Journal of Chemical Ecology

, 35:265 | Cite as

Factors Influencing Responses to Alarm Pheromone by Larvae of Invasive Cane Toads, Bufo marinus



If pheromonal communication systems of invasive species differ from those of native biota, it may be possible to control the invader by exploiting that difference. When injured, the larvae of cane toads, Bufo marinus, an invasive species of major concern in tropical Australia, produce species-specific chemical cues that alert conspecific tadpoles to danger. Repeated exposure to the alarm chemical reduces tadpole survival rates and body sizes at metamorphosis and, thus, could help control toad populations. To evaluate the feasibility of this approach, we need to know how the intensity of toad tadpole response to the alarm chemical is affected by factors such as water temperature, time of day, larval stage and feeding history, geographic origin of the tadpoles, and habituation. Information on these topics may enable us to optimize deployment, so that tadpoles encounter pheromone at the times and places that confer maximum effect. In our studies, tadpole density, nutritional state, larval stage, and geographic origin had little effect on the intensity of the alarm response, but tadpoles reacted most strongly in higher water temperatures and during daylight hours. Repeated, once-daily exposure to pheromone did not induce habituation, but repeated exposure at 15-min intervals did not elicit further responses after 2 h total exposure. The insensitivity of response to most factors tested means that the effectiveness of the pheromone as a control agent should be relatively robust.


Alarm pheromone Anuran Biological control Chemical communication Invasive species 



We thank the Australian Research Council for funding, and the members of Team Bufo for help in many ways. In particular, Michelle Gray and Georgia Ward-Fear helped us to clean containers, and Melanie Elphick prepared the figures for this manuscript.


