Avoiding the last supper: parentage analysis indicates multi-generational survival of re-introduced ‘toad-smart’ lineage

Abstract

Invasive species are a leading cause of animal extinctions. It is difficult to eradicate established and widespread populations of invaders, so we need novel approaches to reduce their impact on imperilled wildlife. In Australia, the toxic cane toad Rhinella marina has caused local extinctions of northern quolls Dasyurus hallucatus. Quolls lack immunity to toad toxins, and die after attacking adult toads. Using a novel approach, we modified quoll behaviour by feeding them small, non-lethal toads laced with a nausea-inducing chemical. Quolls that consumed the baits became ill, and subsequently ignored toads. We reintroduced these ‘toad-smart’ quolls to Kakadu National Park to determine whether aversion training could be an effective conservation tool. To measure the success of our innovation, it was important that reintroduced quolls survived to reproduce in a toad-infested landscape. We used parentage analysis to confirm the maternity of 12 wild-born quolls. ‘Toad-smart’ female quolls not only survived to reproduce, but their children and grandchildren survived as well. Training a single cohort of quolls yielded a long-term conservation benefit, without requiring continued conservation effort or eradication of the toxic invader.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Begg RJ (1981) The small mammals of Little Nourlangie Rock, N. T. III. Ecology of Dasyurus hallucatus, the Northern Quoll (Marsupialia: Dasyuridae). Aust Wildl Res 8:73–85. doi:10.1071/WR9810073

    Article  Google Scholar 

  2. Braithwaite RW, Griffiths AD (1994) Demographic variation and range contraction in the northern quoll, Dasyurus hallucatus (Marsupialia : Dasyuridae). Wildl Res 21:203–217. doi:10.1071/WR9940203

    Article  Google Scholar 

  3. Bryant SL (1988) Seasonal breeding in the Eastern quoll Dasyurus viverrinus (Marsupialia: Dasyuridae). University of Tasmania, Hobart

    Google Scholar 

  4. Burnett S (1997) Colonizing cane toads cause population declines in native predators: Reliable anecdotal information and management implications. Pac Conserv Biol 3:65–72. doi:10.1071/PC970065

    Article  Google Scholar 

  5. Caro TM, Hauser MD (1992) Is there teaching in nonhuman animals. Q Rev Biol 67:151–174. doi:10.1086/417553

    CAS  Article  PubMed  Google Scholar 

  6. Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110. doi:10.1016/j.tree.2005.01.003

    Article  PubMed  Google Scholar 

  7. Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

    Google Scholar 

  8. Dickman CR, Doncaster CP (1984) Responses of small mammals to red fox (Vulpes vulpes) odour. J Zool 204:521–531

    Article  Google Scholar 

  9. Francis DD, Szegda K, Campbell G, Martin WD, Insel TR (2003) Epigenetic sources of behavioral differences in mice. Nat Neurosci 6:445–446. doi:10.1038/nn1038

    CAS  PubMed  Google Scholar 

  10. Galef BG, Giraldeau LA (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav 61:3–15. doi:10.1006/anbe.2000.1557

    Article  PubMed  Google Scholar 

  11. Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140. doi:10.3758/BF03196014

    CAS  Article  PubMed  Google Scholar 

  12. Jones PC, King RB, Stanford KM, Lawson TD, Thomas M (2009) Frequent consumption and rapid digestion of prey by the Lake Erie watersnake with implications for an invasive prey species. Copeia:437–445. doi:10.1643/ch-08-119

    Google Scholar 

  13. Kalinowski ST (2006) hw-quickcheck: an easy-to-use computer program for checking genotypes for agreement with Hardy–Weinberg expectations. Mol Ecol Notes 6:974–979

    Article  Google Scholar 

  14. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. doi:10.1111/j.1365-294x.2007.03089.x

    Article  PubMed  Google Scholar 

  15. Kearney M, Phillips BL, Tracy CR, Christian KA, Betts G, Porter WP (2008) Modelling species distributions without using species distributions: the cane toad in Australia under current and future climates. Ecography 31:423–434. doi:10.1111/j.2008.0906-7590-05457.x

    Article  Google Scholar 

  16. Krutzen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB (2005) Cultural transmission of tool use in bottlenose dolphins. Proc Natl Acad Sci USA 102:8939–8943. doi:10.1073/pnas.0500232102

    Article  PubMed  PubMed Central  Google Scholar 

  17. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655. doi:10.1046/j.1365-294x.1998.00374.x

    CAS  Article  PubMed  Google Scholar 

  18. Mirza SN, Provenza FD (1990) Preference of the mother affects selection and avoidance of foods by lambs differing in age. Appl Anim Behav Sci 28:255–263. doi:10.1016/0168-1591(90)90104-l

