Biological Invasions

, Volume 12, Issue 5, pp 1045–1051 | Cite as

Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad)

  • John Llewelyn
  • Lin Schwarzkopf
  • Ross Alford
  • Richard Shine
Original Paper


Predictions from foraging theory suggest that the probability a native predator will incorporate a novel type of prey (such as an invasive species) into its diet depends upon the potential benefits (e.g., nutrient input) vs. costs (e.g., handling time) of ingesting it. Cane toads (Bufo marinus) were introduced to Australia in 1935 and are highly toxic to many frog-eating snakes, thus there was strong selection to delete toads from the diet of these species. What has happened, however, to the feeding responses of an Australian snake species that is able to consume toads without dying? Our field surveys in northeastern Queensland show that, despite their high tolerance to toad toxins (compared to other native snakes), keelbacks (Tropidonophis mairii) feed primarily on native frogs rather than cane toads. This pattern occurs because the snakes show active prey preferences; even under standardized conditions in the laboratory, snakes are more likely to consume frogs than toads. When they are force-fed, snakes frequently regurgitate toads but not frogs. Thus, despite the high availability of the abundant toads, these invasive anurans are largely avoided as prey. This probably occurs because consumption of toads, although not lethal to keelbacks, causes significant sublethal effects and confers little nutritional benefit. Hence, keelback populations are not threatened by toad invasion, but neither do the snakes benefit substantially from the availability of a new type of potential prey.


Bufo marinus Chemical defense Foraging behavior Predation Rhinella marina Tropidonophis mairii 



We thank Victoria Llewelyn, Matthew Vucko, Mathew Vickers, Ben Phillips, Matthew Greenlees and Clewdd Burns for their assistance in the field. We also thank Ben Phillips, Melanie Elphick and Greg Brown for their feedback on this manuscript. This research was supported financially by the Australian Research Council. The experiments in this study comply with current Australian laws and were approved by the JCU Animal Ethics Committee (approval #A1114).


