Advertisement

Biological Invasions

, Volume 18, Issue 6, pp 1645–1652 | Cite as

Far from home: responses of an American predator species to an American prey species in a jointly invaded area of Australia

  • Uditha Wijethunga
  • Matthew Greenlees
  • Richard Shine
Original Paper

Abstract

Far from their native ranges in the Americas, two invasive species come into contact in Australian waterbodies. Cane toads (Rhinella marina) fatally poison many anurophagous predators, whereas eastern mosquito fish (Gambusia holbrooki) voraciously consume anuran larvae. As cane toads spread south along Australia’s east coast, they are colonizing areas where mosquito fish are abundant. What happens when these two American invaders encounter each other in Australia? We tested the responses to toad tadpoles of mosquito fish from populations that were sympatric versus allopatric with cane toads. Toad-sympatric fish generally ignored toad tadpoles. Toad-allopatric fish initially consumed a few tadpoles, but rapidly developed an aversion to these toxic prey items. The laboratory-reared progeny of toad-allopatric fishes were more likely to approach toad tadpoles than were the offspring of toad-sympatric fishes, but the two groups learned toad-avoidance at similar rates. Thus, mosquito fish show an innate aversion to cane toad tadpoles (perhaps reflecting coevolution with North American bufonid taxa), as well as an ability to rapidly learn taste-aversion. Our comparisons among populations suggest that several decades of toad-free existence in Australia caused a decline in the fishes’ innate (heritable) aversion to toads, but did not affect the fishes’ capacity to learn toad-avoidance after an initial exposure. Any impact of mosquito fish on cane toads thus is likely to be transitory. The rapid (<100-year) time frame of these shifts (the initial weakening of the fishes’ response during toad-allopatry, and its recovery after secondary contact) emphasizes the dynamic nature of faunal responses during biological invasions, and the interplay between adaptation and phenotypic plasticity.

Keywords

Bufo marinus Coevolution Conservation Invasive species Preadaptation Predator–prey 

Notes

Acknowledgments

We thank Stewart Harris (Sutherland Shire Council) for logistical support and assistance with field work; Jason Bishop and Jeff Thomas (NSW NPWS), Pamela Gray (Tweed Shire Council), Glenn Murray, Peter Geise, Lesley Reid, Chris Shannon, Sharon Lehman and Russell Jago for assistance with access to field sites; Melanie Elphick assisted with figure preparation and Chalene Bezzina, Jai Thomas for assistance with field-work and husbandry. The work was funded by the Australian Research Council and all experiments were conducted under the approval of the University of Sydney Animals Ethics Committee (Protocol L04/08-2012/3/5808).

