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Review of research on hookworms (Uncinaria lucasi Stiles, 1901) in northern fur seals (Callorhinus ursinus Linnaeus, 1758)

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Abstract

The objective of this article is to review knowledge on the hookworm Uncinaria lucasi Stiles, 1901 in northern fur seals, Callorhinus ursinus Linnaeus, 1758. Emphasis is placed on research on this host–parasite system in the Pribilof Islands, AK, USA where the bulk of the studies has been performed.

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Acknowledgments

This investigation (paper no. 10-14-118) was made in connection with a project of the University of Kentucky Agricultural Experiment Station and is published with the approval of the director.

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Correspondence to Eugene T. Lyons.

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Lyons, E.T., Spraker, T.R., De Long, R.L. et al. Review of research on hookworms (Uncinaria lucasi Stiles, 1901) in northern fur seals (Callorhinus ursinus Linnaeus, 1758). Parasitol Res 109, 257–265 (2011). https://doi.org/10.1007/s00436-011-2420-6

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