Skip to main content
Log in

Morphology and molecular taxonomy of Gyrodactylus jennyae n. sp. (Monogenea) from tadpoles of captive Rana catesbeiana Shaw (Anura), with a review of the species of Gyrodactylus Nordmann, 1832 parasitising amphibians

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Gyrodactylus jennyae n. sp. is described from the body surface and mouthparts of tadpoles of the bullfrog Rana catesbeiana Shaw imported presumably from Missouri, USA, into a federal government facility in Moncton, New Brunswick, Canada. Its morphology resembles most closely that of G. chologastris Mizelle, Whittaker & McDougal, 1969 described from two amblyopsids (blind cave fishes) in Kentucky and North Carolina. Both species have long slender hamuli, a ventral bar with a relatively long membrane and small anterolateral processes, a cirrus with two rows of small spines and marginal hooks with a well-developed sickle heel and short handle. The two species differ morphologically; G. jennyae has a marginal hook sickle with a more pronounced heel than that found in G. chologastris. A BLAST search using a 945 base pair sequence that included the nuclear ribosomal DNA internal transcribed spacers 1 and 2 and the 5.8S rRNA gene from G. jennyae n. sp. showed that the overall similarity with other Gyrodactylus sequences on GenBank was relatively low. The ITS1 region was similar to that of G. misgurni Ling, 1962; however, no ITS2 and 5.8S rRNA sequences are available for that species. A separate search using 5.8S sequences revealed that G. markakulensis Gvosdev, 1950 and G. laevis Malmberg, 1957 were the closest to G. jennyae (1 and 2 bp differences, respectively). These species are parasites of cyprinids (or their predators) and are similar to G. jennyae and G. chologastris in having a double row of small hooks on the cirrus and overall similar morphologies of the haptoral hard parts. There are now five species of Gyrodactylus described exclusively from amphibians and this appears to have involved at least three separate host-switches from fishes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  • Andrews, K. D., Lampley, R. L., Gillman, M. A., Corey, D. T., Ballard, S. R., Blasczyk, M. J., et al. (1992). Helminths of Rana catesbeiana in southern Illinois with a checklist of helminths in bullfrogs of North America. Transactions of the Illinois State Academy of Sciences, 85, 147–172.

    Google Scholar 

  • Bakke, T. A., Cable, J., & Harris, P. D. (2007). The biology of gyrodactylid monogeneans: The “Russian-doll killers”. Advances in Parasitology, 64, 161–376.

    Article  PubMed  CAS  Google Scholar 

  • Bakke, T. A., Harris, P. D., & Cable, J. (2002). Host specificity dynamics: Observations on gyrodactylid monogeneans. International Journal for Parasitology, 31, 281–308.

    Article  Google Scholar 

  • Barber, I. (2007). Parasites, behaviour and welfare in fish. Applied Animal Behaviour Science, 104, 251–264.

    Article  Google Scholar 

  • Cable, J., Harris, P. D., & Tinsley, R. C. (1997). Melanin deposition in the gut of the monogenean Macrodactylus polypteri Malmberg 1957. International Journal for Parasitology, 27, 1323–1331.

    Article  PubMed  CAS  Google Scholar 

  • Cone, D. K., & Dechtiar, A. O. (1984). Gyrodactylus fryi n sp. (Monogenea) from Esox masquinongy Mitchill in Ontario. Canadian Journal of Zoology, 62, 1089–1090.

    Article  Google Scholar 

  • Crawshaw, G. J. (1997). Disease in Canadian amphibian populations. Herpetological Conservation, 1, 258–270.

    Google Scholar 

  • Dodd, K. C. Jr., Gunzburger, M. S., Barichivich, W. J., & Staiger, J. S. (2004). Southeast amphibian research and monitoring initiative (National Wildlife Refuges Summary Report for 2004). United States Geological Survey. Gainsville, FL: Florida Integrated Science Center. http://armi.usgs.gov/SEARMI2004Report.pdf.

  • Geets, A., Appleby, C., & Ollivier, F. (1999). Host-dependent and seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from Gasterosteus arculeatus: A multivariate approach. Parasitology, 119, 27–40.

    Article  PubMed  Google Scholar 

  • Green, D. E., & Dodd, C. K., Jr. (2007). Presence of amphibian chytrid fungus Batrachochytrium dendrobatidis and other amphibian pathogens at warm-water fish hatcheries in southeastern North America. Herpetological Conservation and Biology, 2, 43–47.

    Google Scholar 

  • Gunzburger, M. S., Dodd, C. K. Jr., Barichivich, W. J., & Staiger, J. S. (2005). Southeast amphibian research and monitoring initiative (2005 Annual Report). United States Geological Survey. Gainsville, FL: Florida Integrated Science Center. http://fl.biology.usgs.gov/armi/2005_Annual_Report/2005_annual_report.html.

  • Herman, C. A. (1992). Endocrinology. In M. E. Feder & W. W. Burggren (Eds.), Environmental physiology of the amphibians (pp. 40–54). Chicago: University of Chicago Press.

    Google Scholar 

  • Huyse, T., Audenaert, V., & Volckaert, F. A. M. (2003). Speciation and host–parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). International Journal for Parasitology, 33, 1679–1689.

