Abstract
This study presents morphological and molecular data on hookworms from the Australian fur seal Arctocephalus pusillus doriferus (Schreber) currently identified in Australian waters as Uncinaria hamiltoni Baylis, 1933. Additional specimens from the Australian sea lion Neophoca cinerea (Péron) and the New Zealand fur seal Arctocephalus forsteri (Lesson) from Australia, and the Southern elephant seal Mirounga leonina (Linnaeus) from Antarctica, were included. Using the internal transcribed spacer (ITS), hookworms from A. p. doriferus, N. cinerea and A. forsteri were found to be genetically similar but distinct from Uncinaria spp. found in M. leonina from Antarctica, as well as from Zalophus californianus (Lesson) and Callorhinus ursinus (Linnaeus) from California. Few morphological differences were detected between these taxa.
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Anderson, G. R., & Barker, S. C. (1993). Species differentiation in the Didymozoidae (Digenea): restriction fragment length differences in internal transcribed spacer and 5.8S ribosomal DNA. International Journal for Parasitology, 23, 133–136.
Andrews, R. H., & Beveridge, I. (1990). Apparent absence of genetic differences among species of Teladorsagia (Nematoda: Trichostrongylidae). Journal of Helminthology, 64, 290–294.
Baylis, H. A. (1933). A new species of the nematode genus Uncinaria from a sea lion, with some observations on related species. Parasitology, 25, 308–316.
Baylis, H. A. (1947). A redescription of Uncinaria lucasi Stiles, a hookworm of seals. Parasitology, 38, 160–162.
Beron-Vera, B., Crespo, E. A., Raga, J. A., & Pedraza, S. N. (2004). Uncinaria hamiltoni (Nematoda: Ancylostomatidae) in South American sea lions, Otaria flavescens, from Northern Patagonia, Argentina. Journal of Parasitology, 90, 860–863.
Beveridge, I. (1980). Uncinaria hydromyidis sp. n. (Nematoda: Ancylostomatidae) from the Australian water rat, Hydromys chrysogaster. Journal of Parasitology, 66, 1030.
Beveridge, I. (2002). Australian hookworms (Ancylostomatoidea): a review of the species present, their distributions and biogeographical origins. Parassitologia, 44, 83–88.
Blair, D., Agatsuma, T., Watanobe, T., Okamoto, M., & Ito, A. (1997). Geographical genetic structure within the human lung fluke, Paragonimus westermani, detected from DNA sequences. Parasitology, 115, 411–417.
Blasco-Costa, I., Balbuena, A., Raga, J. A., Kostadinova, A., & Olson, P. D. (2010). Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology, 137, 287–302.
Botto, C., & Mane-Garzon, F. (1975). Sobre una nueva subespecie del género Uncinaria (Nematoda, Strongyloidea) de Otaria flavescens Shaw y la especiación en el genero Uncinaria en pinnipedos americanos. Revista de Biología del Uruguay, 3, 127–141.
Castinel, A., Duignan, P. J., Pomroy, W. E., Lyons, E. T., Nadler, S. A., Dailey, M. D., Wilkinson, I. S., & Chilvers, B. L. (2006). First report and characterization of adult Uncinaria spp. in New Zealand sea lion (Phocarctos hookeri) pups. Parasitology Research, 98, 304–309.
Castinel, A., Duignan, P. J., Lyons, E. T., Pomroy, W. E., Gibbs, N., Lopez-Villalobos, N., Chilvers, B. L., & Wilkinson, I. S. (2007). Epidemiology of hookworm (Uncinaria spp.) infection in New Zealand (Hooker’s) sea lion (Phocarctos hookeri) pups on Enderby Island, Auckland Islands (New Zealand) during the breeding seasons from 1999/2000 to 2004/2005. Parasitology Research, 101, 53–62.
Chilton, N. B., Gasser, R. B., & Beveridge, I. (1995). Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology, 25, 647–651.
Chilton, N. B. (2004). The use of ribosomal DNA markers for the identification of bursate nematodes (order Strongylida) and for the diagnosis of infections. Animal Health Research Reviews, 5, 173–187.
Chilvers, B. L., Duignan, P. J., & Robertson, B. C. (2009). Effects of hookworms (Uncinaria sp.) on the early growth and survival of New Zealand sea lion (Phocarctos hookeri) pups. Polar Biology, 32, 295–302.
Dailey, M. D., & Hill, B. L. (1970). A survey of metazoan parasites infecting the California (Zalophus californianus) and Steller (Eumetopias jubatus) sea lion. Bulletin of the Southern California Academy of Science, 69, 126–132.
Durette-Desset (1983). Keys to genera of the superfamily Trichostrongyloidea. In: Anderson, R. C. & Chabaud, A. G. (Eds.), CIH keys to the nematode parasites of vertebrates. No.10. Commonwealth Agricultural Bureaux; Farnham Royal, UK, pp. 1–68.
Gasser, R. B., Chilton, N. B., Hoste, H., & Beveridge, I. (1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminthes. Nucleic Acids Research, 21, 2525–2526.
George-Nascimento, M., Lima, M., & Ortiz, E. (1992). A case of parasite mediated competition? Phenotypic differentiation among hookworms Uncinaria sp. (Nematoda: Ancylostomatidae) in sympatric and allopatric populations of South American sea lions Otaria bryonia, and fur seals Arctocephalus australis (Carnivora: Otariidae). Marine Biology, 112, 527–533.
Johnston, T. H., & Mawson, P. M. (1945). Parasitic Nematodes Part 2. British, Australian and New Zealand Antarctic Research Expedition Reports, Series B, 5, 73–160.
