Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-18T02:00:40.310Z Has data issue: false hasContentIssue false

Size and sex matter: infection dynamics of an invading parasite (the pentastome Raillietiella frenatus) in an invading host (the cane toad Rhinella marina)

Published online by Cambridge University Press:  20 July 2012

CRYSTAL KELEHEAR*
Affiliation:
School of Biological Sciences, A08, University of Sydney, NSW 2006, Australia
GREGORY P. BROWN
Affiliation:
School of Biological Sciences, A08, University of Sydney, NSW 2006, Australia
RICHARD SHINE
Affiliation:
School of Biological Sciences, A08, University of Sydney, NSW 2006, Australia
*
*Corresponding author: Tel: +61 2 9351 3772. Fax: +61 2 9351 5609. E-mail: [email protected]

Summary

Correlations between host phenotype and vulnerability to parasites can clarify the processes that enhance rates of parasitism, and the effects of parasites on their hosts. We studied an invasive parasite (the pentastome Raillietiella frenatus, subclass Pentastomida, order Cephalobaenida) infecting a new host (the invasive cane toad Rhinella marina), in tropical Australia. We dissected toads over a 27-month period to investigate seasonal changes in pentastome population dynamics and establish which aspects of host phenotype are related to infection. Pentastome prevalence and intensity varied seasonally; male toads were 4 times more likely to be infected than were females; and prevalence was highest in hosts of intermediate body size. The strong sex effect may reflect habitat or dietary divergence between the sexes, resulting in males encountering parasites more often. The relationship between pentastome prevalence and host size likely reflects a role for acquired immunity in preventing re-infection. Infection did not influence host body condition (fatbody size), suggesting that R. frenatus does not impose high energy costs in cane toads. Infected toads had heavier spleens (likely an immune response to infection) and larger testes (perhaps since reproductively active hosts have altered microhabitat use and/or immunocompetence) than did uninfected conspecifics. Although experimental studies are required to identify the causal bases of such patterns, our data confirm that infection status within a population can be strongly linked to host phenotypic traits.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Abadi, M. A., Stephney, G. and Factor, S. M. (1996). Cardiac pentastomiasis and tuberculosis: the worm-eaten heart. Cardiovascular Pathology 5, 169174.CrossRefGoogle ScholarPubMed
Ali, J. H. and Riley, J. (1983). Experimental life-cycle studies of Raillietiella gehyrae Bovien, 1927 and Raillietiella frenatus Ali, Riley and Self, 1981: pentastomid parasites of geckos utilizing insects as intermediate hosts. Parasitology 86, 147160.CrossRefGoogle Scholar
Ali, J. H., Riley, J. and Self, J. T. (1981). A revision of the taxonomy of the blunt-hooked Raillietiella, pentastomid parasites of African, south-east Asian and Indonesian lizards, with a description of a new species. Systematic Parasitology 3, 193207.CrossRefGoogle Scholar
Almeida, W. O., Guedes, T. B., Freire, E. M. X. and Vasconcellos, A. (2008). Pentastomid infection in Philodryas nattereri Steindachner, 1870 and Oxybelis aeneus (Wagler, 1824) (Squamata: Colubridae) in a caatinga of northeastern Brazil. Brazilian Journal of Biology 68, 193197.CrossRefGoogle Scholar
Anjos, L. A., Almeida, W. O., Vasconcellos, A., Freire, E. M. X. and Rocha, C. F. D. (2007). The alien and native pentastomids fauna of an exotic lizard population from Brazilian northeast. Parasitology Research 101, 627628.CrossRefGoogle ScholarPubMed
Awachie, J. B. E. (1974). On the pathogenic effects of Raillietiella affinis Bovien (Pentastomida) on the house wall gecko (Hemidactylus brookii angulatus Hallowell) with notes on the aetiology of human porocephalosis in Africa. Proceedings of the 3rd International Congress of Parasitology, Munich 2, 10241025.Google Scholar
Ayinmode, A. B., Adedokun, A. O., Aina, A. and Taiwo, V. (2010). The zoonotic implications of pentastomiasis in the royal python (Python regius). Ghana Medical Journal 44, 115118.Google ScholarPubMed
Bartelt, P. E., Peterson, C. R. and Klaver, R. W. (2004). Sexual differences in the post-breeding movements and habitats selected by western toads (Bufo boreas) in southeastern Idaho. Herpetologica 60, 455467.CrossRefGoogle Scholar
Barton, D. P. (2007). Pentastomid parasites of the introduced Asian house gecko, Hemidactylus frenatus (Gekkonidae), in Australia. Comparative Parasitology 74, 254259.CrossRefGoogle Scholar
