. , and Glanznig A. (2004). Predation, competition and lethal toxic ingestion caused by cane toads (Bufo marinus). Key Threatening Process Nomination to Commonwealth Government, WWF Australia.

Webb, J. K. , Shine, R. , and Christian, K. A. (2005). Does intraspecific niche partitioning in a native predator influence its response to an invasion by a toxic prey species? Austral Ecology 30, 201–209.
| Crossref | GoogleScholarGoogle Scholar | Weigel J. (1988). ‘Care of Australian Reptiles in Captivity.’ (Reptile Keepers Association: Gosford, NSW.)

Woinarski, J. C. Z. , Armstrong, A. , Price, O. , McCartney, J. , Griffiths, A. D. , and Fisher, A. (2004). The terrestrial vertebrate fauna of Litchfield National Park, Northern Territory: monitoring over a 6-year period and response to fire history. Wildlife Research 31, 587–596.
| Crossref | GoogleScholarGoogle Scholar | Yaffee R. A. , and McGee M. (2000). ‘Introduction to Time Series Analysis and Forecasting.’ (Academic Press: New York.)

Yeatman E. M. (1988). Resource partitioning by three congeneric species of skink (Tiliqua) in sympatry in South Australia. Ph.D. Thesis, Flinders University, Adelaide.

Zug, G. R. , and Zug, P. B. (1979). The marine toad, Bufo marinus: a natural history resumé of native populations. Smithsonian Contributions to Zoology 284, 1–54.