Can conditioned taste aversion be deployed at a landscape level to mitigate the impact of invasive cane toads on northern quolls?
Naomi L. Indigo
A * , Ella Kelly B , James Smith C D , Jonathan K. Webb A and Ben L. Phillips B
+ Author Affiliations
- Author Affiliations
A School of Life Sciences, University of Technology Sydney, PO Box 123, Broadway, Sydney, NSW 2007, Australia.
B School of BioSciences, University of Melbourne, Parkville, Vic. 3010, Australia.
C Department of Environment and Water, Natural Resources Kangaroo Island, Kingscote, SA 5223, Australia.
D Australian Wildlife Conservancy, Mornington Wildlife Sanctuary, PMB 925, Derby, WA 6728, Australia.
Wildlife Research 50(12) 1046-1057 https://doi.org/10.1071/WR21151
Submitted: 8 September 2020 Accepted: 18 January 2023 Published: 20 February 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Animals can be taught new behaviours to mitigate threatening processes. However, it is yet to be confirmed if such teaching can be deployed in the field. Here we test this possibility using the invasion of cane toads because they are highly toxic novel prey items to many predators across northern Australia.
Aims: Research has shown that training predators to avoid toads, using conditioned taste aversion (CTA), significantly improves the survival rates of individuals. We sought to determine if deployment of CTA baits, in situ, could reduce cane toad impacts on a mammalian predator, the northern quoll (Dasyurus hallucatus).
Methods: The work was conducted in the Kimberley, Western Australia, where we treated three quoll populations with training baits from November 2015–November 2017, and kept four populations as controls. We used camera traps and Bayesian hierarchal modelling to estimate the population size of quolls on up to four occasions before, and two occasions after, cane toad arrival.
Key results: We observed a 65% reduction in quoll population size at control sites and a 94% reduction at treatment sites: a significant effect of aversion training, but in the direction opposite to that expected.
Conclusions: Two complexities – decay of aversion, and individual variation – together, may explain our result. Our trials indicate that most animals are no longer averse within 120 days post-training. Earlier studies indicating that aversion training lasts longer may have inadvertently observed innate (i.e. genetically based) aversion to cane toads. Another possibility is that our dose rate of thiabendazole within the CTA baits was, in fact, too low; or the result may be an artefact of the non-random assignment of treatment and control groups. Ultimately, there is no way of determining exactly why our outcome occurred without further laboratory/captive trails. Regardless, our study demonstrates a failure of CTA training to mitigate the impact of cane toads on northern quolls in this system.
Implications: Our result calls into question the value of this approach for conserving quoll populations, at least in its current form. More generally, our results point to the often-unexpected complexities encountered as ideas progress from captive trials to field deployment.
Keywords: Bait uptake, behavioural change, Bufo marinus, conditioned taste aversion, Dasyurus hallucatus, invasive species, Rhinella marina, thiabendazole.
References
Austin, C, Tuft, K, Ramp, D, Cremona, T, and Webb, JK (2017). Bait preference for remote camera trap studies of the endangered northern quoll (Dasyurus hallucatus). Australian Mammalogy 39, 72–77.| Bait preference for remote camera trap studies of the endangered northern quoll (Dasyurus hallucatus).Crossref | GoogleScholarGoogle Scholar |
Berman, DE, Hazvi, S, Stehberg, J, Bahar, A, and Dudai, Y (2003). Conflicting processes in the extinction of conditioned taste aversion: behavioral and molecular aspects of latency, apparent stagnation, and spontaneous recovery. Learning & Memory 10, 16–25.
| Conflicting processes in the extinction of conditioned taste aversion: behavioral and molecular aspects of latency, apparent stagnation, and spontaneous recovery.Crossref | GoogleScholarGoogle Scholar |
Bernstein, IL (1999). Taste aversion learning: a contemporary perspective. Nutrition 15, 229–234.
| Taste aversion learning: a contemporary perspective.Crossref | GoogleScholarGoogle Scholar |
Bogliani, G, and Fiorella, B (1998). Conditioned aversion as a tool to protect eggs from avian predators in heron colonies. Colonial Waterbirds 21, 69–72.
| Conditioned aversion as a tool to protect eggs from avian predators in heron colonies.Crossref | GoogleScholarGoogle Scholar |
Bolger DT, Vance BT, Morrison TA, Farid H (2011) ‘Wild-ID, Version 1.0 edn.’ (Dartmouth College: Hanover, NH, USA)
Bouton, ME (1993). Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychological Bulletin 114, 80–99.