Barton, D. P. and Riley, J. (2004). Raillietiella indica (Pentastomida) from the lungs of the giant toad Bufo marinus (Amphibia), in Hawaii, U.S.A. Comparative Parasitology 71, 251254.CrossRefGoogle Scholar
Bowcock, H., Brown, G. P. and Shine, R. (2008). Sexual communication in cane toads, Chaunus marinus: what cues influence the duration of amplexus? Animal Behaviour 75, 15711579. doi: 10.1016/j.anbehav.2007.10.011.CrossRefGoogle Scholar
Brookins, M. D., Wellehan, J. F. X., Roberts, J. F., Allison, K., Curran, S. S., Childress, A. L. and Greiner, E. C. (2009). Massive visceral pentastomiasis caused by Porocephalus crotali in a dog. Veterinary Pathology 46, 460463. doi: 10.1354/vp.07-VP-0246-R-BC.CrossRefGoogle Scholar
Brown, G. P., Kelehear, C. and Shine, R. (2011). Effects of seasonal aridity on the ecology and behaviour of invasive cane toads (Rhinella marina) in the Australian wet-dry tropics. Functional Ecology 25, 13391347. doi: 10.1111/j.1365-2435.2011.01888.x.CrossRefGoogle Scholar
Bull, E. L. (2006). Sexual differences in the ecology and habitat selection of western toads (Bufo boreas) in northeastern Oregon. Herpetological Conservation and Biology 1, 2738.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443449.CrossRefGoogle ScholarPubMed
Davies, N. B. and Halliday, T. R. (1979). Competitive mate searching in male common toads, Bufo bufo. Animal Behaviour 27, 12531267. doi: 10.1016/0003-3472(79)90070-8.CrossRefGoogle Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603622.CrossRefGoogle Scholar
Freeland, W. J. (1983). Parasites and the coexistance of animal host species. American Naturalist 121, 223236.CrossRefGoogle Scholar
Goldberg, S. R. and Bursey, C. R. (2000). Transport of helminths to Hawaii via the brown anole, Anolis sagrei (Polychrotidae). Journal of Parasitology 86, 750755.CrossRefGoogle ScholarPubMed
Hansen, J. D. and Zapata, A. G. (1998). Lymphocyte development in fish and amphibians. Immunological Reviews 166, 199220. doi: 10.1111/j.1600-065X.1998.tb01264.x.CrossRefGoogle ScholarPubMed
Harris, J. A. (1972). Seasonal variation in some hematological characteristics of Rana pipiens. Comparative Biochemistry and Physiology A 43, 975989.CrossRefGoogle ScholarPubMed
Hudson, P. J. and Dobson, A. P. (1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations (eds. Grenfell, B. T. and Dobson, A. P.), pp. 144176. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 22562258.CrossRefGoogle ScholarPubMed
Jackman, S. (2011). pscl: Classes and methods for R developed in the Political Science Computational Laboratory, Stanford University. Department of Political Science. In R package version 1.04.1. Stanford, California, USA.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2001). Protopolystoma xenopodis (Monogenea) primary and secondary infections in Xenopus laevis. Parasitology 123, 455463. doi: 10.1017/S0031182001008745.CrossRefGoogle ScholarPubMed
Jacobson, E. R. (2007). Parasites and parasitic diseases of reptiles. In Infectious Diseases and Pathology of Reptiles (ed. Jacobson, E. R.), pp. 590592. Taylor & Francis Group, Boca Raton, FL, USA.CrossRefGoogle Scholar
John, J. L. (1995). Parasites and the avian spleen: helminths. Biological Journal of the Linnean Society 54, 87106.CrossRefGoogle Scholar
Jørgensen, C. B., Shakuntala, K. and Vijayakumar, S. (1986). Body size, reproduction and growth in a tropical toad, Bufo melanostictus, with a comparison of ovarian cycles in tropical and temperate zone anurans. Oikos 46, 379389.CrossRefGoogle Scholar
Kearney, M., Phillips, B. L., Tracy, C. R., Christian, K. A., Betts, G. and Porter, W. P. (2008). Modelling species distributions without using species distributions: the cane toad in Australia under current and future climates. Ecography 31, 423434. doi: 10.1111/j.2008.0906-7590-05457.x.CrossRefGoogle Scholar
Kelehear, C., Brown, G. P. and Shine, R. (2011 a). Influence of lung parasites on the growth rates of free-ranging and captive adult cane toads. Oecologia 165, 585592. doi: 10.1007/s00442-010-1836-5.CrossRefGoogle ScholarPubMed
Kelehear, C., Spratt, D. M., Dubey, S., Brown, G. P. and Shine, R. (2011 b). Using combined morphological, allometric and molecular approaches to identify species of the genus Raillietiella (Pentastomida). PLoS ONE 6, e24936. doi: 10.1371/journal.pone.0024936.CrossRefGoogle ScholarPubMed