References

  1. Adams CK, Saenz D, Conner RN (2011) Palatability of twelve species of anuran larvae in eastern Texas. Am Midl Nat 166:211–223CrossRefGoogle Scholar
  2. Anson J, Dickman C (2013) Behavioral responses of native prey to disparate predators: naiveté and predator recognition. Oecologia 171:367–377CrossRefPubMedGoogle Scholar
  3. Arthington AH (1989) Diet of Gambusia affinis holbrooki, Xiphorus helleri, X. maculatus and Poecilia reticulata (Pisces: Peociliidae) in streams of southeastern Queensland, Australia. Asian Fish Sci 2:193–212Google Scholar
  4. Arthington AH, Lloyd LN (1989) Introduced poeciliids in Australia and New Zealand. In: Meffe GK, Snelson FF (eds) Ecology and evolution of livebearing fishes (Poeciliidae). Prentice-Hall, New Jersey, pp 333–348Google Scholar
  5. Beckmann C, Crossland MR, Shine R (2011) Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina. Biol Invasions 13:2925–2934CrossRefGoogle Scholar
  6. Bence JR (1988) Indirect effects and biological control of mosquitoes by mosquitofish. J Appl Ecol 25:505–521CrossRefGoogle Scholar
  7. Blackburn TM, Duncan RP (2001) Establishment patterns of exotic birds are constrained by non-random patterns in introduction. J Biogeogr 28:927–939CrossRefGoogle Scholar
  8. Blumstein DT (2006) The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217CrossRefGoogle Scholar
  9. Blumstein DT, Ferando E, Stankowich T (2009) A test of the multipredator hypothesis: yellow-bellied marmots respond fearfully to the sight of novel and extinct predators. Anim Behav 78:873–878CrossRefGoogle Scholar
  10. Caller G, Brown C (2013) Evolutionary responses to invasion: cane toad sympatric fish show enhanced avoidance learning. PLoS ONE 8:e54909CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen K, Kovaříková A (1967) Pharmacology and toxicology of toad venom. J Pharm Sci 56:1535–1541CrossRefPubMedGoogle Scholar
  12. 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
  13. Crossland MR, Alford RA (1998) Evaluation of the toxicity of eggs, hatchlings and tadpoles of the introduced toad Bufo marinus (Anura: Bufonidae) to native Australian aquatic predators. Aust J Ecol 23:129–137CrossRefGoogle Scholar
  14. 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
  15. Dickman C (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322CrossRefGoogle Scholar
  16. Elton CS (2000) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoGoogle Scholar
  17. García-Berthou E (1999) Food of introduced mosquitofish: ontogenetic diet shift and prey selection. J Fish Biol 55:135–147CrossRefGoogle Scholar
  18. Gosner KL (1960) A simplified table for staging anuran embryos and larvae. Herpetologica 16:183–190Google Scholar
  19. Greenlees MJ, Shine R (2011) Impacts of eggs and tadpoles of the invasive cane toad (Bufo marinus) on aquatic predators in tropical Australia. Austral Ecol 36:53–58CrossRefGoogle Scholar
  20. Grubb JC (1972) Differential predation by Gambusia affinis on the eggs of seven species of anuran amphibians. Am Midl Nat 88:102–108CrossRefGoogle Scholar
  21. Hayes RA, Crossland MR, Hagman M, Capon RJ, Shine R (2009) Ontogenetic variation in the chemical defenses of cane toads (Bufo marinus): toxin profiles and effects on predators. J Chem Ecol 35:391–399CrossRefPubMedGoogle Scholar
  22. Kerfoot WC (1982) A question of taste: crypsis and warning coloration in freshwater zooplankton communities. Ecology 63:538–554CrossRefGoogle Scholar
  23. Komak S, Crossland MR (2000) An assessment of the introduced mosquitofish (Gambusia affinis holbrooki) as a predator of eggs, hatchlings and tadpoles of native and non-native anurans. Wildl Res 27:185–189CrossRefGoogle Scholar
  24. Lawler KL, Hero J-M (1997) Palatability of Bufo marinus tadpoles to a predatory fish decreases with development. Wildl Res 24:327–334CrossRefGoogle Scholar
  25. Lever C (2001) The cane toad. The history and ecology of a successful colonist. Westbury Academic and Scientific Publishing, OtleyGoogle Scholar
  26. Licht L (1967) Death following possible ingestion of toad eggs. Toxicon 5:141–142CrossRefPubMedGoogle Scholar
  27. Llewelyn JS, Phillips BL, Shine R (2009) Sublethal costs associated with the consumption of toxic prey by snakes. Austral Ecol 34:179–184CrossRefGoogle Scholar
  28. Llewelyn J, Schwarzkopf L, Alford R, Shine R (2010) Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad). Biol Invasions 12:1045–1051CrossRefGoogle Scholar
  29. Lloyd LN, Arthington AH, Milton DA (1986) The mosquitofish: a valuable mosquito control agent or a pest? In: Kitching RN (ed) Ecology of exotic plants and animals in Australasia. Jacaranda-Wiley Press, Brisbane, pp 7–25Google Scholar
  30. Mack RN, Lonsdale WM (2001) Humans as global plant dispersers: getting more than we bargained for. Bioscience 51:95–102CrossRefGoogle Scholar