| Context, time, and memory retrieval in the interference paradigms of Pavlovian learning.Crossref | GoogleScholarGoogle Scholar |
Bouton, ME (2004). Context and behavioral processes in extinction. Learning & Memory 11, 485–494.
| Context and behavioral processes in extinction.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.
| Colonizing cane toads cause population declines in native predators: reliable anecdotal information and management implications.Crossref | GoogleScholarGoogle Scholar |
Clarke, JC, Westbrook, RF, and Irwin, J (1979). Potentiation instead of overshadowing in the pigeon. Behavioral and Neural Biology 25, 18–29.
| Potentiation instead of overshadowing in the pigeon.Crossref | GoogleScholarGoogle Scholar |
Conover MR (1995) Behavioral principles governing conditioned food aversions based on deception. In ‘Paper presented at the USDA National Wildlife Research Center Symposia National Wildlife Research Center Repellents Conference 1995. Paper 11, 29–41’. (University of Nebraska: Lincoln, USA)
Cremona, T, Spencer, P, Shine, R, and Webb, JK (2017a). Avoiding the last supper: parentage analysis indicates multi-generational survival of re-introduced ‘toad-smart’ lineage. Conservation Genetics 18, 1475–1480.
| Avoiding the last supper: parentage analysis indicates multi-generational survival of re-introduced ‘toad-smart’ lineage.Crossref | GoogleScholarGoogle Scholar |
Cremona, T, Crowther, MS, and Webb, JK (2017b). High mortality and small population size prevent population recovery of a reintroduced mesopredator. Animal Conservation 20, 555–563.
| High mortality and small population size prevent population recovery of a reintroduced mesopredator.Crossref | GoogleScholarGoogle Scholar |
Diete, RL, Meek, PD, Dixon, KM, Dickman, CR, and Leung, LK-P (2015). Best bait for your buck: bait preference for camera trapping north Australian mammals. Australian Journal of Zoology 63, 376–382.
| Best bait for your buck: bait preference for camera trapping north Australian mammals.Crossref | GoogleScholarGoogle Scholar |
Dilov, P, Chaleva, E, Dzhurov, A, Stoianov, P, and Iotsev, M (1982). Toxicological evaluation of “Farmakhim” thiabendazole in mammals and birds. Veterinarno-meditsinski nauki 19, 92–100.
Doak, DF, and Mills, LS (1994). A useful role for theory in Conservation. Ecology 75, 615–626.
| A useful role for theory in Conservation.Crossref | GoogleScholarGoogle Scholar |
Doody, JS, McHenry, C, Rhind, D, Gray, C, and Clulow, S (2021). Impacts of invasive cane toads on an Endangered marsupial predator and its prey. Endangered Species Research 46, 269–277.
| Impacts of invasive cane toads on an Endangered marsupial predator and its prey.Crossref | GoogleScholarGoogle Scholar |
Driscoll, DA, and Lindenmayer, DB (2012). Framework to improve the application of theory in ecology and conservation. Ecological Monographs 82, 129–147.
| Framework to improve the application of theory in ecology and conservation.Crossref | GoogleScholarGoogle Scholar |
Environment Protection and Biodiversity Conservation Act (2011) Referral guidelines for the endangered northern quoll, Dasyurus hallucatus. Available at https://www.dcceew.gov.au/environment/biodiversity/threatened/publications/referral-guideline-northern-quoll
Gelman, A, and Rubin, DB (1992a). Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–472.
| Inference from iterative simulation using multiple sequences.Crossref | GoogleScholarGoogle Scholar |
Gelman, A, and Rubin, DB (1992b). Practical Markov chain Monte Carlo: rejoinder: replication without contrition. Statistical Science 7, 503–511.
| Practical Markov chain Monte Carlo: rejoinder: replication without contrition.Crossref | GoogleScholarGoogle Scholar |
Gentle, M, Massei, G, and Saunders, G (2004). Levamisole can reduce bait monopolization in wild red foxes Vulpes vulpes. Mammal Review 34, 325–330.
| Levamisole can reduce bait monopolization in wild red foxes Vulpes vulpes.Crossref | GoogleScholarGoogle Scholar |
Glendinning, JI (2007). How do predators cope with chemically defended foods? The Biological Bulletin 213, 252–266.
