Hostname: page-component-5cf477f64f-mgq6s Total loading time: 0 Render date: 2025-04-03T10:04:20.862Z Has data issue: false hasContentIssue false
  • English
  • Français

Rhabdias pseudosphaerocephala infection in Bufo marinus: lung nematodes reduce viability of metamorph cane toads

Published online by Cambridge University Press:  15 June 2009

C. KELEHEAR ,
J. K. WEBB  and
R. SHINE
C. KELEHEAR
Affiliation:
School of Biological Sciences A08, University of Sydney, NSW2006, Australia
J. K. WEBB
Affiliation:
School of Biological Sciences A08, University of Sydney, NSW2006, Australia
R. SHINE*
Affiliation:
School of Biological Sciences A08, University of Sydney, NSW2006, Australia
*
*Corresponding author. Tel: +61 2 9351 3772. Fax: +61 2 9351 5609. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Cane toads (Bufo marinus) were introduced to Australia in 1935 and have since spread widely over the continent, generating concern regarding ecological impacts on native predators. Most Australian cane toad populations are infected with lung nematodes Rhabdias pseudosphaerocephala, a parasite endemic to New World (native-range) cane toad populations; presumably introduced to Australia with its toad host. Considering the high intensities and prevalence reached by this parasite in Australian toad populations, and public ardour for developing a control plan for the invasive host species, the lack of experimental studies on this host-parasite system is surprising. To investigate the extent to which this lungworm influences cane toad viability, we experimentally infected metamorph toads (the smallest and presumably most vulnerable terrestrial phase of the anuran life cycle) with the helminth. Infected toads exhibited reduced survival and growth rates, impaired locomotor performance (both speed and endurance), and reduced prey intake. In summary, R. pseudosphaerocephala can substantially reduce the viability of metamorph cane toads.