Lee, K. A. and Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology and Evolution 19, 523529. doi:10.1016/j.tree.2004.07.012.CrossRefGoogle ScholarPubMed
Lever, C. (2001). The cane toad: the history and ecology of a successful colonist, Westbury Academic and Scientific Publishing, Otley, West Yorkshire.Google Scholar
Maragno, F. P. and Souza, F. L. (2011). Diet of Rhinella scitula (Anura, Bufonidae) in the Cerrado, Brazil: the importance of seasons and body size. Revista Mexicana de Biodiversidad 82, 879886.CrossRefGoogle Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. and Schad, G. A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131133.CrossRefGoogle Scholar
Matsuo, K. and Oku, Y. (2002). Endoparasites of three species of house geckoes in Lampung, Indonesia. Journal of Helminthology 76, 5357.CrossRefGoogle ScholarPubMed
McClelland, B. E. and Wilczynski, W. (1989). Sexually dimorphic laryngeal morphology in Rana pipiens. Journal of Morphology 201, 293299.CrossRefGoogle ScholarPubMed
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
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
Morand, S. and Poulin, R. (2000). Nematode parasite species richness and the evolution of spleen size in birds. Canadian Journal of Zoology 78, 13561360.CrossRefGoogle Scholar
Morton, M. L. and Pereyra, M. E. (2010). Habitat use by Yosemite toads: life history traits and implications for conservation. Herpetological Conservation and Biology 5, 388394.Google Scholar
Noble, G. K. (1931). Biology of the Amphibia, McGraw Hill, New York.CrossRefGoogle Scholar
Pare, J. A. (2008). An overview of pentastomiasis in reptiles and other vertebrates. Journal of Exotic Pet Medicine 17, 285294. doi: 10.1053/j.jepm.2008.07.005.CrossRefGoogle Scholar
Pence, D. B. and Selcer, K. W. (1988). Effects of pentastome infection on reproduction in a southern Texas population of the Mediterranean gecko, Hemidactylus turcicus. Copeia 1988, 565572.CrossRefGoogle Scholar
Phillips, B. L., Brown, G. P., Greenlees, M., Webb, J. K. and Shine, R. (2007). Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecology 32, 169176. doi: 10.1111/j.1442-9993.2007.01664.x.CrossRefGoogle Scholar
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147, 287295.CrossRefGoogle Scholar
Poulin, R. (2011). The many roads to parasitism: a tale of convergence. Advances in Parasitology 74, 140. doi: 10.1016/B978-0-12-385897-9.00001-X.CrossRefGoogle ScholarPubMed
Pulis, E. E., Tkach, V. V. and Newman, R. A. (2011). Helminth parasites of the wood frog, Lithobates sylvaticus, in prairie pothole wetlands of the northern Great Plains. Wetlands 31, 675685. doi: 10.1007/s13157-011-0183-6.CrossRefGoogle Scholar
Riley, J. and Walters, L. S. (1980). Porocephalus dominicana n.sp. from the Dominican boa (Constrictor constrictor nebulosus). Systematic Parasitology 1, 123126.CrossRefGoogle Scholar
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
Schmidt, R. S. (1972). Release calling and inflating movements in anurans. Copeia 1972, 240245.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology (Suppl.), 111, S111S133.CrossRefGoogle ScholarPubMed
Suthers, R. A., Narins, P. M., Lin, W.-Y., Schnitzler, H.-U., Denzinger, A., Xu, C.-H. and Feng, A. S. (2006). Voices of the dead: complex nonlinear vocal signals from the larynx of an ultrasonic frog. Journal of Experimental Biology 209, 49844993. doi: 10.1242/jeb.02594.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1995). Parasitic disease in amphibians: control by the regulation of worm burdens. Parasitology 111 (Suppl.), S153S178.CrossRefGoogle ScholarPubMed
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (eds. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 644. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Yao, M. H., Wu, F. and Tang, L. F. (2008). Human pentastomiasis in China: case report and literature review. Journal of Parasitology 94, 12951298.CrossRefGoogle Scholar
Yapo Ette, H., Fanton, L., Adou Bryn, K. D., Botti, K., Koffi, K. and Malicier, D. (2003). Human pentastomiasis discovered postmortem. Forensic Science International 137, 5254. doi: 10.1016/S0379-0738(03)00281-0.CrossRefGoogle ScholarPubMed
Zhang, Y., Zhang, S., Li, K., Chen, H. and Xie, H. (1988). Reports on pentastomiasis in Gecko gecko in China. Journal of Guangxi Agricultural College 7, 6164.Google Scholar
Zimmitti, S. J. (1999). Individual variation in morphological, physiological, and biochemical features associated with calling in spring peepers (Pseudacris crucifer). Physiological and Biochemical Zoology 72, 666676.CrossRefGoogle ScholarPubMed