| How do predators cope with chemically defended foods?Crossref | GoogleScholarGoogle Scholar |
Greggor, AL, Clayton, NS, Phalan, B, and Thornton, A (2014). Comparative cognition for conservationists. Trends in Ecology & Evolution 29, 489–495.
| Comparative cognition for conservationists.Crossref | GoogleScholarGoogle Scholar |
Griffin, AS, Blumstein, DT, and Evans, CS (2000). Training captive-bred or translocated animals to avoid predators. Conservation Biology 14, 1317–1326.
| Training captive-bred or translocated animals to avoid predators.Crossref | GoogleScholarGoogle Scholar |
Gustavson, CR, Garcia, J, Hankins, WG, and Rusiniak, KW (1974). Coyote predation control by aversive conditioning. Science 184, 581–583.
| Coyote predation control by aversive conditioning.Crossref | GoogleScholarGoogle Scholar |
Gustavson, CR, Gustavson, JC, and Holzer, GA (1983). Thiabendazole-based taste aversions in dingoes (Canis familiaris dingo) and New Guinea wild dogs (Canis familiaris hallstromi). Applied Animal Ethology 10, 385–388.
| Thiabendazole-based taste aversions in dingoes (Canis familiaris dingo) and New Guinea wild dogs (Canis familiaris hallstromi).Crossref | GoogleScholarGoogle Scholar |
Haselgrove, M, and Pearce, JM (2003). Facilitation of extinction by an increase or a decrease in trial duration. Journal of Experimental Psychology: Animal Behavior Processes 29, 153–166.
| Facilitation of extinction by an increase or a decrease in trial duration.Crossref | GoogleScholarGoogle Scholar |
Hayes, RA, Crossland, MR, Hagman, M, Capon, RJ, 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 |
Hohnen, R, Ashby, J, Tuft, K, and McGregor, H (2013). Individual identification of northern quolls (Dasyurus hallucatus) using remote cameras. Australian Mammalogy 35, 131–135.
| Individual identification of northern quolls (Dasyurus hallucatus) using remote cameras.Crossref | GoogleScholarGoogle Scholar |
Indigo, N, Smith, J, Webb, JK, and Phillips, B (2018). Not such silly sausages: evidence suggests northern quolls exhibit aversion to toads after training with toad sausages. Austral Ecology 43, 592–601.
| Not such silly sausages: evidence suggests northern quolls exhibit aversion to toads after training with toad sausages.Crossref | GoogleScholarGoogle Scholar |
Indigo, N, Smith, J, Webb, JK, and Phillips, BL (2019). Bangers and cash: baiting efficiency in a heterogeneous population. Wildlife Society Bulletin 43, 669–677.
| Bangers and cash: baiting efficiency in a heterogeneous population.Crossref | GoogleScholarGoogle Scholar |
Indigo, NL, Jolly, CJ, Kelly, E, Smith, J, Webb, JK, and Phillips, BL (2021). Effects of learning and adaptation on population viability. Conservation Biology 35, 1245–1255.
| Effects of learning and adaptation on population viability.Crossref | GoogleScholarGoogle Scholar |
Jolly, CJ, and Phillips, BL (2021). Rapid evolution in predator-free conservation havens and its effects on endangered species recovery. Conservaion Biology 35, 383–385.
| Rapid evolution in predator-free conservation havens and its effects on endangered species recovery.Crossref | GoogleScholarGoogle Scholar |
Jolly, CJ, Kelly, E, Gillespie, GR, Phillips, B, and Webb, JK (2018). Out of the frying pan: reintroduction of toad-smart northern quolls to southern Kakadu National Park. Austral Ecology 43, 139–149.
| Out of the frying pan: reintroduction of toad-smart northern quolls to southern Kakadu National Park.Crossref | GoogleScholarGoogle Scholar |
Kelly, E, and Phillips, BL (2017). Get smart: native mammal develops toad-smart behavior in response to a toxic invader. Behavioral Ecology 28, 854–858.
| Get smart: native mammal develops toad-smart behavior in response to a toxic invader.Crossref | GoogleScholarGoogle Scholar |
Kelly, E, and Phillips, BL (2018). Targeted gene flow and rapid adaptation in an endangered marsupial. Conservation Biology 33, 112–121.