Keyes, M. C. (1965). Pathology of the northern fur seal. Journal of the American Veterinary Medical Association, 147, 1090–1095.
Lo Giudice, K. (2003). Trophically transmitted parasites and the conservation of small populations: raccoon roundworm and the imperiled Allegheny woodrat. Conservation Biology, 17, 258–266.
Lucas, F. A. (1899). The causes of mortality among seals. In: Jordan, D. S. (Ed.), The fur seals and fur-seal islands of the North Pacific Ocean, part III. Special papers relating to the fur-seal and to the natural history of the Pribilof Islands. Government Printing Office; Washington, DC, pp. 75–98.
Lyons, E. T., Delong, R. L., Melin, S. R., & Tolliver, S. C. (1997). Uncinariasis in northern fur seals and California sea lion pups from California. Journal of Wildlife Diseases, 33, 848–852.
Lyons, E. T., Delong, R. L., Gulland, F. M., Melin, S. R., Tolliver, S. C., & Spraker, T. R. (2000). Comparative biology of Uncinaria spp. in the California sea lion (Zalophus californianus) and the Northern fur seal (Callorhinus ursinus) in California. Journal of Parasitology, 86, 1348–1352.
Lyons, E. T., Melin, S. R., Delong, R. L., Orr, A. J., Gulland, F. M., & Tolliver, S. C. (2001). Current prevalence of adult Uncinaria spp. in northern fur seal (Callorhinus ursinus) and California sea lion (Zalophus californianus) pups on San Miguel Island, California, with notes on the biology of these hookworms. Veterinary Parasitology, 97, 309–318.
Lyons, E. T., Delong, R. L., Nadler, S. A., Laake, J. L., Orr, A. J., Delong, B. L., & Pagan, C. (2011). Investigations of peritoneal and intestinal infections of adult hookworms (Uncinaria spp.) in northern fur seal (Callorhinus ursinus) and California sea lion (Zalophus californianus) pups on San Miguel Island, California (2003). Parasitology Research, 109, 581–589.
Mizuno, A. (1997). Ecological study on the hookworm, Uncinaria lucasi, of northern fur seal, Callorhinus ursinus, in Bering Island, Russia. Japanese Journal of Veterinary Research, 45, 109–110.
Nadler, S. A., Adams, B. J., Lyons, E. T., Delong, R. L., & Melin, S. R. (2000). Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions (Zalophus californianus) and northern fur seals (Callorhinus ursinus). Journal of Parasitology, 86, 1099–1106.
Nadler, S. A. (2002). Species delimitation and nematode biodiversity: phylogenies rule. Nematology, 4, 620–625.
Nolan, M. J., & Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163.
Oliva, D. (1988). Otaria byronia (de Blainville, 1820), the valid scientific name for the southern sea lion (Carnivora: Otariidae). Journal of Natural History, 22, 767–772.
Olsen, O. W. (1958). Hookworms, Uncinaria lucasi Stiles, 1901, in fur seals, Callorhinus ursinus (Linn.), on the Pribilof Islands. Transactions of the Twenty-third North American Wildlife Conference. Washington DC: Wildlife Management Institute, 152–175.
Olsen, O. W., & Lyons, E. T. (1965). Life cycle of Uncinaria lucasi Stiles, 1901 (Nematoda: Ancylostomatidae) of fur seals, Callorhinus ursinus Linn., on the Pribilof Islands, Alaska. Journal of Parasitology, 51, 689–700.
Prociv, P., & Croese, J. (1996). Human enteric infection with Ancylostoma caninum: hookworms re-appraised in the light of a ‘new’ zoonosis. Acta Tropica, 62, 23–44.
Sepulveda, M. S., & Alcaino, H. (1993). Fauna helmintologica en el lobo fino de Juan Fernandez, Arctocephalus philippii (Peters, 1866). Parasitologia al Dia, 17, 19–24.
Sepulveda, M. S. (1998). Hookworms (Uncinaria sp.) in Juan Fernandez fur seal pups (Arctocephalus philippii) from Alejandro Selkirk Island. Journal of Parasitology, 84, 1305–1306.
Spraker, T. R., De Long, R. L., Lyons, E. T., & Melin, S. R. (2007). Hookworm enteritis with bacteremia in California sea lion pups on San Miguel Island. Journal of Wildlife Diseases, 43, 179–188.
Traub, R. J., Inpankaew, T., Sutthikornchai, C., Sukthana, Y., & Thompson, R. C. (2008). PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Veterinary Parasitology, 155, 67–73.
Zhang, J. S., Daszak, P., Huang, H. L., Yang, G. Y., Kilpatrick, A. M., & Zhang, S. Y. (2008). Parasite threat to panda conservation. EcoHealth, 5, 6–9.
Acknowledgements
We wish to thank Roger Kirkwood, Tony Mitchell, Andrew Hoskins and Parks Victoria for logistical support and assistance in sample collection; Garry Anderson for statistical analysis; Robin Gasser and Matthew Nolan for molecular input; Angela Kapparis for editing assistance; Zoos Victoria, the University of Melbourne Department of Veterinary Science and the Melbourne Zoo veterinary department for logistical and financial support.
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Ramos, P., Lynch, M., Hu, M. et al. Morphometric and molecular characterization of the species of Uncinaria Frölich, 1789 (Nematoda) parasitic in the Australian fur seal Arctocephalus pusillus doriferus (Schreber), with notes on hookworms in three other pinniped hosts. Syst Parasitol 85, 65–78 (2013). https://doi.org/10.1007/s11230-013-9407-x
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DOI: https://doi.org/10.1007/s11230-013-9407-x