Keywords

anurangrowth ratehelminthlocomotor performancemortalityprey intake
Type
Research Article
Information
Parasitology , Volume 136 , Issue 8 , July 2009 , pp. 919 - 927
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baker, M. R. (1979). The free-living and parasitic development of Rhabdias spp. (Nematoda: Rhabdiasidae) in amphibians. Canadian Journal of Zoology 57, 161–178.CrossRefGoogle Scholar
Barton, D. P. (1994). A checklist of helminth parasites of Australian amphibia. Records of the South Australian Museum 27, 13–30.Google Scholar
Barton, D. P. (1997). Introduced animals and their parasites: The cane toad, Bufo marinus, in Australia. Australian Journal of Ecology 22, 316–324.CrossRefGoogle Scholar
Barton, D. P. (1998). Dynamics of natural infections of Rhabdias cf. hylae (Nematoda) in Bufo marinus (Amphibia) in Australia. Parasitology 117, 505–513.CrossRefGoogle ScholarPubMed
Barton, D. P. (1999). Ecology of helminth communities in tropical Australian amphibians. International Journal for Parasitology 29, 921–926.CrossRefGoogle ScholarPubMed
Beck, C. W. and Congdon, J. D. (2000). Effects of age and size at metamorphosis on performance and metabolic rates of southern toad, Bufo terrestris, metamorphs. Functional Ecology 14, 32–38.CrossRefGoogle Scholar
Bennett, A. F. and Licht, P. (1974). Anaerobic metabolism during activity in amphibians. Comparative and Biochemical Physiology 48, 319–327.CrossRefGoogle Scholar
Blaustein, A. R. and Kiesecker, J. M. (2002). Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5, 597–608.CrossRefGoogle Scholar
Brown, G. P., Shilton, C. M. and Shine, R. (2006). Do parasites matter? Assessing the fitness consequences of haemogregarine infection in snakes. Canadian Journal of Zoology 84, 668–676.CrossRefGoogle Scholar
Burnett, S. (1997). Colonising cane toads cause population declines in native predators: reliable anecdotal information and management implications. Pacific Conservation Biology 3, 65–72.CrossRefGoogle Scholar
Candolin, U. and Voigt, H. R. (2001). No effect of a parasite on reproduction in stickleback males: a laboratory artefact. Parasitology 122, 457–464.CrossRefGoogle Scholar
Christin, M.-S., Gendron, A. D., Brousseau, P., Ménard, L., Marcogliese, D. J., Cyr, D., Ruby, S. and Fournier, M. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22, 1127–1133.CrossRefGoogle ScholarPubMed
Coors, A. and De Meester, L. (2008). Synergistic, antagonistic and additive effects of multiple stressors, predation threat, parasitism and pesticide exposure in Daphnia magna. Journal of Applied Ecology 45, 1820–1828.CrossRefGoogle Scholar
Dare, O. K. and Forbes, M. R. (2008). Rates of development in male and female Wood Frogs and patterns of parasitism by lung nematodes. Parasitology 135, 385–393.CrossRefGoogle ScholarPubMed
Doody, J. S., Green, B., Sims, R., Rhind, D., West, P. and Steer, D. (2006). Indirect impacts of invasive cane toads (Bufo marinus) on nest predation in pig-nosed turtles (Carettochelys insculpta). Wildlife Research 33, 349–354.CrossRefGoogle Scholar
Dubey, S. and Shine, R. (2008). Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17, 4418–4424.CrossRefGoogle ScholarPubMed
Dunlap, K. D. and Mathies, T. (1993). Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards. Copeia 1993, 1045–1048.CrossRefGoogle Scholar
Freeland, W. J. and Kerin, S. H. (1991). Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildlife Research 18, 431–443.CrossRefGoogle Scholar
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., Nussbaum, R. A., Lynch, J. D., Green, D. M. and Wheeler, W. C. (2006). The amphibian tree of life. Bulletin of the American Museum of Natural History 297, 1–371.CrossRefGoogle Scholar
Gendron, A. D., Marcogliese, D. J., Barbeau, S., Christin, M.-S., Brousseau, P., Ruby, S., Cyr, D. and Fournier, M. (2003). Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135, 469–476.CrossRefGoogle ScholarPubMed
Goater, C. P. (1992). Experimental population dynamics of Rhabdias bufonis (Nematoda) in toads (Bufo bufo): density-dependence in the primary infection. Parasitology 104, 179–187.CrossRefGoogle ScholarPubMed
Goater, C. P., Semlitsch, R. D. and Bernasconi, M. V. (1993). Effects of body size and parasite infection on the locomotory performance of juvenile toads, Bufo bufo. Oikos 66, 129–136.CrossRefGoogle Scholar
Goater, C. P. and Ward, P. I. (1992). Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival or toads (Bufo bufo). Oecologia 89, 161–165.CrossRefGoogle ScholarPubMed
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
Hutchinson, V. H. and Miller, K. (1979). Anaerobic capacity of amphibians. Comparative Biochemistry and Physiology 63A, 213–216.CrossRefGoogle Scholar
Jokela, J., Taskinen, J., Mutikainen, P. and Kopp, K. (2005). Virulence of parasites in hosts under environmental stress: experiments with anoxia and starvation. Oikos 108, 156–164.CrossRefGoogle Scholar
Kiesecker, J. M. (2002). Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature. Proceedings of the National Academy of Sciences, USA 99, 9900–9904.CrossRefGoogle ScholarPubMed
Kumaraguru, A. K., Beamish, F. W. H. and Woo, P. T. K. (1995). Impact of a pathogenic haemoflagellate, Cryptobia salmositica Katz, on the metabolism and swimming performance of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 18, 297–305.CrossRefGoogle Scholar
Lever, C. (2001). The Cane Toad: the History and Ecology of a Successful Colonist, Westbury Academic and Scientific Publishing, OtleyWest Yorkshire, UK.Google Scholar
Main, A. R. and Bull, C. M. (2000). The impact of tick parasites on the behaviour of the lizard Tiliqua rugosa. Oecologia 122, 574–581.CrossRefGoogle ScholarPubMed
Munger, J. C. and Karasov, W. H. (1989). Sublethal parasites and host energy budgets: tapeworm infection in white-footed mice. Ecology 70, 904–921.CrossRefGoogle Scholar
Oppliger, A., Célérier, M. L. and Clobert, J. (1996). Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitology 113, 433–438.CrossRefGoogle Scholar
Pizzatto, L. and Shine, R. (2008). The behavioral ecology of cannibalism in cane toads (Bufo marinus). Behavioral Ecology and Sociobiology 63, 123–133.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn.Princeton University Press, Princeton CT, USA.CrossRefGoogle Scholar
Propper, C. R. and Dixon, T. B. (1997). Differential effects of arginine vasotocin and gonadotropin-releasing hormone on sexual behaviors in an anuran amphibian. Hormones and Behavior 32, 99–104.CrossRefGoogle Scholar
Putnam, R. W. (1979). The basis for differences in lactic acid content after activity in different species of anuran amphibians. Physiological Zoology 52, 509–519.CrossRefGoogle Scholar
Rollins-Smith, L. (1998). Metamorphosis and the amphibian immune system. Immunological Reviews 166, 221–230.CrossRefGoogle ScholarPubMed
SAS (2002). JMP. Version 5. SAS Institute Incorporated, Cary North Carolina, USA.Google Scholar
Schall, J. J., Bennett, A. F. and Putman, R. W. (1982). Lizards infected with malaria: physiological and behavioral consequences. Science 217, 1057–1059.CrossRefGoogle ScholarPubMed
Scott, D. E. (1994). The effect of larval density on adult demographic traits in Ambystoma opacum. Ecology 75, 1383–1396.CrossRefGoogle Scholar
Semlitsch, R. D., Scott, D. E. and Pechmann, J. H. K. (1988). Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69, 184–192.CrossRefGoogle Scholar
Smith, D. C. (1987). Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68, 344–350.CrossRefGoogle Scholar
Speare, R. (1990). A review of the diseases of the cane toad, Bufo marinus, with comments on biological control. Australian Wildlife Research 17, 387–410.CrossRefGoogle Scholar
Todd, B. T. (2007). Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. The American Naturalist 170, 793–799.CrossRefGoogle ScholarPubMed
Tracy, C. R. (1976). A model for the dynamic exchanges of water and energy between a terrestrial amphibian and its environment. Ecological Monographs 46, 293–326.CrossRefGoogle Scholar
Urban, M. C., Phillips, B. L., Skelly, D. K. and Shine, R. (2007). The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society of London, B 274, 1413–1419.Google ScholarPubMed
Van Beurden, E. (1980). Report on the results of Stage 3 of an ecological and physiological study of the Queensland cane toad Bufo marinus. Australian National Parks and Wildlife Service, Canberra, Australia.Google Scholar
Walton, M. (1988). Relationships among metabolic, locomotory, and field measures of organismal performance in the Fowler's toad (Bufo woodhousei fowleri). Physiological Zoology 61, 107–118.CrossRefGoogle Scholar
Wassersug, R. J. and Sperry, D. G. (1977). The relationship of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58, 830–839.CrossRefGoogle Scholar
Webb, J. K., Shine, R. and Christian, K. A. (2005). Does intraspecific niche partitioning in a native predator influence its response to an invasion by a toxic prey species? Austral Ecology 30, 201–209.CrossRefGoogle Scholar
Zug, G. R. and Zug, P. B. (1979). The marine toad, Bufo marinus: a natural history resume of native populations. Smithsonian Contributions to Zoology 284, 1–58.Google Scholar