Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Queensland northern quolls are not immune to cane toad toxin

Beata Ujvari A , Meri Oakwood B and Thomas Madsen C D E
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Science, University of Sydney, NSW 2006, Australia.

B Envirotek Ecological Services, PO Box 4022, Coffs Harbour Jetty, NSW 2450, Australia.

C School of Molecular and Microbial Biosciences, University of Sydney, NSW 2006, Australia.

D School of Biological Sciences, University of Wollongong, NSW 2522, Australia.

E Corresponding author. Email: madsen@uow.edu.au

Wildlife Research 40(3) 228-231 https://doi.org/10.1071/WR13011
Submitted: 17 January 2013  Accepted: 3 April 2013   Published: 24 April 2013

Abstract

Context: The release of the highly toxic South American cane toad (Bufo marinus) to the toad-free Australian continent in 1935, and their subsequent rapid spread over large areas of tropical Australia, has resulted in a massive decline of predators such as yellow-spotted goannas (Varanus panoptes) and northern quolls (Dasyurus hallucatus). In spite of dramatic declines of northern quoll populations in the Northern Territory, a few populations still persist in areas of Queensland where northern quolls have co-existed with toads for several decades.

Aims: To determine whether the remaining quoll populations in Queensland have evolved resistance to cane toad toxins.

Methods: The extracellular H1–H2 domain of the α1 subunit of the sodium–potassium-ATPase gene was sequenced in four Queensland as well as four Northern Territory quolls. The transcribed sodium–potassium-ATPase enzyme from this gene is specifically targeted by toad toxins.

Key results: In all of the eight quolls, the sequences representing the 36 bp of the H1–H2 domain of the α1 subunit of the sodium–potassium-ATPase gene were identical.

Conclusions: Our results showed that Queensland quolls have not evolved an increased resistance to the toad toxins. We therefore suggest that the persistence of northern quolls in a few toad infested areas of Queensland could to be due to a combination of optimal habitat quality, and concomitant large quoll numbers, as well as an aversion to feeding on these highly toxic amphibians.

Implications: We suggest that a sample of northern quolls from the Queensland populations should be captured and their response, as well as that of their offspring and grand-offspring, to cane toads should be investigated to guide management of this declining species.


References

Aubret, F., Burghardt, G. M., Maumelat, S., Bonnet, X., and Bradshaw, D. (2006). Feeding preferences in two disjunct populations of tiger snakes, Notechis scutatus (Elapidae). Behavioral Ecology 17, 716–725.
Feeding preferences in two disjunct populations of tiger snakes, Notechis scutatus (Elapidae).Crossref | GoogleScholarGoogle Scholar |

Blumstein, D. T., and Daniel, J. C. (2005). The loss of anti-predator behaviour following isolation on islands. Proceedings. Biological Sciences 272, 1663–1668.
The loss of anti-predator behaviour following isolation on islands.Crossref | GoogleScholarGoogle Scholar |

Brown, G., Ujvari, B., Madsen, T., and Shine, R. (2013). Invader impact clarifies the roles of top-down and bottom-up effects on tropical snake populations. Functional Ecology , .
Invader impact clarifies the roles of top-down and bottom-up effects on tropical snake populations.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.

Doody, J. S., Green, B., Sims, R., Rhind, D., West, P., and Steer, D. (2006). Indirect impacts of invasive cane toads Bufo marinus on nest predation in pig-nosed turtles Carettochelys insulpta. Wildlife Research 33, 349–354.
Indirect impacts of invasive cane toads Bufo marinus on nest predation in pig-nosed turtles Carettochelys insulpta.Crossref | GoogleScholarGoogle Scholar |

Flannery, T. (1994). ‘The Future Eaters: an Ecological History of the Australasian Lands and People.’ (Reed New Holland: Sydney.)

Grant, P. (1998). ‘Evolution on Islands.’ (Oxford University Press: Oxford, UK.)

