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

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Abstract

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.

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References

  • Arnold SJ (1977) Polymorphism and geographic variation in the feeding behavior of the garter snake Thamnophis elegans. Science 197:676–678

    Article  Google Scholar 

  • 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 35:510–515

    Article  Google Scholar 

  • Breeden K (1963) Cane toad (Bufo marinus). Wildl Aust 1:31

    Google Scholar 

  • Brown G, Shine R (2007) Rain, prey and predators: climatically driven shifts in frog abundance modify reproductive allometry in a tropical snake. Oecologia 154:361–368

    Article  PubMed  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  CAS  Google Scholar 

  • Cogger HG (2000) Reptiles and amphibians of Australia. Reed New Holland, Sydney

    Google Scholar 

  • Cooper CB, Hochachka WM, Dhondt AA (2007) Contrasting natural experiments confirm competition between house finches and house sparrows. Ecology 88:864–870

    Google Scholar 

  • Crossland MR (2001) Ability of predatory native Australian fishes to learn to avoid toxic larvae of the introduced toad Bufo marinus. J Fish Biol 59:319–329

    Article  Google Scholar 

  • Crossland MR, Azevedo-Ramos C (1999) Effects of Bufo (Anura: Bufonidae) toxins on tadpoles from native and exotic Bufo habitats. Herpetologica 55:192–199

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • 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 33:349–354

    Article  Google Scholar 

  • 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 12:46–53

    Article  Google Scholar 

  • 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 77:99–108

    Article  CAS  PubMed  Google Scholar 

  • Freeland WJ, Kerin SH (1991) Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildl Res 18:431–444

    Article  Google Scholar 

  • 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 297:1–370

  • Gittleman JL, Harvey PH, Greenwood PJ (1980) The evolution of conspicuous coloration: some experiments in bad taste. Anim Behav 28:897–899

    Article  Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  • 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 9:431–438

    Article  Google Scholar 

  • King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84:108–115

    Article  Google Scholar 

  • Knapp RA (2005) Effects of nonnative fish and habitat characteristics on lentic herpetofauna in Yosemite National Park, USA. Biol Conserv 121:265–279

    Article  Google Scholar 

  • LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710

    Article  CAS  PubMed  Google Scholar 

  • Leberg PL, Vrijenhoek RC (1994) Variation among desert topminnows in their susceptibility to attack by exotic parasites. Conserv Biol 8:419–424

    Article  Google Scholar 

  • Lindstrom L, Alatalo RV, Mappes J (1999) Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey. Behav Ecol 10:317–322

    Article  Google Scholar 

  • Llewelyn J, Phillips BL, Shine R (2009) Sublethal costs associated with the consumption of toxic prey by snakes. Austral Ecol 34:179–184

    Article  Google Scholar 

  • Low T (1999) Feral future: the untold story of Australia’s exotic invaders. Penguin Books Australia, Ringwood

    Google Scholar 

  • Lyon B (1973) Observations on the common keelback snake, Natrix mairii, in Brisbane, south-eastern Queensland. Herpetofauna 6:2–5

    Google Scholar 

  • Malnate EV, Underwood G (1988) Australasian snakes of the genus Tropidonophis. Proc Acad Nat Sci Phila 140:59–201

    Google Scholar 

  • 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 105:4582–4586

    Article  CAS  PubMed  Google Scholar 

  • 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 1:3–19

    Article  Google Scholar 

  • Phillips BL, Shine R (2004) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci USA 101:17150–17155

    Article  CAS  PubMed  Google Scholar 

  • 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 273:1545–1550

    Article  Google Scholar 

  • Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17:1738–1747

    Article  Google Scholar 

  • Pockley D (1965) The free and the caged. Blackwoods Mag 298:439–466

    Google Scholar 

  • Pramuk J (2007) Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zool J Linn Soc 146:407–452

    Article  Google Scholar 

  • Rayward A (1974) Giant toads: a threat to Australian wildlife. Wildlife 17:506–507

    Google Scholar 

  • Reznick D, Sexton OJ, Mantis C (1981) Initial prey preferences in the lizard Sceloporus malachiticus. Copeia 1981:681–686

  • Schiffman PM (1994) Promotion of exotic weed establishment by endangered giant kangaroo rats (Dipodomys ingens) in a California grassland. Biodivers Conserv 3:524–537

    Article  Google Scholar 

  • Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246

    Article  Google Scholar 

  • Shine R (1989) Constraints allometry and adaptation: food habits and reproductive biology of Australian brown snakes (Pseudonaja: Elapidae). Herpetologica 45:195–207

    Google Scholar 

  • Shine R (1991) Strangers in a strange land: ecology of the Australian colubrid snakes. Copeia 1991:120–131

    Article  Google Scholar 

  • Stammer D (1981) Some notes on the cane toad (Bufo marinus). Aust J Herpetol 1:61

    Google Scholar 

  • Terrick TD, Mumme RL, Burghardt GM (1995) Aposematic coloration enhances chemosensory recognition of noxious prey in the garter snake Thamnophis radix. Anim Behav 49:857–866

    Article  Google Scholar 

  • 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 17:1350–1360

    Article  Google Scholar 

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Acknowledgments

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).

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Correspondence to John Llewelyn.

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Llewelyn, J., Schwarzkopf, L., Alford, R. et al. Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad). Biol Invasions 12, 1045–1051 (2010). https://doi.org/10.1007/s10530-009-9521-5

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  • DOI: https://doi.org/10.1007/s10530-009-9521-5

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