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Rates of development in male and female Wood Frogs and patterns of parasitism by lung nematodes

Published online by Cambridge University Press:  09 November 2007

O. K. DARE*
Affiliation:
Department of Biology, Carleton University, Nesbitt Bldg., 1125 Colonel By Dr., Ottawa, Ontario K1S 5B6, Canada
M. R. FORBES
Affiliation:
Department of Biology, Carleton University, Nesbitt Bldg., 1125 Colonel By Dr., Ottawa, Ontario K1S 5B6, Canada
*
*Corresponding author. Tel: +613 520 2600 Ext.1846. Fax: +613 520 3539. E-mail: odare@connect.carleton.ca

Summary

Researchers are becoming interested in testing whether investment in growth and/or development trades off against investment in parasite defence. We tested this idea by examining relations between development of Wood Frogs (Rana sylvatica) and susceptibility to lung nematodes (Rhabdias ranae). Male and female frogs reared in outdoor mesocosms were the same length and mass at metamorphosis. However, males metamorphosed sooner than females. Lung nematodes were no more likely to penetrate male versus female metamorphs following controlled exposures, but males had higher intensities of adult female worms and the largest worms per host were, on average, of larger size in male metamorphs. Males that took longer to metamorphose carried higher numbers of worms in their lungs than males that metamorphosed early. In comparison, females that developed faster harboured more worms in their lungs than females that took longer to reach metamorphosis. Our results suggest that variation in susceptibility to lung nematodes is influenced by host sex and possibly also by sex-specific relations with developmental rate. Further, male hosts might prove to be a more important source of infective stages of worms than female hosts.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Baker, M. R. (1979). The free-living and parasitic development of Rhabdias spp. (Nematoda: Rhabdiasidiae) in amphibians. Canadian Journal of Zoology 57, 161178.CrossRefGoogle Scholar
Bastien, H. and Leclair, R. (1992). Aging wood frogs (Rana sylvatica) by skeletochronology. Journal of Herpetology 26, 222225.CrossRefGoogle Scholar
Berven, K. A. (1982). The genetic basis of altitudinal variations in the wood frog (Rana sylvatica). An experimental analysis of life history traits. Evolution 36, 962983.Google ScholarPubMed
Bush, A. O., Laffery, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Bush, A. O., Fernandez, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism. The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
Dare, O., Rutherford, P. L. and Forbes, M. R. (2006). Rearing density and susceptibility of Rana pipiens metamorphs to cercariae of a digenetic trematode. Journal of Parasitology 92, 543547.CrossRefGoogle ScholarPubMed
Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicolis. Ecology Letters 7, 8894.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, 469476.Google Scholar
Goater, C. P. (1992). Experimental population dynamics of Rhabdias bufonis (Nematoda) in toads (Bufo bufo)- density-dependence in the primary infection. Parasitology 104, 179187.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, 129136.CrossRefGoogle Scholar
Goater, C. P. and Vandenbos, R. E. (1997). Effects of larval history and lungworm infection on the growth and survival of juvenile Wood frogs (Rana sylvatica). Herpetologica 53, 331338.Google Scholar
Goater, C. P. and Ward, P. I. (1992). Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161165.CrossRefGoogle ScholarPubMed
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183190.Google Scholar
Greenwood, P. J. and Wheeler, P. (1985). The evolution of sexual size dimorphism in birds and mammals: a “ hot blooded” hypothesis. In Evolution: Essays in Honour of John Maynard Smith (ed. Greenwood, P. J., Harvey, P. H. and Slatkin, M.), pp. 287299. Cambridge University Press, Cambridge, UK.Google Scholar
Hine, R. L., Les, B. L. and Hellmich, B. F. (1981). Leopard Frog populations and mortality in Wisconsin, 1974–76. DNR, Madison,Wisconsin. Technical Bulletin No. 122. http://digital.library.wisc.edu/1711.dl/EcoNatRes.DNRBull122.Google Scholar
Howard, R. D. (1985). Proximate mechanisms of sexual selection in wood frogs. Evolution 39, 260277.CrossRefGoogle ScholarPubMed
