Oecologia

, Volume 158, Issue 4, pp 625–632 | Cite as

Impact of the invasive cane toad (Bufo marinus) on an Australian frog (Opisthodon ornatus) depends on minor variation in reproductive timing

  • Michael R. Crossland
  • Ross A. Alford
  • Richard Shine
Population Ecology - Original Paper

Abstract

Invasive species are widely viewed as unmitigated ecological catastrophes, but the reality is more complex. Theoretically, invasive species could have negligible or even positive effects if they sufficiently reduce the intensity of processes regulating native populations. Understanding such mechanisms is crucial to predicting ultimate ecological impacts. We used a mesocosm experiment to quantify the impact of eggs and larvae of the introduced cane toad (Bufo marinus) on fitness-related traits (number, size and time of emergence of metamorphs) of a native Australian frog species (Opisthodon ornatus). The results depended upon the timing of oviposition of the two taxa, and hence the life-history stages that came into contact. Growth and survival of O. ornatus tadpoles were enhanced when they preceded B. marinus tadpoles into ponds, and reduced when they followed B. marinus tadpoles into ponds, relative to when tadpoles of both species were added to ponds simultaneously. The dominant tadpole–tadpole interaction is competition, and the results are consistent with competitive priority effects. However, these priority effects were reduced or reversed when O. ornatus tadpoles encountered B. marinus eggs. Predation on toxic toad eggs reduced the survival of O. ornatus and B. marinus. The consequent reduction in tadpole densities allowed the remaining O. ornatus tadpoles to grow more rapidly and to metamorphose at larger body sizes (>60% disparity in mean mass). Thus, exposure to B. marinus eggs reduced the number of O. ornatus metamorphs, but increased their body sizes. If the increased size at metamorphosis more than compensates for the reduced survival, the effective reproductive output of native anurans may be increased rather than decreased by the invasive toad. Minor interspecific differences in the seasonal timing of oviposition thus have the potential to massively alter the impact of invasive cane toads on native anurans.

