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Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy

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Abstract

Trematodes of the genus Alaria develop into an arrested stage, known as mesocercariae, within their amphibian second intermediate host. The mesocercariae are frequently transmitted to a non-obligate paratenic host before reaching a definitive host where further development and reproduction can occur. Snakes are common paratenic hosts for Alaria spp. with the mesocercariae often aggregating in the host’s tail. In the current study, we used morphological examination and molecular analyses based on partial sequences of nuclear large ribosomal subunit gene and mitochondrial cytochrome C oxidase subunit 1 gene to identify larvae in the tails of red-sided garter snakes (Thamnophis sirtalis parietalis) as mesocercariae of Alaria marcianae, Alaria mustelae, and Alaria sp. as well as metacercariae of Diplostomidae sp. of unknown generic affiliation. We assessed infection prevalence, absolute and relative intensity, and associated pathological changes in these snakes. Infection prevalence was 100 % for both male and female snakes. Infection intensity ranged from 11 to more than 2000 mesocercariae per snake tail but did not differ between the sexes. Gross pathological changes included tail swelling while histopathological changes included mild inflammation and the presence of mucus-filled pseudocysts surrounding mesocercariae, as well as the compression and degeneration of muscle fibers. Our results indicate that mesocercariae can lead to extensive muscle damage and loss in both sexes which likely increases the fragility of the tail making it more prone to breakage. As tail loss in garter snakes can affect both survival and reproduction, infection by Alaria mesocercariae clearly has serious fitness implications for these snakes.

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Acknowledgments

We thank Chris Friesen and Ehren Bentz for help in the field and Leslie Blakemore for assistance in the lab. We also thank Manitoba Conservation, particularly Dave Roberts, for assistance with permits. William Font, Don Nichols, and Mike Kinsella provided help with initial genus-level identification of parasites. Don Nichols also shared many useful thoughts on the host–parasite interaction. Chris Friesen, Richard Whittington, and two anonymous reviewers provided insightful comments on earlier versions of this manuscript.

Compliance with Ethical Standards

All procedures utilized in this research were approved by the Oregon State University Animal Care and Use Committee (ACUP no. 4317). This research complied with guidelines established by the National Institutes of Health Guide for the Care and Use of Laboratory Animals and was carried out under the authority of Manitoba Wildlife Scientific Permit WB12405.

Conflict of interest

The authors declare that they have no conflicts of interest.

Financial support

The molecular portion of this study was supported by a National Institutes of Health grant (R15AI092622) awarded to VVT.

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Authors and Affiliations

  1. Department of Integrative Biology, Oregon State University, 3029 Cordley Hall, Corvallis, OR, 97331, USA

    Emily J. Uhrig & Robert T. Mason

  2. Department of Biomedical Sciences, Oregon State University, 106 Dryden Hall, Corvallis, OR, 97331, USA

    Sean T. Spagnoli & Michael L. Kent

  3. Department of Biology, University of North Dakota, 10 Cornell Street, Grand Forks, ND, 58202, USA

    Vasyl V. Tkach

  4. Department of Microbiology, Oregon State University, 220 Nash Hall, Corvallis, OR, 97331, USA

    Michael L. Kent

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  1. Emily J. Uhrig
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Correspondence to Emily J. Uhrig.

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Uhrig, E.J., Spagnoli, S.T., Tkach, V.V. et al. Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy. Parasitol Res 114, 4451–4461 (2015). https://doi.org/10.1007/s00436-015-4686-6

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