    Article  PubMed  Google Scholar 

  • Leblanc, J., Hansen, H., Burt, M., & Cone, D. (2006). Gyrodactylus neili n. sp. (Monogenea: Gyrodactylidae), a parasite of chain pickerel Esox niger Lesueur (Esocidae) from freshwaters of New Brunswick, Canada. Systematic Parasitology, 65, 43–48.

    Article  PubMed  Google Scholar 

  • Malmberg, G. (1970). The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv För Zoologie, 23, 1–237.

    Google Scholar 

  • Malmberg, G. (1993). Gyrodactilidae et gyrodactylose des salmonidae. Bulletin Français de la Pêche et de la Pisciculture, 328, 5–46.

    Article  Google Scholar 

  • Matějusová, I., Gelnar, M., McBeath, A. J. A., Collins, C. M., & Cunningham, C. O. (2001). Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology, 31, 738–745.

    Article  PubMed  Google Scholar 

  • Mizelle, J. D., Kritsky, D. C., & Bury, R. B. (1968). Studies on the monogenetic trematodes. XLI. Gyrodactylus ensatus sp. n., the first species of the genus described from Amphibia. Journal of Parasitology, 54, 281–282.

    Article  PubMed  CAS  Google Scholar 

  • Mizelle, J. D., Kritsky, D. C., & McDougal, H. D. (1969). Studies on monogenetic trematodes. XLII. New species of Gyrodactylus from Amphibia. Journal of Parasitology, 55, 740–741.

    Article  Google Scholar 

  • Nieto, N. C., Camann, M. A., Foley, J. E., & Reiss, J. O. (2007). Disease associated with integumentary and cloacal parasites in tadpoles of northern red-legged frog Rana aurora aurora. Diseases of Aquatic Organisms, 78, 61–71.

    Article  PubMed  Google Scholar 

  • Prudhoe, S., & Bray, R. A. (1982). Platyhelminth parasites of the Amphibia. Oxford: Oxford University Press, 217 pp.

    Google Scholar 

  • Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L., et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783–1786.

    Article  PubMed  CAS  Google Scholar 

  • Stunkard, H. W., & Dunihue, F. W. (1933). Gyrodactylus as a parasite of the tadpoles of Rana catesbeiana. Journal of Parasitology, 20, 137.

    Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • Vojtkova, L. (1989). The occurrence of the representatives of the class Monogenea in amphibians in Europe. Scripta Facultatis Scientarium Naturalium Universitatis Purkynianae Brunensis, 19, 331–338.

    Google Scholar 

  • Volgar-Pastukhova, L. G. (1959). Parasitic fauna of the Anura in the Danube delta. In Y. I. Polyanksy (Ed.), Ecological parasitology (pp. 58–95). Leningrad: Leningradskogo Universiteta. (In Russian).

    Google Scholar 

  • Wootton, D. M., Ryan, K. A., Demaree, R. S., & Critchfield, R. L. (1993). A new species of Gyrodactylus (Monogenea: Monopisthocotylea) on tadpoles of Rana catesbeiana from California, U.S.A. Transactions of the American Microscopical Society, 112, 230–233.

    Article  Google Scholar 

  • You, P., Easy, R. H., & Cone, D. K. (2008). Gyrodactylus parvae n. sp. (Monogenea) from the fins and body surface of Pseudorasbora parva (Cyprinidae) in central China. Comparative Parasitology, 75, 28–32.

    Article  Google Scholar 

  • Ziętara, M., Huyse, T., Lumme, J., & Volckaert, F. A. M. (2002). Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology, 124, 39–52.

    PubMed  Google Scholar 

  • Ziętara, M. S., & Lumme, J. (2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution, 56, 2445–2458.

    PubMed  Google Scholar 

  • Zug, G. R. (1993). Herpetology: An introductory biology of amphibians and reptiles. San Diego, California: Academic Press, 527 pp.

    Google Scholar 

Download references

Acknowledgements

This work was partly funded by the Natural Science and Engineering Research Council of Canada through Discovery Grants awarded to D.K.C. and J.D.M., an NSERC Postgraduate Scholarship (PGS M) awarded to L.P., and funds from the Pesticide Science Fund (PSF, Environment Canada) to D.J.M. and Bruce Pauli. T.H. is funded through a postdoctoral grant of the Research Foundation—Flanders (FWO-Vlaanderen). The authors thank Dr Eric Hoberg for arranging loan of museum material, Dr David E. Green for sharing field data and Dr Rodney Bray for sharing records. Ken Doe and Paula Jackman (Environment Canada) are gratefully acknowledged for providing the tadpoles, as is Bruce Pauli (Environment Canada) for coordinating the PSF project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David J. Marcogliese.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paetow, L., Cone, D.K., Huyse, T. et al. Morphology and molecular taxonomy of Gyrodactylus jennyae n. sp. (Monogenea) from tadpoles of captive Rana catesbeiana Shaw (Anura), with a review of the species of Gyrodactylus Nordmann, 1832 parasitising amphibians. Syst Parasitol 73, 219–227 (2009). https://doi.org/10.1007/s11230-009-9183-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-009-9183-9

Keywords

Navigation