Keywords

Competition Density dependence Predation Recruitment Priority effects 

References

  1. Alford RA (1989a) Effects of parentage and competitor phenology on the growth of larval Hyla chrysoscelis. Oikos 54:325–330CrossRefGoogle Scholar
  2. Alford RA (1989b) Variation in predator phenology affects predator performance and prey community composition. Ecology 70:206–219CrossRefGoogle Scholar
  3. Alford RA (1999) Ecology: resource use, competition, and predation. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, IL, pp 240–278Google Scholar
  4. Alford RA, Wilbur HM (1985) Priority effects in experimental pond communities: competition between Bufo and Rana. Ecology 66:1097–1105CrossRefGoogle Scholar
  5. Alford RA, Cohen MP, Crossland MR, Hearnden MN, Schwarzkopf L (1995) Population biology of Bufo marinus in northern Australia. In: Finlayson CM (ed) Wetland research in the wet-dry tropics of Australia. Office of the Supervising Scientist, Canberra, pp 173–181Google Scholar
  6. Barker J, Grigg GC, Tyler MJ (1995) A field guide to Australian frogs. Surrey Beatty and Sons, SydneyGoogle Scholar
  7. Berven KA, Gill DE (1983) Interpreting geographic variation in life-history traits. Am Zool 23:85–97Google Scholar
  8. Biek R, Funk WC, Maxell BA, Mills LS (2002) What is missing in amphibian decline research: insights from ecological sensitivity analysis. Conserv Biol 16:728–734CrossRefGoogle Scholar
  9. Boone MD (2005) Juvenile frogs compensate for small metamorph size with terrestrial growth: overcoming the effects of larval density and insecticide exposure. J Herpetol 39:416–423CrossRefGoogle Scholar
  10. Brönmark C, Rundle SD, Erlandsson A (1991) Interactions between freshwater snails and tadpoles: competition and facilitation. Oecologia 87:8–18CrossRefGoogle Scholar
  11. Chelgren ND, Rosenberg DK, Heppell SS, Gitelman AI (2006) Carryover aquatic effects on survival of metamorphic frogs during pond emigration. Ecol Appl 16:250–261PubMedCrossRefGoogle Scholar
  12. Child T (2007) The spatial and temporal ecology of metamorph cane toads (Chaunus marinus) in tropical Australia. B.Sc. (Honours) thesis, School of Biological Sciences, University of Sydney, SydneyGoogle Scholar
  13. Child T, Phillips BL, Brown GP, Shine R (2008) The spatial ecology of cane toads (Bufo marinus) in tropical Australia: why do metamorph toads stay near the water? Austral Ecol 33:630–640Google Scholar
  14. Clarke RD (1974) Postmetamorphic growth rates in a natural population of Fowler’s toad, Bufo woodhousei fowleri. Can J Zool 52:1489–1498CrossRefGoogle Scholar
  15. Cohen MP, Alford RA (1993) Growth, survival, and activity patterns of recently metamorphosed Bufo marinus. Wildl Res 20:1–13CrossRefGoogle Scholar
  16. Corbin JD, D’Antonio CM (2004) Competition between native perennial and exotic annual grasses: implications for an historical invasion. Ecology 85:1273–1283CrossRefGoogle Scholar
  17. Covacevich J, Archer M (1975) The distribution of the cane toad, Bufo marinus, in Australia and its effects on indigenous vertebrates. Mem Queensl Mus 17:305–310Google Scholar
  18. Crossland MR (1998) A comparison of cane toad and native tadpoles as predators of native anuran eggs, hatchlings and larvae. Wildl Res 25:373–381CrossRefGoogle Scholar
  19. Crossland MR (2000) Direct and indirect effects of the introduced toad Bufo marinus (Anura: Bufonidae) on populations of native anuran larvae in Australia. Ecography 23:283–290CrossRefGoogle Scholar
  20. 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
  21. 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
  22. Crossland MR, Brown GP, Anstis M, Shilton C, Shine R (2008) Mass mortality of native anuran tadpoles in tropical Australia due to the invasive cane toad (Bufo marinus). Biol Conserv 141:2387–2394CrossRefGoogle Scholar
  23. Doak DF, Estes JA, Halpern BS, Jacob U, Lindberg DR, Lovvorn J, Monson DH, Tinker MT, Williams TM, Wootton JT, Carroll I, Emmerson M, Micheli F, Novak M (2008) Understanding and predicting ecological dynamics: are major surprises inevitable? Ecology 89:952–961PubMedCrossRefGoogle Scholar
  24. 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
  25. Drake JA (1991) Community-assembly mechanics and the structure of an experimental species ensemble. Am Nat 137:1–26CrossRefGoogle Scholar
  26. Easteal S, Van Beurden EK, Floyd RB, Sabath MD (1985) Continuing geographical spread of Bufo marinus in Australia: range expansion between 1974 and 1980. J Herpetol 19:185–188CrossRefGoogle Scholar
  27. Eubanks MD (2001) Estimates of the direct and indirect effects of red imported fire ants on biological control in field crops. Biol Control 21:35–43CrossRefGoogle Scholar
  28. 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, Wheeler WC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:1–370CrossRefGoogle Scholar
  29. Gamarra JGP, Montoya JM, Alonso D, Solé RV (2005) Competition and introduction regime shape exotic bird communities in Hawaii. Biol Invasions 7:297–307CrossRefGoogle Scholar
  30. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  31. Govindarajulu P, Altwegg R, Anholt BR (2005) Matrix model investigation of invasive species control: bullfrogs on Vancouver Island. Ecol Appl 15:2161–2170CrossRefGoogle Scholar