| Targeted gene flow and rapid adaptation in an endangered marsupial.Crossref | GoogleScholarGoogle Scholar |
Kelly, E, Phillips, BL, and Webb, JK (2018). Taste overshadows less salient cues to elicit food aversion in endangered marsupial. Applied Animal Behaviour Science 209, 83–87.
| Taste overshadows less salient cues to elicit food aversion in endangered marsupial.Crossref | GoogleScholarGoogle Scholar |
Kery M, Schaub M (2011) ‘Bayesian Population Analysis using WinBUGS: a Hierarchical Perspective.’ (Elsevier Science & Technology, San Diego, CA, USA)
Maguire, GS, Stojanovic, D, and Weston, MA (2009). Conditioned taste aversion reduces fox depredation on model eggs on beaches. Wildlife Research 36, 702–708.
| Conditioned taste aversion reduces fox depredation on model eggs on beaches.Crossref | GoogleScholarGoogle Scholar |
Mappes, J, Marples, N, and Endler, JA (2005). The complex business of survival by aposematism. Trends in Ecology and Evolution 20, 598–603.
| The complex business of survival by aposematism.Crossref | GoogleScholarGoogle Scholar |
Massei, G, Lyon, A, and Cowan, DP (2003). Potential compounds for inducing conditioned taste aversion in ferrets. New Zealand Journal of Zoology 30, 95–100.
| Potential compounds for inducing conditioned taste aversion in ferrets.Crossref | GoogleScholarGoogle Scholar |
Moseby KE, Carthey A, Schroeder T (2015) The influence of predators and prey naivety on reintroduction success; current and future directions. In ‘Advances in Reintroduction Biology of Australian and New Zealand Fauna’. (Eds DP Armstrong, MW Hayward, D Moro, PJ Seddon) pp. 29–42. (CSIRO Publishing: Melbourne, Vic., Australia)
Nachman, M, and Ashe, JH (1973). Learned taste aversions in rats as a function of dosage, concentration, and route of administration of LiCl. Physiology and Behavior 10, 73–78.
| Learned taste aversions in rats as a function of dosage, concentration, and route of administration of LiCl.Crossref | GoogleScholarGoogle Scholar |
Oakwood M (1997) The ecology of the northern quoll, Dasyurus hallucatus. PhD thesis. The Australian National University, Canberra, ACT, Australia.
Oakwood, M (2004). Case of the disappearing spots. Nature Australia 28, 26–35.
Oakwood M (2008) Monitoring extinction of the northern quoll, Australian Academy of Science Newsletter, 71 (March 2008), 6.
Oakwood, M, Bradley, AJ, and Cockburn, A (2001). Semelparity in a large marsupial. Proceedings of the Royal Society of London B: Biological Sciences 268, 407–411.
| Semelparity in a large marsupial.Crossref | GoogleScholarGoogle Scholar |
Otis DL, Burnham KP, White GC, Anderson DR (1978) ‘Statistical inference from capture data on closed animal populations.’ Wildlife Monographs 62 (October 1978), 3–135 (Wiley: West Sussex, UK)
O’Donnell, S, Webb, JK, 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 |
Pavlov IP (1927) ‘Conditioned Reflexes.’ (Oxford University Press: London, UK)
Phillips, BL, Brown, GP, Greenlees, M, Webb, JK, and Shine, R (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 |
Plummer M (2016) rjags: Bayesian Graphical Models using MCMC. R package version 4-6, (CRAN–R Project) Available at https://cran.r-project.org/web/packages/rjags/rjags.pdf>
R Core Team (2019) ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria)
Read, JL, Peacock, D, Wayne, AF, and Moseby, KE (2015). Toxic Trojans: can feral cat predation be mitigated by making their prey poisonous? Wildlife Research 42, 689–696.
| Toxic Trojans: can feral cat predation be mitigated by making their prey poisonous?Crossref | GoogleScholarGoogle Scholar |
Royle, JA, Dorazio, RM, and Link, WA (2007). Analysis of multinomial models with unknown index using data augmentation. Journal of Computational and Graphical Statistics 16, 67–85.
| Analysis of multinomial models with unknown index using data augmentation.Crossref | GoogleScholarGoogle Scholar |
Scheibel, NC, Dembkowski, DJ, Davis, JL, and Chipps, SR (2016). Impacts of northern pike on stocked rainbow trout in pactola reservoir, South Dakota. North American Journal of Fisheries Management 36, 230–240.
