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Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Paradoxical population resilience of a keystone predator to a toxic invasive species

J. Sean Doody https://orcid.org/0000-0002-9023-6206 A B E , David Rhind C and Simon Clulow B D
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, University of South Florida – St Petersburg, FL 33701, USA.

B School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia.

C School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

D Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.

E Corresponding author. Email: jseandoody@gmail.com

Wildlife Research 47(3) 260-266 https://doi.org/10.1071/WR19150
Submitted: 24 August 2019  Accepted: 23 November 2019   Published: 13 May 2020

Abstract

Context: The invasive cane toad (Rhinella marina) has decimated populations of a keystone predator, the yellow-spotted monitor (Varanus panoptes), causing trophic cascades in Australian animal communities. Paradoxically, some V. panoptes populations coexist with toads. Demonstrating patterns in heterogeneous population-level impacts could reveal mechanisms that mediate individual effects, and provide managers with the ability to predict future impacts and assist in population recovery.

Aims: The aim of the present study was to search for spatial patterns of population resilience of V. panoptes to invasive cane toads.

Methods: Published literature, unpublished data, reports and anecdotal information from trained herpetologists were used to test the emerging hypothesis that resilient predator populations are mainly coastal, whereas non-resilient populations are mostly inland.

Key results: Post-toad invasion data from 23 V. panoptes populations supported the idea that toad impacts on V. panoptes were heterogeneous; roughly half the populations could be designated as resilient (n = 13) and half as non-resilient (n = 10). Resilient populations had longer times since toad invasion than did non-resilient populations (39 versus 9 years respectively), supporting the idea that some recovery can occur. Non-resilient populations were exclusively inland (n = 10), whereas resilient populations were split between inland (n = 5) and coastal (n = 8) populations. Resilient inland populations, however, were mainly confined to areas in which decades had passed since toad invasion.

Conclusions: The findings suggest that coastal V. panoptes populations fare much better than inland populations when it comes to surviving invading cane toads.

Implications: Unambiguous recovery of monitor populations remains undemonstrated and will require long-term population monitoring before and after toad invasion.

Additional keywords: abundance, behaviour, ecology, invasive species, pest management.


References

Blamires, S. J. (2004). Habitat preferences of coastal goannas (Varanus panoptes): are they exploiters of sea turtle nests at Fog Bay, Australia? Copeia 2004, 370–377.
Habitat preferences of coastal goannas (Varanus panoptes): are they exploiters of sea turtle nests at Fog Bay, Australia?Crossref | GoogleScholarGoogle Scholar |

Britton, A. R., Britton, E. K., and McMahon, C. R. (2013). Impact of a toxic invasive species on freshwater crocodile (Crocodylus johnstoni) populations in upstream escarpments. Wildlife Research 40, 312–317.
Impact of a toxic invasive species on freshwater crocodile (Crocodylus johnstoni) populations in upstream escarpments.Crossref | GoogleScholarGoogle Scholar |

Cameron, E. E., and Cogger, H. G. (Eds) (1992). ‘The Herpetofauna of the Weipa region, Cape York Peninsula.’ (Australian Museum: Sydney.)

Catling, P., Hertog, A., Burt, R., Wombey, J. C., and Forrester, R. I. (1999). The short-term effect of cane toads (Bufo marinus) on native fauna in the Gulf Country of the Northern Territory. Wildlife Research 26, 161–185.
The short-term effect of cane toads (Bufo marinus) on native fauna in the Gulf Country of the Northern Territory.Crossref | GoogleScholarGoogle Scholar |

Christian, K. A., Corbett, L., Green, B., and Weavers, B. W. (1995). Seasonal activity and energetics of two species of varanid lizards in tropical Australia. Oecologia 103, 349–357.
Seasonal activity and energetics of two species of varanid lizards in tropical Australia.Crossref | GoogleScholarGoogle Scholar | 28306829PubMed |

Clulow, J., and Clulow, S. (2016). Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed. Reproduction, Fertility and Development 28, 1116–1132.
Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed.Crossref | GoogleScholarGoogle Scholar |

Clulow, J., Pomering, M., Herbert, D., Uptin, R., Calatayud, N., Clulow, S., Mahony, M. J., and Trudeau, V. L. (2018). Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review. General and Comparative Endocrinology 265, 141–148.
Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review.Crossref | GoogleScholarGoogle Scholar | 29859744PubMed |

De Lisle, H. F. (2008). Ritual combat in Varanus panoptes panoptes. Biawak 2, 152–159.

Cogger, H. (2014). ‘Reptiles and Amphibians of Australia.’ (CSIRO Publishing: Melbourne.)

