Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-27T22:38:02.091Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the haemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility

Published online by Cambridge University Press:  30 March 2012

I.A. Levakin ,
E.A. Losev ,
K.E. Nikolaev  and
K.V. Galaktionov
I.A. Levakin
Affiliation:
The Laboratory of Parasitic Worms, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
E.A. Losev
Affiliation:
Department of Invertebrate Zoology, St. Petersburg State University, St. Petersburg 199034, Russia
K.E. Nikolaev
Affiliation:
The White Sea Biological Station, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
K.V. Galaktionov*
Affiliation:
Department of Invertebrate Zoology, St. Petersburg State University, St. Petersburg 199034, Russia The White Sea Biological Station, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
*
* E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Infectivity of Himasthla elongata cercariae to mussels, their second intermediate hosts, and resistance by these hosts to infection were assessed on the basis of the cercariae's ability to encyst in mussel haemolymph in vitro. A series of experimental in vivo infections of mussels with batches of cercariae, each batch released from a different single infected mollusc and referred to as a clone (due to their shared genotype), demonstrated that the results of the in vitro tests corresponded to the actual indices of infectivity/susceptibility of the parasites and their hosts. Most cercarial clones had high infectivity, with a few clones having very high or, at the other extreme, very low infectivity. A similar pattern was revealed in mussel resistance to cercarial infection. Most of the molluscs tested were moderately susceptible to cercarial infection, but at each extreme a small fraction (less than 10%) displayed very high or very low susceptibility. It was shown that there were no totally compatible or totally incompatible ‘cercaria clone/mussel’ combinations. Results obtained are compared with the data on intra-population variability using the characters parasite infectivity/host compatibility for trematode/mollusc–first intermediate host associations. Results are made relevant to actual infection levels in mussel settlements at the White Sea.

Type
Research Papers
Information
Journal of Helminthology , Volume 87 , Issue 2 , June 2013 , pp. 180 - 188
Copyright
Copyright © Cambridge University Press 2012 