| Impacts of northern pike on stocked rainbow trout in pactola reservoir, South Dakota.Crossref | GoogleScholarGoogle Scholar |
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 |
Simberloff, D (1988). The contribution of population and community biology to conservation science. Annual Review of Ecology and Systematics 19, 473–511.
| The contribution of population and community biology to conservation science.Crossref | GoogleScholarGoogle Scholar |
Smith, JG, and Phillips, BL (2006). Toxic tucker: the potential impact of cane toads on Australian reptiles. Pacific Conservation Biology 12, 40–49.
| Toxic tucker: the potential impact of cane toads on Australian reptiles.Crossref | GoogleScholarGoogle Scholar |
Smith, EP, Orvos, DR, and Cairns, J (1993). Impact assessment using the before-after-control-impact (BACI) model: concerns and comments. Canadian Journal of Fisheries and Aquatic Sciences 50, 627–637.
| Impact assessment using the before-after-control-impact (BACI) model: concerns and comments.Crossref | GoogleScholarGoogle Scholar |
Smith, J, Legge, S, James, A, and Tuft, K (2017). Optimising camera trap deployment design across multiple sites for species inventory surveys. Pacific Conservation Biology 23, 43–51.
| Optimising camera trap deployment design across multiple sites for species inventory surveys.Crossref | GoogleScholarGoogle Scholar |
Tan, LXL, van Dongen, WFD, Sherman, CDH, Ekanayake, KB, Dann, P, Sutherland, DR, and Weston, MA (2021). Transmission of a novel predatory behaviour is not restricted to kin. Biological Invasions 23, 2473–2484.
| Transmission of a novel predatory behaviour is not restricted to kin.Crossref | GoogleScholarGoogle Scholar |
Tanner, MA, and Wong, WH (1987). The calculation of posterior distributions by data augmentation. Journal of the American Statistical Association 82, 528–540.
| The calculation of posterior distributions by data augmentation.Crossref | GoogleScholarGoogle Scholar |
Tingley, R, Ward-Fear, G, Schwarzkopf, L, et al. (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 |
Urban, MC, Phillips, BL, Skelly, DK, and Shine, R (2007). The cane toad’s (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 1413–1419.
| The cane toad’s (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model.Crossref | GoogleScholarGoogle Scholar |
Wandile, (2018). Ethical deliberations on using placebos in clinical trials. Association of Clinical Research Professionals 32, 30–41.
Ward-Fear, G, Pearson, DJ, Brown, GP, and Balanggarra Rangers, Shine R (2016). Ecological immunization: in situ training of free-ranging predatory lizards reduces their vulnerability to invasive toxic prey. Biology Letters 12, .
| Ecological immunization: in situ training of free-ranging predatory lizards reduces their vulnerability to invasive toxic prey.Crossref | GoogleScholarGoogle Scholar |
Ward-Fear, G, Thomas, J, Webb, JK, Pearson, DJ, and Shine, R (2017). Eliciting conditioned taste aversion in lizards: live toxic prey are more effective than scent and taste cues alone. Integrative Zoology 12, 112–120.
| Eliciting conditioned taste aversion in lizards: live toxic prey are more effective than scent and taste cues alone.Crossref | GoogleScholarGoogle Scholar |
Watson M, Woinarski JCZ (2004) Vertebrate monitoring and re-sampling in Kakadu National Park, Year 3, 2003–4. Tropical Savanas Research Centre, Darwin, NT, Australia.
Webb, JK, Brown, GP, Child, T, Greenlees, MJ, Phillips, BL, 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, Legge S, Tuft K, Cremona T, Austin C (2015) Can we mitigate cane toad impacts on northern quolls?. National Environmental Research Program, Northern Australia Hub, Charles Darwin University, Casuarina, NT. Australia.
Woinarski JCZ, Oakwood M, Winter J, et al. (2008) Surviving the toads: patterns of persistence of the northern quoll Dasyurus hallucatus in Queensland. Report to The Australian Government’s Natural Heritage Trust, Canberra, ACT, Australia
Woolf, SH (2008). The meaning of translational research and why it matters. Journal of the American Medical Association 299, 211–213.
| The meaning of translational research and why it matters.Crossref | GoogleScholarGoogle Scholar |