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 insculpta). Wildlife Research 33, 349–354.
Indirect impacts of invasive cane toads (Bufo marinus) on nest predation in pig-nosed turtles (Carettochelys insculpta).Crossref | GoogleScholarGoogle Scholar |

Doody, J. S., Green, B., Rhind, D., Castellano, C., 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 |

Doody, J. S., Castellano, C., Rhind, D., and Green, B. (2013). Indirect facilitation of a native mesopredator by an invasive species: are cane toads re-shaping tropical riparian communities? Biological Invasions 15, 559–568.
Indirect facilitation of a native mesopredator by an invasive species: are cane toads re-shaping tropical riparian communities?Crossref | GoogleScholarGoogle Scholar |

Doody, J. S., Mayes, P., Clulow, S., Rhind, D., Green, B., Castellano, C., D’Amore, D., and Mchenry, C. (2014). Impacts of the invasive cane toad on aquatic reptiles in a highly modified ecosystem: the importance of replicating impact studies. Biological Invasions 16, 2303–2309.
Impacts of the invasive cane toad on aquatic reptiles in a highly modified ecosystem: the importance of replicating impact studies.Crossref | GoogleScholarGoogle Scholar |

Doody, J. S., Clulow, S., Kay, G., D’Amore, D., Rhind, D., Wilson, S., Ellis, R., Castellano, C., McHenry, C. M., Qayle, M., Hands, K., Saywer, G., and Bass, M. (2015). The dry season shuffle: gorges provide refugia for animal communities in tropical savannah ecosystems. PLoS One 10, e0131186.
The dry season shuffle: gorges provide refugia for animal communities in tropical savannah ecosystems.Crossref | GoogleScholarGoogle Scholar | 26135472PubMed |

Doody, J. S., Rhind, D., Green, B., Castellano, C., McHenry, C., and Clulow, S. (2017). Chronic effects of an invasive species on an animal community. Ecology 98, 2093–2101.
Chronic effects of an invasive species on an animal community.Crossref | GoogleScholarGoogle Scholar | 28477376PubMed |

Else, P. L. (1994). Plasma potassium may protect sodium pumps of toad hearts from an endogenous inhibitor. American Journal of Physiology 267, 754–761.

Frankham, R. (2010). Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143, 1919–1927.
Challenges and opportunities of genetic approaches to biological conservation.Crossref | GoogleScholarGoogle Scholar |

Freeland, W. J., and Martin, K. C. (1985). The rate of range expansion by Bufo marinus in Northern Australia, 1980–84. Wildlife Research 12, 555–559.
The rate of range expansion by Bufo marinus in Northern Australia, 1980–84.Crossref | GoogleScholarGoogle Scholar |

Griffiths, A. D., and Holland, D. C. (2004). Impacts of the exotic cane toad (Bufo marinus) on the survival of lowland Varanas species in Kakadu National Park. Report to Kakadu National Park. Charles Darwin University, Darwin, NT, Australia.

Jolly, C. J., Shine, R., and Greenlees, M. J. (2015). The impact of invasive cane toads on native wildlife in southern Australia. Ecology and Evolution 5, 3879–3894.
The impact of invasive cane toads on native wildlife in southern Australia.Crossref | GoogleScholarGoogle Scholar | 26445649PubMed |

Jolly, C. J., Shine, R., and Greenlees, M. J. (2016). The impacts of a toxic invasive prey species (the cane toad, Rhinella marina) on a vulnerable predator (the lace monitor, Varanus varius). Biological Invasions 18, 1499–1509.
The impacts of a toxic invasive prey species (the cane toad, Rhinella marina) on a vulnerable predator (the lace monitor, Varanus varius).Crossref | GoogleScholarGoogle Scholar |

Kolbe, J. J., Kearney, M., and Shine, R. (2010). Modeling the consequences of thermal trait variation for the cane toad invasion of Australia. Ecological Applications 20, 2273–2285.
Modeling the consequences of thermal trait variation for the cane toad invasion of Australia.Crossref | GoogleScholarGoogle Scholar | 21265457PubMed |

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 |

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

Madsen, T., Shine, R., Olsson, M., and Wittzell, H. (1999). Conservation biology: restoration of an inbred adder population. Nature 402, 34–35.
Conservation biology: restoration of an inbred adder population.Crossref | GoogleScholarGoogle Scholar |

Mehta, S. V., Haight, R. G., Homans, F. R., Polasky, S., and Venette, R. (2007). Optimal detection and control strategies for invasive species management. Ecological Economics 61, 237–245.
Optimal detection and control strategies for invasive species management.Crossref | GoogleScholarGoogle Scholar |

Menke, S. B., Ward, P. S., and Holway, D. A. (2018). Long‐term record of Argentine ant invasions reveals enduring ecological impacts. Ecology 99, 1194–1202.
Long‐term record of Argentine ant invasions reveals enduring ecological impacts.Crossref | GoogleScholarGoogle Scholar | 29504667PubMed |

Mooney, H. A., and Hobbs, R. J. (2000). ‘Invasive Species in a Changing World.’ (Island Press: Washington, DC.)

