Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-28T15:31:25.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Migration and site selection of Ornithodiplostomum ptychocheilus (Trematoda: Digenea) metacercariae in the brain of fathead minnows (Pimephales promelas)

Published online by Cambridge University Press:  07 December 2009

CHELSEA E. MATISZ ,
CAMERON P. GOATER  and
DOUGLAS BRAY
CHELSEA E. MATISZ*
Affiliation:
Department of Biological Sciences, University of Lethbridge, 4401 University Drive, Lethbridge, Alberta, CanadaT1K 3M4
CAMERON P. GOATER
Affiliation:
Department of Biological Sciences, University of Lethbridge, 4401 University Drive, Lethbridge, Alberta, CanadaT1K 3M4
DOUGLAS BRAY
Affiliation:
Department of Biological Sciences, University of Lethbridge, 4401 University Drive, Lethbridge, Alberta, CanadaT1K 3M4
*
*Corresponding author: Tel: +403 329 2319. Fax: +403 329 2082. E-mail: chelsea.matisz@uleth.ca
Get access Rights & Permissions [Opens in a new window]

Summary

The migration of subadult parasites to preferred sites within final hosts is well characterized. In contrast, the migration of larval stages of trematodes to specific sites within their second intermediate hosts is poorly understood. We used a serial necropsy approach to characterize the migration of Ornithodiplostomum ptychocheilus diplostomules from the point of cercarial penetration, to encystment within the outermost tissues of the brain of fathead minnows. Diplostomules utilized peripheral nerves to access the central nerve cord, or they used specific cranial nerves to directly access the brain. Within 3 h of exposure to cercariae, 46% of all diplostomules were observed within the medulla of the brain. Diplostomules subsequently utilized specific neural tracts to reach lateral regions of the outermost tissue layer of the optic lobes, the stratum marginale. Diplostomules remained in this layer during their 4-week growth phase, then shifted site to the adjacent meninges for encystment. Characterization of a habitat shift for developing versus encysted metacercariae helps explain the results of previous ecological studies that document transient changes in the effects of metacercariae on the surivival, behaviour, and anti-parasite defences of infected fish.

Keywords

Strigeoid trematodeparasite navigationparasite migrationmeningesoptic lobescerebellumhabitat shift
Type
Research Article
Information
Parasitology , Volume 137 , Issue 4 , April 2010 , pp. 719 - 731
Copyright
Copyright © Cambridge University Press 2009