  1. Beroza, M., and Knipling, E. F. 1972. Gypsy moth control with sexual attractant pheromone. Science 177:19–27.PubMedCrossRefGoogle Scholar
  2. Burnett, S. 1997. Colonising cane toads cause population declines in native predators: reliable anecdotal information and management implications. Pacific Conserv. Biol. 3:65–72.Google Scholar
  3. Cooper, W. E. 2000. Effect of temperature on escape behaviour by an ectothermic vertebrate, the keeled earless lizard (Holbrookia propinqua). Behaviour 137:1299–1315.CrossRefGoogle Scholar
  4. Crossland, M. R., and Alford, R. A. 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. 23:129–137.CrossRefGoogle Scholar
  5. Dalesman, S., Cotton, P. A., Bilton, D. T., and Rundle, S. D. 2007. Phylogenetic relatedness and ecological interactions determine antipredator behaviour. Ecology 88:2462–2467.PubMedCrossRefGoogle Scholar
  6. Ferrari, M. C. O., Messier, F., and Chivers, D. P. 2008. Degradation of alarm cues under natural conditions: risk assessment by larval amphibians. Chemoecology 17:263–266.CrossRefGoogle Scholar
  7. Fraker, M. E. 2008a. The influence of the circadian rhythm of green frog (Rana clamitans) tadpoles on their antipredator behaviour and the strength of the nonlethal effect of predators. Am. Nat. 171:545–552.CrossRefGoogle Scholar
  8. Fraker, M. E. 2008b. The effect of hunger on the strength and duration of the antipredator behavioural response of green frog (Rana clamitans) tadpoles. Behav. Ecol. Sociobiol. 62:1201–1205.CrossRefGoogle Scholar
  9. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De sa, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drewes, R. C. R., Nussbaum, A., Lynch, J. D., Green, D. M., and Wheeler, W. C. 2006. The amphibian tree of life. Bull. Am. Mus. Nat. Hist. 297:1–370.CrossRefGoogle Scholar
  10. Gosner, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190.Google Scholar
  11. Gould, S. J., and Lewontin, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205:581–598.PubMedCrossRefGoogle Scholar
  12. Greene, H. W. 1988. Antipredator mechanisms in reptiles, pp. 1–152, in C. Gans, and R. B. Huey (eds.). Biology of the Reptilia, vol. 16. Alan R. Liss, New York.Google Scholar
  13. Hagman, M., and Shine, R. 2006. Spawning-site selection by feral cane toads (Bufo marinus) at an invasion front in tropical Australia. Austral Ecol. 31:551–558.CrossRefGoogle Scholar
  14. Hagman, M., and Shine, R. 2008a. Understanding the toad code: behavioural responses of cane toad (Chaunus marinus) larvae and metamorphs to chemical cues. Austral Ecol. 33:37–44.Google Scholar
  15. Hagman, M., and Shine, R. 2008b. Australian tadpoles do not avoid chemical cues from invasive cane toads (Bufo marinus). Wildl. Res. 35:59–64.CrossRefGoogle Scholar
  16. Hagman, M., Hayes, R., Capon, R., and Shine, R. 2009. Alarm cues experienced by cane toad tadpoles affect post-metamorphic morphology and chemical defences. Funct. Ecol. 23:126–132.CrossRefGoogle Scholar
  17. Hengeveld, R. 1989. Dynamics of Biological Invasions. Chapman and Hall, New York.Google Scholar
  18. Horat, P., and Semlitsch, R. D. 1994. Effects of predation risk and hunger on the behaviour of two species of tadpoles. Behav. Ecol. Sociobiol. 34:393–401.CrossRefGoogle Scholar
  19. Huey, R., and Slatkin, M. 1976. Costs and benefits of lizard thermoregulation. Q. Rev. Biol. 51:363–384.PubMedCrossRefGoogle Scholar
  20. Langkilde, T., Schwarzkopf, L., and Alford, R. 2003. An ethogram for adult male rainbow skinks, Carlia jarnoldae. Herpetol. J. 13:141–148.Google Scholar
  21. Lever, C. 2001. The Cane Toad. The History and Ecology of a Successful Colonist. Westbury Academic and Scientific, Otley, West Yorkshire.Google Scholar
  22. Newsome, A. E., and Noble, I. R. 1986. Ecological and physical characteristics of invading species, pp. 1–20, in R. H. Groves, and J. J. Burdon (eds.). Ecology of Biological Invasions. An Australian Perspective. Australian Academy of Science, Canberra.Google Scholar
  23. Parker, I. M., Simberloff, D., Lonsdale, W. M., Goodell, K., Wonham, M., Karieva, P. M., Williamson, M. H., Von Holle, B., Moyel, P. B., Byers, J. E., and Goldwasser, L. 1999. Impact: toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1:3–19.CrossRefGoogle Scholar
  24. Passek, K. M., and Gillingham, J. C. 1997. Thermal influence on defensive behaviours of the Eastern garter snake, Thamnophis sirtalis. Anim. Behav. 54:629–633.PubMedCrossRefGoogle Scholar
  25. Peacock, T. 2007. Community On-Ground Cane Toad Control in the Kimberley. Report to the Western Australian Government. Invasive Animals Cooperative Research Centre, Canberra, ACT.Google Scholar
  26. Pelozuelo, L., and Frerot, B. 2006. Behaviour of male European corn borer, Ostrinia nubilalis Hubner (Lep.; Crambidae) towards pheromone-baited delta traps, buckets and wire mesh cone traps. J. Appl. Entomol. 130:230–237.CrossRefGoogle Scholar
  27. Phillips, B. L., Brown, G. P., and Shine, R. 2003. Assessing the potential impact of cane toads on Australian snakes. Conserv. Biol. 17:1738–1747.CrossRefGoogle Scholar
  28. Pramuk, J. B. 2006. Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zool. J. Linn. Soc. 146:407–452.CrossRefGoogle Scholar
  29. Rajchard, J. 2006. Antipredator pheromones in amphibians: a review. Vet. Medicina 51:409–413.Google Scholar
  30. Semeniuk, M., Lemckert, F., and Shine, R. 2007. Breeding-site selection by cane toads (Bufo marinus) and native frogs in northern New South Wales. Wildl. Res. 34:59–66.CrossRefGoogle Scholar
  31. Shine, R., Olsson, M. M., Lemaster, M. P., Moore, I. T., and Mason, R. T. 2000. Effects of sex, body size, temperature and location on the antipredator tactics of free-ranging gartersnakes (Thamnophis sirtalis, Colubridae). Behav. Ecol. 11:239–245.CrossRefGoogle Scholar
  32. Spieler, M., and Linsenmair, K. E. 1999. Aggregation behaviour of Bufo maculatus as an antipredator mechanism. Ethology 105:665–686.CrossRefGoogle Scholar
  33. Summey, M. R., and Mathis, A. 1998. Alarm responses to chemical stimuli from damaged conspecifics by larval anurans: tests of three neotropical species. Herpetologica 54:402–408.Google Scholar
  34. Wassersug, R. J. 1997. Assessing and controlling amphibian populations from the larval perspective, pp. 271–281, in D. M. Green (ed.). Amphibians in Decline: Canadian Studies of a Global Problem. Herpetological Conservation No. 1. Society for the Study of Amphibians and Reptiles, Saint Louis, MO.Google Scholar
  35. Werner, E. E., and Anholt, B. 1993. Ecological consequences of the trade-off between growth and predation mortality rates mediated by foraging activity. Am. Nat. 142:242–272.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.School of Biological Sciences A08University of SydneySydneyAustralia
  2. 2.Department of ZoologyStockholm UniversityStockholmSweden

Personalised recommendations