    Article  Google Scholar 

  19. Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320. doi:10.1016/s0169-5347(00)01914-5

    CAS  Article  PubMed  Google Scholar 

  20. O’Donnell S, Webb JK, Shine R (2010) Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader. J Appl Ecol 47:558–565. doi:10.1111/j.1365-2664.2010.01802.x

    Article  Google Scholar 

  21. Oakwood M, Foster P (2008) Monitoring extinction of the northern quoll. Aust Acad Sci Newsl 71:6

    Google Scholar 

  22. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Rankmore BR et al. (2008) Island translocation of the northern quoll Dasyurus hallucatus as a conservation response to the spread of the cane toad Chaunus [Bufo] marinus in the Northern Territory. The Australian Government’s Natural Heritage Trust, Australia

    Google Scholar 

  24. Slate J, Marshall TC, Pemberton JM (2000) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9:801–808. doi:10.1046/j.1365-294x.2000.00930.x

    CAS  Article  PubMed  Google Scholar 

  25. Soderquist TR, Serena M (2000) Juvenile behaviour and dispersal of chuditch (Dasyurus geoffroii) (Marsupialia : Dasyuridae). Aust J Zool 48:551–560. doi:10.1071/ZO00029

    Article  Google Scholar 

  26. Spencer P, Cardoso M, How RA, Williams J, Bunce M, Schmitt LH (2007) Cross-species amplification at microsatellite loci in Australian quolls including the description of five new markers from the Chuditch (Dasyurus geoffroii). Mol Ecol Notes 7:1100–1103. doi:10.1111/j.1471-8286.2007.01791.x

    CAS  Article  Google Scholar 

  27. Webb JK, Brown GP, Child T, Greenlees MJ, Phillips BL, Shine R (2008) A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader. Austral Ecol 33:821–829. doi:10.1111/j.1442-9993.2008.01847.x

    Article  Google Scholar 

  28. Webb J, Legge S, Tuft K, Cremona T, Austin C (2015) Can we mitigate cane toad impacts on northern quolls. Final report National Environmental Research Program. Northern Australia Hub Charles Darwin University, Darwin

    Google Scholar 

  29. Woinarski JCZ et al. (2011) The disappearing mammal fauna of northern Australia: context, cause, and response. Conserv Lett 4:192–201. doi:10.1111/j.1755-263X.2011.00164.x

    Article  Google Scholar 

Download references

Acknowledgements

We thank Damien Stanioch, Lynda Veyret, Dion Wedd, and the Territory Wildlife Park staff for raising quolls, training, and assistance in the field. We thank Stephanie O’Donnell for assisting with quoll training and the reintroduction to the field site. We particularly thank the Traditional Owners for supporting the project and allowing us to work in the East Alligator region. We are indebted to the Kakadu Rangers, trainees, and all the volunteers, especially Libby Dwyer, Belinda McCarthy, Sandra Riemer, and Tim Dempster, who provided assistance in the field. We thank Steve Winderlich, Anne O’Dea, Greg Sattler, Matthew Dunn, and Patrick Shaughnessy for advice and logistical support. We would also like to acknowledge the technical assistance of Mia Hillyer and the WA Department of Parks and Wildlife for processing of DNA samples. Financial assistance was kindly provided by the Federal Government’s Caring for Our Country grant scheme, the Australian Research Council, the Mazda Foundation, and the National Geographic Conservation Trust. We thank two anonymous reviewers for their constructive feedback on an earlier draft of the manuscript, and the Flora and Fauna Division of the NT Department of Environment and Natural Resources for allowing us to use the image of the northern quoll.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Teigan Cremona.

Ethics declarations

Ethical approval

The study was conducted within Kakadu National Park in accordance with The Australian Code of Practice for the Care and Use of Animals for Scientific Purposes (1997). The area is jointly managed by traditional land-owners and the Australian federal government. Permission to undertake the study was obtained through Kakadu National Park (Permit Number: RK844). The research was approved by the University of Sydney Animal Ethics Committee (Protocol L04/7-2008/3/4823) and the University of Technology Sydney Animal Care and Ethics Committee (Protocol 2012-082A).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cremona, T., Spencer, P., Shine, R. et al. Avoiding the last supper: parentage analysis indicates multi-generational survival of re-introduced ‘toad-smart’ lineage. Conserv Genet 18, 1475–1480 (2017). https://doi.org/10.1007/s10592-017-0973-3

Download citation

Keywords

  • Maternity
  • Conditioned taste aversion
  • Reintroduction
  • Marsupial
  • Invasive