Phillips, B. L., Brown, G. P., Webb, J. K., and Shine, R. (2006). Invasion and the evolution of speed in toads. Nature 439, 803.
Invasion and the evolution of speed in toads.Crossref | GoogleScholarGoogle Scholar | 16482148PubMed |

Phillips, B. L., Brown, G. P., and Greenlees, M. (2007). Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecology 32, 169–176.
Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia.Crossref | GoogleScholarGoogle Scholar |

Pinch, K., Madsen, T., and Ujvari, B. (2017). No signs of Na+/K+-ATPase adaptations to an invasive exotic toxic prey in native squamate predators. Austral Ecology 42, 929–933.

Ruiz, G. M., and Carlton, J. T. (2003). ‘Invasion Vectors: A Conceptual Framework for Management.’ (Island Press: Washington, DC.)

Sabath, M. D., Boughton, W. C., and Easteal, S. (1981). Expansion of the range of the introduced toad Bufo marinus in Australia 1935–1974. Copeia 1981, 676–680.
Expansion of the range of the introduced toad Bufo marinus in Australia 1935–1974.Crossref | GoogleScholarGoogle Scholar |

Shine, R. (1986). Food habits, habitats and reproductive biology of four sympatric species of varanid lizards in tropical Australia. Herpetologica 42, 346–360.

Shine, R. (2010). The ecological impact of invasive cane toads (Bufo marinus) in Australia. The Quarterly Review of Biology 85, 253–291.
The ecological impact of invasive cane toads (Bufo marinus) in Australia.Crossref | GoogleScholarGoogle Scholar | 20919631PubMed |

Simberloff, D., and Von Holle, B. (1999). Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1, 21–32.
Positive interactions of nonindigenous species: invasional meltdown?Crossref | GoogleScholarGoogle Scholar |

Simberloff, D., Martin, J.-L., Genovesi, P., Maris, V., Wardle, D., Aronson, J., Courchamp, F., Galil, B., Garcia-Berthou, E., Pascal, M., Pysek, P., Sousa, R., Tabacchi, E., and Vila, M. (2013). Impacts of biological invasions: what’s what and the way forward. Trends in Ecology & Evolution 28, 58–66.
Impacts of biological invasions: what’s what and the way forward.Crossref | GoogleScholarGoogle Scholar |

Somaweera, R., and Shine, R. (2012). The (non) impact of invasive cane toads on freshwater crocodiles at Lake Argyle in tropical Australia. Animal Conservation 15, 152–163.
The (non) impact of invasive cane toads on freshwater crocodiles at Lake Argyle in tropical Australia.Crossref | GoogleScholarGoogle Scholar |

Somaweera, R., Shine, R., Webb, J., Dempster, T., and Letnic, M. (2013). Why does vulnerability to toxic invasive cane toads vary among populations of Australian freshwater crocodiles? Animal Conservation 16, 86–96.
Why does vulnerability to toxic invasive cane toads vary among populations of Australian freshwater crocodiles?Crossref | GoogleScholarGoogle Scholar |

Sutherst, R. W., Floyd, R. B., and Maywald, G. F. (1996). The potential geographical distribution of the cane toad, Bufo marinus in Australia. Conservation Biology 10, 294–299.
The potential geographical distribution of the cane toad, Bufo marinus in Australia.Crossref | GoogleScholarGoogle Scholar |

Tingley, R., Ward-Fear, G., Schwarzkopf, L., Greenlees, M. J., Phillips, B. L., Brown, G., Clulow, S., Webb, G., Capon, R., Sheppard, A., Strive, T., Tizard, M., and Shine, R. (2017). New weapons in the Toad Toolkit: a review of methods to control and mitigate the biodiversity impacts of invasive cane toads (Rhinella marina). The Quarterly Review of Biology 92, 123–149.
New weapons in the Toad Toolkit: a review of methods to control and mitigate the biodiversity impacts of invasive cane toads (Rhinella marina).Crossref | GoogleScholarGoogle Scholar | 29562120PubMed |

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

Urban, M., Phillips, B. L., Skelly, D. K., and Shine, R. (2007). The cane toad’s (Chaunus marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings. Biological Sciences 274, 1413–1419.
The cane toad’s (Chaunus marinus) increasing ability to invade Australia is revealed by a dynamically updated range model.Crossref | GoogleScholarGoogle Scholar | 17389221PubMed |

Wardle, D. A., Bellingham, P. J., Fukami, T., and Bonner, K. (2012). Soil-mediated indirect impacts of an invasive predator on plant growth. Biology Letters 8, 574–577.
Soil-mediated indirect impacts of an invasive predator on plant growth.Crossref | GoogleScholarGoogle Scholar | 22496079PubMed |

Webb, G. J., and Manolis, S. C. (2010). Australian freshwater crocodile Crocodylus johnstoni. In ‘Crocodiles. Status Survey and Conservation Action Plan.’ (Eds S. C. Manolis, and C. Stevenson.) pp. 66–70. (Wildlife Management International: Darwin.)

Whiteley, A. R., Fitzpatrick, S. W., Funk, W. C., and Tallmon, D. (2015). Genetic rescue to the rescue. Trends in Ecology & Evolution 30, 42–49.
Genetic rescue to the rescue.Crossref | GoogleScholarGoogle Scholar |

Woinarski, J., 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 |