Isomursu, M., Ratti, O., Helle, P. and Hollmen, T. (2006). Sex and age influence intestinal parasite burden in three boreal grouse species. Journal of Avian Biology 37, 516522.Google Scholar
JMP. Version 4. (1989–2002). SAS Institute Inc. Cary, NC. USA.Google Scholar
Leclair, R. J., Leclair, M. H., Dubois, J. and Daoust, J. L. (2000). Age and size of wood frogs, Rana sylvatica, from Kuujjuarapik, Northern Quebec. Canadian Field Naturalist 114, 381387.CrossRefGoogle Scholar
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798.CrossRefGoogle Scholar
Marcogliese, D. J. (1997). Fecundity of sealworm (Pseudoterranova decipiens) infecting grey seals (Halichoerus grypus) in the Gulf of St Lawrence, Canada: lack of density-dependence. International Journal for Parasitology 27, 14011409.CrossRefGoogle Scholar
McCurdy, D. G., Shutler, D., Mullie, A. and Forbes, M. R. (1998). Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303312.CrossRefGoogle Scholar
Molan, A. L. and James, B. L. (1984). The effects of sex, age and diet of mice and gerbils on susceptibility to Microphallus pygmaeus (Digenea: Microphallidae). International Journal for Parasitology 14, 521526.CrossRefGoogle Scholar
Moller, A. P., Sorci, G. and Erritzoe, J. (1998). Sexual dimorphism in immune defense. American Naturalist 152, 605619.Google Scholar
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 20152018.CrossRefGoogle ScholarPubMed
Poulin, R. (1996 a). Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147, 287295.CrossRefGoogle Scholar
Poulin, R. (1996 b). Helminth growth in vertebrate hosts: does host sex matter? International Journal for Parasitology 26, 13111315.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (1997). Parasite body size distributions: interpreting patterns of skewness. International Journal for Parasitology 27, 959964.Google Scholar
Rollins-Smith, L. A. (1998). Metamorphosis and the amphibian immune system. Immunological Reviews 166, 221230.CrossRefGoogle ScholarPubMed
Schalk, G. and Forbes, M. R. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 6774.CrossRefGoogle Scholar
Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London, B 270, 357366.CrossRefGoogle Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317321.Google Scholar
Sheridan, L. A. D., Poulin, R., Ward, D. F. and Zuk, M. (2000). Sex differences in parasitic infections among arthropod hosts: is there a male bias? Oikos 88, 327334.CrossRefGoogle Scholar
Shine, R. (1979). Sexual selection and sexual dimorphism in the amphibia. Copeia 2, 297306.CrossRefGoogle Scholar
Skorping, A. and Jensen, K. H. (2004). Disease dynamics: all caused by males? Trends in Ecology and Evolution 19, 219220.CrossRefGoogle ScholarPubMed
Soler, J. J., de Neve, L., Perez-Contreras, T., Soler, M. and Sorci, G. (2003). Trade-off between immunocompetence and growth in magpies: an experimental study. Proceedings of the Royal Society of London, B 270, 241248.CrossRefGoogle Scholar
SPSS (2000). SPSS for Windows VS 10.0.7. SPSS Inc, Chicago, IL.Google Scholar
Swanson, J. A., Falvo, R. and Bone, L. W. (1984). Nippostrongylus brasiliensis: effects of testosterone on reproduction and establishment. International Journal for Parasitology 14, 241247.Google Scholar
Tata, J. R. (1999). Amphibian metamorphosis as a model for studying the developmental actions of thyroid hormone. Biochimie 81, 359366.Google Scholar
Tompkins, D. M. and Hudson, P. J. (1999). Regulation of nematode fecundity in the ring-necked pheasant (Phasianus colchicus): not just density dependence. Parasitology 118, 417423.CrossRefGoogle Scholar
Tschirren, B., Fitze, P. S. and Richner, H. (2003). Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology 72, 839845.Google Scholar
Tschirren, B. and Richner, H. (2006). Parasite shape the optimal investment in immunity. Proceedings of the Royal Society of London, B 273, 17731777.CrossRefGoogle Scholar
Waldman, B. (1982). Adaptive significance of communal oviposition in wood frogs (Rana sylvatica). Behavioral Ecology and Sociobiology 10, 169174.Google Scholar
Werner, E. E. (1986). Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. American Naturalist 128, 319341.CrossRefGoogle Scholar
Zar, J. H. (1996). Biostatistical Analysis. 4th Edn. Prentice-Hall, Upper Saddle River, USA.Google Scholar