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

Ballabeni, P. and Ward, P. I. (1993). Local adaptation of the trematode Diplostomum phoxini to the European minnow Phoxini phoxinus, its second intermediate host. Functional Ecology 7, 84–90.Google Scholar
Barber, I. and Crompton, D. W. T. (1997). The distribution of the metacercariae of Diplostomum phoxini in the brain of minnows, Phoxinus phoxinus. Folia Parasitologica 4, 19–25.Google Scholar
Bush, A. O., Fernandez, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
Conn, D. B., Goater, C. P. and Bray, D. (2008). Developmental and functional ultrastructure of Ornithodiplostomum ptychocheilus diplostomula (Trematoda: Strigeoidea) during invasion of the brain of the fish intermediate host, Pimephales promelas. Journal of Parasitology 94, 635–642. DOI: 10.1645/GE-1421.1Google Scholar
Erasmus, D. A. (1972). The Biology of Trematodes. Edward Arnold Limited, London, UK.Google Scholar
Goater, C. P., Bray, D. and Conn, D. B. (2005). Cellular aspects of early development of Ornithsodiplostomum ptychocheilus metacercariae in the brain of fathead minnows, Pimephales promelas. Journal of Parasitology 91, 814–821.Google Scholar
Haas, W., Wulff, C., Grabe, K., Meyer, V. and Haeberlein, S. (2007). Navigation within host tissues: cues for orientation of Diplostomum spathaceum (Trematoda) in fish towards veins, head, and eye. Parasitology 134, 1013–1023. DOI:10.1017/S0031182007002430Google Scholar
Hendrickson, G. L. (1979). Ornithodiplostomum ptychocheilus: migration to the brain of the fish intermediate host, Pimephales promelas. Experimental Parasitology 48, 245–258.Google Scholar
Hoffman, G. L. and Hoyme, J. B. (1958). The experimental histopathology of the tumor on the brain of the stickleback caused by Diplostomum baeri eucaliae Hoffman and Hundley, 1957 (Trematoda: Strigeoidea). Journal of Parasitology 44, 374–378.CrossRefGoogle Scholar
Hoglund, J. (1991). Ultrastructural observations and radiometric assay on cercarial penetration and migration of the digenean Diplostomum spathaceum in the rainbow trout Oncorhynchus mykiss. Parasitology Research 77, 283–289.CrossRefGoogle Scholar
James, C. T., Noyes, K. J., Stumbo, A. D., Wisendon, B. D. and Goater, C. P. (2008). Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnows, Pimephales promelas. Journal of Fish Biology 73, 2238–2248. doi: 10.1111/j.1095-8649.2008.02052.xGoogle Scholar
Johnson, K. A. (1971). The migration of Cotylurus erraticus cercariae (Trematoda: Strigeidae) in rainbow trout (Salmo gairdneri) and their effects on the host. Journal of Parasitology 57, 244–251.Google Scholar
Matisz, C. E., Goater, C. P. and Bray, D. (2009). Density and maturation of rodlet cells in brain tissue of fathead minnows (Pimephales promelas) exposed to trematode cercariae. International Journal of Parasitology (in the Press). doi:10.1016/j.ijpara.2009.08.013Google Scholar
Momose, Y., Kohno, K. and Ito, R. (1988). Ultrastructural study on the meninx of the goldfish brain. Journal of Comparative Neurology 270, 327–336.CrossRefGoogle Scholar
Radabaugh, D. C. (1980). Encystment site selection in the brain-inhabiting metacercariae of Ornithodiplostomum ptychocheilus (Trematoda: Strigeoidea). Journal of Parasitology 66, 183–184.CrossRefGoogle Scholar
Roberts, L., Javony, J. and Schmidt, P. (2004). Foundations of Parasitology. 7th Edn.McGraw-Hill Companies, Inc., New York, USA.Google Scholar
Sandland, G. J. and Goater, C. P. (2000). Development and intensity of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 1056–1060. doi: 10.1645/0022-3395CrossRefGoogle ScholarPubMed
Sandland, G. J. and Goater, C. P. (2001). Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows. Journal of Parasitology 87, 267–272.Google Scholar
Schwartz, H., Muller-Schmid, A. and Hoffman, W. (1993). Ultrastructural localization of ependymins in the endomeninx of the brain of the rainbow trout: possible association with collagen fibrils of the extracellular matrix. Cell and Tissue Research 273, 417–425.Google Scholar
Shirakashi, S. and Goater, C. P. (2005). Chronology of parasite-induced alteration of fish behavior: effects of parasite maturation and host experience. Parasitology 130, 1–7.Google Scholar
So, F. W. and Wittrock, D. D. (1982). Ultrastructure of the metacercarial cyst of Ornithodiplostomum ptychocheilus (Trematoda: Diplostomidae) from the brains of fathead minnows. Transactions of the American Microscopical Society 10, 181–185.Google Scholar
Speare, D. and Frasca, S. (2006). Nervous system. In (ed. Ferguson, H.), Systemic Pathology of Fish: A Text and Atlas of Normal Tissues in Teleosts and their Responses to Disease. Scotian Press London, UK.Google Scholar
Sukhdeo, M. V. K. and Sukhdeo, S. C. (1994). Optimal habitat selection by helminthes within the host environment. Parasitology 109, S1–S55.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. and Sukhdeo, S. C. (2004). Trematode behaviours and the perceptual worlds of parasites. Canadian Journal of Zoology 82, 292–315.Google Scholar
Williams, M. O. (1966). Studies on the morphology and life cycle of Diplostomum gasterostei (Strigeida: Trematoda). Parasitology 56, 693–706.Google Scholar
Wilson, P. A. G. (1994). Doubt and certainty about the pathways of invasive juvenile parasites inside hosts. Parasitology 109, S57–S67.Google Scholar
Wullimann, M. F., Rupp, B. and Reichert, H. (1996). Neuroanatomy of the Zebrafish Brain: A Topological Atlas. Birkhäuser, Basel, Switzerland.Google Scholar