Hasenfuss, G., and Teerlink, J. R. (2011). Cardiac inotropes: current agents and future directions. European Heart Journal 32, 1838–1845.
Cardiac inotropes: current agents and future directions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVSiu7vJ&md5=84747d41acae4fbf1484529935adfb52CAS | 21388993PubMed |

Holzinger, F., Frick, C., and Wink, M. (1992). Molecular basis for the insensitivity of the monarch Danaus plexippus to cardiac glycosides. FEBS Letters 314, 477–480.
Molecular basis for the insensitivity of the monarch Danaus plexippus to cardiac glycosides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXns1Sltg%3D%3D&md5=16eb1e44c73f620c11cadb2e627996e1CAS | 1334851PubMed |

Jaisser, F., Canessa, C. M., Horisberger, J. D., and Rossier, B. C. (1992). Primary sequence and functional expression of a novel ouabain-resistant Na,K-ATPase. The Journal of Biological Chemistry 267, 16 895–16 903.
| 1:CAS:528:DyaK3sXkt1emtb4%3D&md5=6fbda4245c644ce32da93f4831b8f265CAS |

Lever, C. (2001). ‘The Cane Toad. The History and Ecology of a Successful Colonist.’ (Westbury Academic and Scientific Publishing: Otley, Yorkshire.)

Lingrel, J. B. (2010). The physiological significance of the cardiotonic steroid/ouabain-binding site of the Na,K-ATPase. Annual Review of Physiology 72, 395–412.
The physiological significance of the cardiotonic steroid/ouabain-binding site of the Na,K-ATPase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktFKktL8%3D&md5=080e0e66363e7add0c9d8db03cb3addbCAS | 20148682PubMed |

Losos, J. B., and Ricklefs, R. E. (2009). Adaptation and diversification on islands. Nature 457, 830–836.
Adaptation and diversification on islands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhslCnsbY%3D&md5=a2c09f240fc32a142942181de438b87dCAS | 19212401PubMed |

Low, T. (2001). ‘Feral Future. The Untold Story of Australia’s Exotic Invaders.’ (Penguin Books: Melbourne.)

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 |

Oakwood, M. (2002). Spatial and social organisation of a carnivorous marsupial Dasyurus hallucatus (Marsupialia: Dasyuridae). Journal of Zoology 257, 237–248.
Spatial and social organisation of a carnivorous marsupial Dasyurus hallucatus (Marsupialia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |

Oakwood, M. (2008). Monitoring extinction of the northern quoll. Report to the Australian Academy of Science, Canberra.

Pimm, S. L., Moulton, M. P., and Justice, L. J. (1994). Bird extinctions in the central Pacific. Philosophical Transactions of the Royal Society of London. B 344, 27–33.
Bird extinctions in the central Pacific.Crossref | GoogleScholarGoogle Scholar |

Price, E. M., Rice, D. A., and Lingrel, J. B. (1990). Structure-function studies of Na,K-ATPase. The Journal of Biological Chemistry 265, 6638–6641.
| 1:CAS:528:DyaK3cXkt1SjurY%3D&md5=2b3922f684fb1f18a31161f5ed2f0331CAS | 2157705PubMed |

Primack, R. B. (1995). ‘A Primer of Conservation Biology.’ (Sinauer Associates: Sunderland, MA)

Soderquist, T. R., and Serena, M. (1994). Dietary niche of the western quoll, Dasyurus geoffroii, in the jarrah forest of Western Australia. Australian Mammalogy 17, 133–136.

Ujvari, B., and Madsen, T. (2009). Increased mortality of naïve varanid lizards after the invasion of non-native cane toads Bufo marinus. Herpetological Conservation and Biology 4, 248–251.

Ujvari, B., Mun, H.-C., Conigrave, A. D., Bray, A., Osterkamp, J., Halling, P., and Madsen, T. (2013). Isolation breeds naivety: island living robs Australian varanid lizards of toad-toxin immunity via four-base-pair mutation. Evolution 67, 289–294.
Isolation breeds naivety: island living robs Australian varanid lizards of toad-toxin immunity via four-base-pair mutation.Crossref | GoogleScholarGoogle Scholar | 23289579PubMed |

Watson, M., and Woinarski, J. C. Z. (2004). Vertebrate monitoring and re-sampling in Kakadu National Park, Year 3, 2003–4. Report to Parks Australia. 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., Perason, 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 |

Wiles, G. J., Bart, J., Beck, R., and Agoun, C. F. (2003). Impacts of the brown tree snakes: patterns of decline and species persistence in Guam’s avifauna. Conservation Biology 17, 1350–1360.
Impacts of the brown tree snakes: patterns of decline and species persistence in Guam’s avifauna.Crossref | GoogleScholarGoogle Scholar |

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, March 2008.

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. Australian Wildlife Research 37, 116–126.
Monitoring indicates rapid and severe decline of native small mammals in Kakadu National Park, northern.Crossref | GoogleScholarGoogle Scholar |

Zentall, T., and Galef, B. G. (1988). ‘Social Learning, Psychological and Biological Perspectives.’ (Lawrence Erlbaum Asssociates: Hillsdale, NJ.)