  32. Hagman M, Shine R (2007) Effects of invasive cane toads on Australian mosquitoes: does the dark cloud have a silver lining? Biol Invasions 9:445–452CrossRefGoogle Scholar
  33. Harrison S, Grace JB, Davies KF, Safford HD, Viers JH (2006) Invasion in a diversity hotspot: exotic cover and native richness in the Californian serpentine flora. Ecology 87:695–703PubMedCrossRefGoogle Scholar
  34. Hearnden MN (1991) Reproductive and larval ecology of Bufo marinus (Anura: Bufonidae). Ph.D. thesis, James Cook University of North Queensland, TownsvilleGoogle Scholar
  35. Hewitt CL, Huxel GR (2002) Invasion success and community resistance in single and multiple species invasion models: do the models support the conclusions? Biol Invasions 4:263–271CrossRefGoogle Scholar
  36. John-Alder HB, Morin PJ (1990) Effects of larval density on jumping ability and stamina in newly metamorphosed Bufo woohousei fowleri. Copeia 1990:856–860Google Scholar
  37. Kelehear C (2007) The effects of lung nematodes (Rhabdias cf. hylae) on metamorph cane toads (Chaunus marinus), and implications for biological control. B.Sc. (Honours) thesis, School of Biological Sciences, University of Sydney, SydneyGoogle Scholar
  38. Lavorel S, Prieur-Richard AH, Grigulis K (1999) Invasibility and diversity of plant communities: from patterns to processes. Divers Distrib 5:41–49CrossRefGoogle Scholar
  39. Lever C (2001) The cane toad: the history and ecology of a successful colonist. Westbury Academic and Scientific Publishing, OtleyGoogle Scholar
  40. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Fakhri AB (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  41. Manly BF (1991) Randomization and Monte Carlo methods in biology, 1st edn. Chapman & Hall, LondonGoogle Scholar
  42. Morin PJ (1981) Predatory salamanders reverse the outcome of competition among three species of anuran tadpoles. Science 212:1284–1286PubMedCrossRefGoogle Scholar
  43. Morin PJ (1983) Predation, competition, and the composition of larval anuran guilds. Ecol Monogr 53:119–138CrossRefGoogle Scholar
  44. Morin PJ (1987) Predation, breeding asynchrony, and the outcome of competition among treefrog tadpoles. Ecology 68:675–683CrossRefGoogle Scholar
  45. Morin PJ, Lawler SP, Johnson EA (1988) Competition between aquatic insects and vertebrates: interaction strength and higher order interactions. Ecology 69:1401–1409CrossRefGoogle Scholar
  46. Nelson DWM (2008) Bufo for breakfast: how cane toads affect native predators and their prey. B.Sc. (Honours) thesis, School of Biological Sciences, University of Sydney, SydneyGoogle Scholar
  47. Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17:1738–1747CrossRefGoogle Scholar
  48. Pramuk JB (2006) Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zool J Linn Soc 146:407–452CrossRefGoogle Scholar
  49. 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
  50. Robinson JF, Dickerson JE Jr (1987) Does invasion sequence affect community structure? Ecology 68:587–595CrossRefGoogle Scholar
  51. Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939CrossRefGoogle Scholar
  52. Sabath MD, Boughton WC, Easteal S (1981) Expansion of the range of the introduced toad Bufo marinus in Australia from 1935 to 1974. Copeia 1981:676–680CrossRefGoogle Scholar
  53. Sait SM, Liu WC, Thompson DJ, Godfray HCJ, Begon M (2000) Invasion sequence affects predator–prey dynamics in a multi-species interaction. Nature 405:448–450PubMedCrossRefGoogle Scholar
  54. Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350CrossRefGoogle Scholar
  55. Smith KG (2005) Effects of nonindigenous tadpoles on native tadpoles in Florida: evidence of competition. Biol Conserv 123:433–441CrossRefGoogle Scholar
  56. Smith KG (2006) Keystone predators (eastern newts, Notophthalmus viridescens) reduce the impacts of an aquatic invasive species. Oecologia 148:342–349PubMedCrossRefGoogle Scholar
  57. Smith JG, Phillips BL (2006) Toxic tucker: the potential impact of cane toads on Australian reptiles. Pac Conserv Biol 12:40–49Google Scholar
  58. Turner FB (1962) The demography of frogs and toads. Q Rev Biol 37:303–314PubMedCrossRefGoogle Scholar
  59. Vonesh JR, De la Cruz O (2002) Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325–333CrossRefGoogle Scholar
  60. Ward SA, Thornton IWB (2000) Chance and determinism in the development of isolated communities. Glob Ecol Biogeogr 9:7–18CrossRefGoogle Scholar
  61. Warner SC, Travis J, Dunson WA (1993) Effect of pH variation on interspecific competition between two species of hylid tadpoles. Ecology 74:183–194CrossRefGoogle Scholar
  62. Webb JK, Brown GP, Child T, Greenlees MJ, Phillips BL, Shine R (2008) A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid toxic cane toads. Austral Ecol (in press)Google Scholar
  63. White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455CrossRefGoogle Scholar
  64. Wilbur HM, Rubenstein DI, Fairchild L (1978) Sexual selection in toads: the roles of female choice and male body size. Evolution 32:264–270CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Michael R. Crossland
    • 1
  • Ross A. Alford
    • 2
  • Richard Shine
    • 1
  1. 1.School of Biological Sciences A08University of SydneySydneyAustralia
  2. 2.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia

Personalised recommendations