  31. Miller RR (1966) Geographical distribution of Central American freshwater fishes. Copeia 1966:773–802CrossRefGoogle Scholar
  32. Molloy KL, Henderson WR (2006) Science of cane toad invasion and control. In: Proceedings of the Invasive Animals CRC/CSIRO/Qld NRM&W Cane Toad Workshop, June 2006, Brisbane. Invasive Animals Cooperative Research Centre, CanberraGoogle Scholar
  33. Nelson DW, Crossland MR, Shine R (2010) Indirect ecological impacts of an invasive toad on predator–prey interactions among native species. Biol Invasions 12:3363–3369CrossRefGoogle Scholar
  34. Nelson DWM, Crossland MR, Shine R (2011) Behavioural responses of native predators to an invasive toxic prey species. Austral Ecol 36:605–611Google Scholar
  35. Pen LJ, Potter IC (1991) Reproduction, growth and diet of Gambusia holbrooki (Girard) in a temperate Australian river. Aquat Conserv 1:159–172CrossRefGoogle Scholar
  36. Phillips BL, Shine R (2006) An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proc R Soc B 273:1545–1550CrossRefPubMedPubMedCentralGoogle Scholar
  37. Phillips BL, Brown GP, Shine R (2004) Assessing the potential for an evolutionary response to rapid environmental change: invasive toads and an Australian snake. Evol Ecol Res 6:799–811Google Scholar
  38. Portheault A, Díaz-Paniagua C, Gómez-Rodríguez C (2007) Predation on amphibian eggs and larvae in temporary ponds: the case of Bufo calamita in southwestern Spain. Rev Écol (Terre Vie) 62:315–322Google Scholar
  39. Punzo F, Lindstrom L (2001) The toxicity of eggs of the giant toad, Bufo marinus to aquatic predators in a Florida retention pond. J Herpetol 35:693–697CrossRefGoogle Scholar
  40. Pyke GH (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fisher 15:339–365CrossRefGoogle Scholar
  41. Pyke GH (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol Syst 39:171–191CrossRefGoogle Scholar
  42. Rehage JS, Barnett B, Sih A (2005) Behavioral responses to a novel predator and competitor of invasive mosquitofish and their non-invasive relatives (Gambusia sp.). Behav Ecol Sociobiol 57:256–266CrossRefGoogle Scholar
  43. Scharf SF, Juanes F, Rountree RE (2000) Predator size-prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248CrossRefGoogle Scholar
  44. Shimada K, Nambara T (1979) Isolation of marinobufagin 3-suberoyl-l-glutamine ester from the skin of Bufo americanus. Tetrahedron Lett 20:163–164CrossRefGoogle Scholar
  45. Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291CrossRefPubMedGoogle Scholar
  46. Shine R (2012) Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evol Appl 5:107–116CrossRefPubMedPubMedCentralGoogle Scholar
  47. Simpkins CA, Shuker JD, Lollback GW, Castley JG, Hero J-M (2014) Environmental variables associated with the distribution and occupancy of habitat specialist tadpoles in naturally acidic, oligotrophic waterbodies. Austral Ecol 39:95–105CrossRefGoogle Scholar
  48. Smith GR, Dibble CJ, Terlecky AJ, Dayer CB, Burner AB, Ogle ME (2013) Effects of invasive western mosquitofish and ammonium nitrate on green frog tadpoles. Copeia 2013:248–253CrossRefGoogle Scholar
  49. Somaweera R, Crossland MR, Shine R (2011) Assessing the potential impact of invasive cane toads on a commercial freshwater fishery in tropical Australia. Wildl Res 38:380–385CrossRefGoogle Scholar
  50. Stenberg JA, Witzell J, Ericson L (2006) Tall herb herbivory resistance reflects historic exposure to leaf beetles in a boreal archipelago age-gradient. Oecologia 148:414–425CrossRefPubMedGoogle Scholar
  51. Tingley R, Vallinoto M, Sequeira F, Kearney MR (2014) Realized niche shift during a global biological invasion. Proc Natl Acad Sci USA 111:10233–10238CrossRefPubMedPubMedCentralGoogle Scholar
  52. Ujvari B, Mun H-C, Conigrave AD, Bray A, Osterkamp J, Halling P, Madsen T (2013) Isolation breeds naivety: island living robs Australian varanid lizards of toad-toxin immunity via four-base-pair mutation. Evolution 67:289–294CrossRefPubMedGoogle Scholar
  53. Wassersug R (1971) On the comparative palatability of some dry-season tadpoles from Costa Rica. Am Midl Nat 86:101–109CrossRefGoogle Scholar
  54. Webb C, Joss J (1997) Does predation by the fish Gambusia holbrooki (Atheriniformes: Poeciliidae) contribute to declining frog populations? Aust Zool 30:316–326CrossRefGoogle Scholar
  55. Zangerl AR, Berenbaum MR (2005) Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proc Natl Acad Sci USA 102:15529–15532CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zeiber RA, Sutton TM, Fisher BE (2008) Western mosquitofish predation on native amphibian eggs and larvae. J Freshw Ecol 23:663–671CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.School of Life and Environmental Sciences A08University of SydneySydneyAustralia

Personalised recommendations