  1. Arnold SJ (1977) Polymorphism and geographic variation in the feeding behavior of the garter snake Thamnophis elegans. Science 197:676–678CrossRefGoogle Scholar
  2. Arnold SJ (1981) Behavioral variation in natural populations. II. The inheritance of a feeding response in crosses between geographic races of the garter snake Thamnophis elegans. Evolution 35:510–515CrossRefGoogle Scholar
  3. Breeden K (1963) Cane toad (Bufo marinus). Wildl Aust 1:31Google Scholar
  4. Brown G, Shine R (2007) Rain, prey and predators: climatically driven shifts in frog abundance modify reproductive allometry in a tropical snake. Oecologia 154:361–368CrossRefPubMedGoogle Scholar
  5. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523CrossRefGoogle Scholar
  6. Cogger HG (2000) Reptiles and amphibians of Australia. Reed New Holland, SydneyGoogle Scholar
  7. Cooper CB, Hochachka WM, Dhondt AA (2007) Contrasting natural experiments confirm competition between house finches and house sparrows. Ecology 88:864–870Google Scholar
  8. Crossland MR (2001) Ability of predatory native Australian fishes to learn to avoid toxic larvae of the introduced toad Bufo marinus. J Fish Biol 59:319–329CrossRefGoogle Scholar
  9. Crossland MR, Azevedo-Ramos C (1999) Effects of Bufo (Anura: Bufonidae) toxins on tadpoles from native and exotic Bufo habitats. Herpetologica 55:192–199Google Scholar
  10. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443–449CrossRefPubMedGoogle Scholar
  11. Doody JS, Green B, Sims R, Rhind D, West P, Steer D (2006) Indirect impacts of invasive cane toads (Bufo marinus) on nest predation in pig-nosed turtles (Carettochelys insculpta). Wildl Res 33:349–354CrossRefGoogle Scholar
  12. Doody JS, Green B, Rhind D, Castellano CM, Sims R, Robinson T (2009) Population-level declines in Australian predators caused by an invasive species. Anim Conserv 12:46–53CrossRefGoogle Scholar
  13. Erspamer V, Erspamer GF, Mazzanti G, Endean R (1984) Active peptides in the skins of one hundred amphibian species from Australia and Papua New Guinea. Comp Biochem Physiol C 77:99–108CrossRefPubMedGoogle Scholar
  14. Freeland WJ, Kerin SH (1991) Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildl Res 18:431–444CrossRefGoogle Scholar
  15. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, De Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, and Wheeler WC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:1–370Google Scholar
  16. Gittleman JL, Harvey PH, Greenwood PJ (1980) The evolution of conspicuous coloration: some experiments in bad taste. Anim Behav 28:897–899CrossRefGoogle Scholar
  17. Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433CrossRefGoogle Scholar
  18. Greenlees MJ, Brown GP, Webb JK, Phillips BL, Shine R (2006) Effects of an invasive anuran (the cane toad, Bufo marinus) on the invertebrate fauna of a tropical Australian floodplain. Anim Conserv 9:431–438CrossRefGoogle Scholar
  19. King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84:108–115CrossRefGoogle Scholar
  20. Knapp RA (2005) Effects of nonnative fish and habitat characteristics on lentic herpetofauna in Yosemite National Park, USA. Biol Conserv 121:265–279CrossRefGoogle Scholar
  21. LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710CrossRefPubMedGoogle Scholar
  22. Leberg PL, Vrijenhoek RC (1994) Variation among desert topminnows in their susceptibility to attack by exotic parasites. Conserv Biol 8:419–424CrossRefGoogle Scholar
  23. Lindstrom L, Alatalo RV, Mappes J (1999) Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey. Behav Ecol 10:317–322CrossRefGoogle Scholar
  24. Llewelyn J, Phillips BL, Shine R (2009) Sublethal costs associated with the consumption of toxic prey by snakes. Austral Ecol 34:179–184CrossRefGoogle Scholar
  25. Low T (1999) Feral future: the untold story of Australia’s exotic invaders. Penguin Books Australia, RingwoodGoogle Scholar
  26. Lyon B (1973) Observations on the common keelback snake, Natrix mairii, in Brisbane, south-eastern Queensland. Herpetofauna 6:2–5Google Scholar
  27. Malnate EV, Underwood G (1988) Australasian snakes of the genus Tropidonophis. Proc Acad Nat Sci Phila 140:59–201Google Scholar
  28. Mollo E, Gavagnin M, Carbone M, Castelluccio F, Pozone F, Roussis V, Templado J, Ghiselin MT, Cimino G (2008) Chemical ecology special feature: factors promoting marine invasions: a chemoecological approach. Proc Natl Acad Sci USA 105:4582–4586CrossRefPubMedGoogle Scholar
  29. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19CrossRefGoogle Scholar
  30. Phillips BL, Shine R (2004) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci USA 101:17150–17155CrossRefPubMedGoogle Scholar
  31. Phillips BL, Shine R (2006) An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proc Roy Soc Ser B 273:1545–1550CrossRefGoogle Scholar
  32. Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17:1738–1747CrossRefGoogle Scholar
  33. Pockley D (1965) The free and the caged. Blackwoods Mag 298:439–466Google Scholar
  34. Pramuk J (2007) Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zool J Linn Soc 146:407–452CrossRefGoogle Scholar
  35. Rayward A (1974) Giant toads: a threat to Australian wildlife. Wildlife 17:506–507Google Scholar
  36. Reznick D, Sexton OJ, Mantis C (1981) Initial prey preferences in the lizard Sceloporus malachiticus. Copeia 1981:681–686Google Scholar
  37. Schiffman PM (1994) Promotion of exotic weed establishment by endangered giant kangaroo rats (Dipodomys ingens) in a California grassland. Biodivers Conserv 3:524–537CrossRefGoogle Scholar
  38. Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246CrossRefGoogle Scholar
  39. Shine R (1989) Constraints allometry and adaptation: food habits and reproductive biology of Australian brown snakes (Pseudonaja: Elapidae). Herpetologica 45:195–207Google Scholar
  40. Shine R (1991) Strangers in a strange land: ecology of the Australian colubrid snakes. Copeia 1991:120–131CrossRefGoogle Scholar
  41. Stammer D (1981) Some notes on the cane toad (Bufo marinus). Aust J Herpetol 1:61Google Scholar
  42. Terrick TD, Mumme RL, Burghardt GM (1995) Aposematic coloration enhances chemosensory recognition of noxious prey in the garter snake Thamnophis radix. Anim Behav 49:857–866CrossRefGoogle Scholar
  43. Wiles GJ, Bart J, Beck RE Jr, Aguon CF (2003) Impacts of the brown tree snake: patterns of decline and species persistence in Guam’s avifauna. Conserv Biol 17:1350–1360CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • John Llewelyn
    • 1
    • 2
  • Lin Schwarzkopf
    • 2
  • Ross Alford
    • 2
  • Richard Shine
    • 1
  1. 1.School of Biological SciencesUniversity of SydneySydneyAustralia
  2. 2.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia

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