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

Adema, C.M. & Loker, E.S. (1997) Specificity of digenean–mollusc association. pp. 229–263in Fried, B. & Graczyk, T.K. (Eds) Advances in trematode biology. Boca Raton, CRC Press.Google Scholar
DeGaffé, G. & Loker, E.S. (1998) Susceptibility of Biomphalaria glabrata infection with Echinostoma paraensei: correlation with the effect of parasite secretory–excretory products on host hemocyte spreading. Journal of Invertebrate Pathology 71, 64–72.CrossRefGoogle ScholarPubMed
Dobrovolskij, A.A. & Ataev, G.L. (2003) The nature of reproduction of trematodes rediae and sporocysts. pp. 273–290in Combes, C. & Jourdane, J. (Eds) Hommage à Louis Euzet — taxonomy, ecology, and evolution of metazoan parasites, vol. 1. Perpignan, Presses Universitaires de Perpignan.Google Scholar
Fried, B. & LaTerra, R. (2002) In vitro and in vivo encystment of the cercariae of Echinostoma caproni. Journal of Parasitology 88, 1124–1129.CrossRefGoogle ScholarPubMed
Galaktionov, N.K., Solovieva, A.I., Fedorov, A.V. & Podgornaya, O.I. (2010) DNA transposon mariner evolvement in Himasthla elongata clonal variation. pp. 24–25in 14th Evolutionary Biology Meeting in Marseille, September 21–24. Conference Abstract Book. Marsielle.Google Scholar
Gorbushin, A.M. & Levakin, I.A. (2005) Encystment in vitro of the cercariae Himasthla elongata (Trematoda: Echinostomatidae). Journal of Evolutionary Biochemistry and Physiology 41, 428–436.CrossRefGoogle Scholar
Grosholz, E.D. (1994) The effects of host genotype and spatial distribution on trematode parasitism in a bivalve population. Evolution 48, 1514–1524.CrossRefGoogle Scholar
Gutiérrez, A., Pointier, J.P., Fraga, J., Jobet, E., Modat, S., Perez, R.T., Yong, M., Sanchez, J., Loker, E.S. & Théron, A. (2003) Fasciola hepatica: identification of molecular markers for resistant and susceptible Pseudosuccinea columella snail hosts. Experimental Parasitology 105, 211–218.CrossRefGoogle ScholarPubMed
Humbert, E. & Coustau, C. (2001) Refractoriness of host haemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrata–Echinostoma caproni system. Parasitology 122, 651–660.CrossRefGoogle ScholarPubMed
Keeler, S.P. & Huffman, J.E. (2009) Echinostomes in the second intermediate host. pp. 61–87in Fried, B. & Toledo, R. (Eds) The biology of echinostomes. New York, Springer.CrossRefGoogle Scholar
Koehler, A.V., Springer, Y.P., Keeney, D.B. & Poulin, R. (2011) Intra- and interclonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis. Biological Journal of Linnaean Society 103, 106–116.CrossRefGoogle Scholar
Lauckner, G. (1983) Diseases of Mollusca: Bivalvia. pp. 477–961in Kinne, O. (Ed.) Diseases of marine animals, vol. 2. Hamburg, Biologische Anstalt Helgoland.Google Scholar
Lively, C.M. (1989) Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43, 1663–1671.CrossRefGoogle ScholarPubMed
Lively, C.M. & Dybdahl, M.F. (2000) Parasite adaptation to locally common host genotypes. Nature 405, 679–681.CrossRefGoogle ScholarPubMed
Loos-Frank, B. (1967) Experimentelle Untersuchungen über Bau, Entwicklungen und Systematik der Himasthline (Trematoda, Echinostomatidae) des Nordenseeraumes. Zeitschrift für Parasitenkunde 28, 299–351.CrossRefGoogle Scholar
Manning, S.D., Woolhouse, M.E.J. & Ndamba, J. (1995) Geographic compatibility of the freshwater snail Bulinus globosus and schistosomes from the Zimbabwe Highveld. International Journal for Parasitology 25, 37–42.CrossRefGoogle ScholarPubMed
Morand, S., Manning, S.D. & Woolhouse, M.E. (1996) Parasite–host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proceedings of the Royal Society of London B 263, 119–128.Google Scholar
Nikolaev, K.E. (2012) Patterns in transmission of the life cycles of trematodes of the families Echinostomatidae and Renicolidae in intertidal ecosystems of the Kandalaksha Bay of the White Sea. PhD thesis, Zoological Institute of the Russian Academy of Sciences, St. Petersburg (in Russian).Google Scholar
Nikolaev, K.E., Sukhotin, A.A. & Galaktionov, K.V. (2006) Patterns in infection of the White Sea blue mussels (Mytilus edulis L.) of different age and size with metacercariae of digenetic trematodes Himasthla elongata (Mehlis, 1831) (Echinostomatidae) and Cercaria parvicaudata Stunkard, Shaw, 1931 (Renicolidae). Diseases of Aquatic Organisms 71, 51–58.CrossRefGoogle Scholar
Prokofiev, V.V. (2006) Strategies of the animal hosts infection with trematode cercariae: an attempt of analysis in marine coastal and lake ecosystems of northwestern Russia. Doctorate of Biological Science Dissertation, Zoological Institute of the Russian Academy of Sciences, St. Petersburg (in Russian).Google Scholar
Prokofiev, V.V., Levakin, I.A., Losev, E.A., Zavirsky, Ya.V. & Galaktionov, K.V. (2011) Clonal variability in expression of geo- and photoorientation in cercariae of Himasthla elongata (Trematoda: Echinostomatidae). Parazitologiya 45, 345–357(in Russian, English summary).Google Scholar
Richards, C.S. (1975) Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 70, 231–241.CrossRefGoogle ScholarPubMed
Richards, C.S. & Shade, P.C. (1987) The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. Journal of Parasitology 73, 1146–1151.CrossRefGoogle ScholarPubMed
Richards, C.S., Knight, M. & Lewis, F.A. (1992) Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitology Today 8, 171–174.CrossRefGoogle ScholarPubMed
Shiff, C.J. (1994) Molluscan defence mechanisms: immunity or population biology? Parasitology Today 10, 188–190.CrossRefGoogle ScholarPubMed
Sokal, R.R. & Rohlf, F.J. (1995) Biometry. 3rd edn.887 pp. New York, W.H. Freeman.Google Scholar
Théron, A. & Coustau, C. (2005) Are Biomphalaria snails resistant to Schistosoma mansoni? Journal of Helminthology 79, 187–191.CrossRefGoogle ScholarPubMed
Théron, A., Coustau, C., Rognon, A., Gourbiere, S. & Blouin, M.S. (2008) Effects of laboratory culture on compatibility between snails and schistosomes. Parasitology 135, 1179–1188.CrossRefGoogle ScholarPubMed
Toledo, R. & Fried, B. (Eds) (2011) Biomphalaria snails and trematodes. 244 pp. New York, Springer.CrossRefGoogle Scholar
Webster, J.P. & Davies, C.M. (2001) Coevolution and compatibility in the snail–schistosome system. Parasitology 123, S41–S56.CrossRefGoogle ScholarPubMed
Webster, J.P. & Woolhouse, M.E.J. (1998) Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution 52, 1627–1634.CrossRefGoogle ScholarPubMed
Webster, J.P., Gower, C.M. & Blair, L. (2004) Do hosts and parasites coevolve? Empirical support from the Schistosoma system. The American Naturalist 164, S33–S51.CrossRefGoogle ScholarPubMed
Werding, B. (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3, 306–333.CrossRefGoogle Scholar
Yoshino, T.P. & Coustau, Ch. (2011) Immunobiology of Biomphalaria–trematode interactions. pp. 159–189in Toledo, R. & Fried, B. (Eds) Biomphalaria snails and trematodes. New York, Springer.CrossRefGoogle Scholar
Zaytszeva, M.A. (2006) Peculiarities of interrelationships in the host–parasite systems formed by trematodes and their molluscan hosts. MSc Thesis, St. Petersburg State University, St. Petersburg (in Russian).Google Scholar