Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-11T14:55:17.106Z Has data issue: false hasContentIssue false

Effects of infection with Echinostoma paraensei on the circulating haemocyte population of the host snail Biomphalaria glabrata

Published online by Cambridge University Press:  06 April 2009

S. Noda
Affiliation:
Department of Biology, The University of New Mexico, Albuquerque, New Mexico 87131, USA
E. S. Loker*
Affiliation:
Department of Biology, The University of New Mexico, Albuquerque, New Mexico 87131, USA
*
Reprint requests to Dr E. S. Loker.

Summary

Circulating haemocytes from Echinostoma paraensei-infected M line Biomphalaria glabrata snails, or from age- and sizematched control snails, were studied on plastic slides with phase-contrast optics. Granulocytes, hyalinocytes, and round cells were consistently present; granulocytes were further categorized as ‘fully spread' (FS) or ‘partially spread' (PS). Among control snails, the relative percentage and estimated number/mm3 of round cells declined significantly with increased snail size, and the corresponding values for both categories of granulocytes increased. At 1 day post-infection (p.i.) with E. paraensei, overall composition of the haemocyte population was relatively unaffected, but by 8 days p.i. infected snails had significantly higher relative percentages of round cells and PS granulocytes than controls. Because a marked increase in the number of circulating haemocytes is also evident by 8 days p.i., infected snails had approximately 12 times more round cells and PS granulocytes/mm3 of haemolymph than did controls. At 30 days p.i. the relative and absolute abundance of PS granulocytes was still significantly elevated, but otherwise haemocyte populations did not differ from control snails. Alterations in granulocyte size in infected snails were also noted. Infection with E. paraensei has a striking impact of circulating haemocyte populations and also increases the relative concentration of haemocytes with less ability to adhere to a foreign surface.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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

Abdul-Salam, J. M. & Michelson, E. H. (1980). Biomphalaria glabrata amoebocytes: Effect of Schistosoma mansoni infection on in vitro phagocytosis. Journal of Invertebrate Pathology 35, 241–8.CrossRefGoogle ScholarPubMed
Cheng, T. C. (1975). Functional morphology and biochemistry of molluscan phagocytes. Annals of the New York Academy of Sciences 266, 343–79.CrossRefGoogle ScholarPubMed
Cheng, T. C. & Garrabrant, T. A. (1977). Acid phosphatase in granulocytic capsules formed in strains of Biomphalaria glabrata totally and partially resistant to Schistosoma mansoni. International Journal for Parasitology 7, 467–72.CrossRefGoogle ScholarPubMed
Dikkeboom, R., Van Der Knapp, W. P. W., Meuleman, E. A. & Sminia, T. (1984). Differences between blood cells of juvenile and adult specimens of the pond snail Lymnaea stagnalis. Cell and Tissue Research 238, 43–7.CrossRefGoogle Scholar
Dikkeboom, R., Van Der Knapp, W. P. W., Meuleman, E. A. & Sminia, T. (1985). A comparative study on the internal defense system of juvenile and adult Lymnaea stagnalis. Immunology 55, 547–53.Google ScholarPubMed
Granath, W. O. Jr & Yoshino, T. P. (1983). Lysosomal enzyme activities in susceptible and refractory strains of Biomphalaria glabrata during the course of infection with Schistosoma mansoni. Journal of Parasitology 69, 1018–26.CrossRefGoogle ScholarPubMed
Jeong, K. H., Lie, K. J. & Heyneman, D. (1984). An ultrastructural study on ventricular capsule reactions in Biomphalaria glabrata exposed to irradiated echinostome parasites. International Journal for Parasitology 14, 127–33.CrossRefGoogle Scholar
Lie, K. J. (1982). Survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata. A discussion of the interference hypothesis. Tropical and Geographical Medicine 34, 111–22.Google Scholar
Lie, K. J. & Heyneman, D. (1976). Studies on resistance in snails. 6. Escape of Echinostoma lindoense sporocyst from encapsulation in the snail heart and subsequent loss of the host's ability to resist infection by the same parasite. Journal of Parasitology 62, 292–7.CrossRefGoogle ScholarPubMed
Lie, K. J., Heyneman, D. & Richards, C. S. (1977). Studies on resistance in snails: interference by nonirradiated echinostome larvae with natural resistance to Schistosoma mansoni in Biomphalaria glabrata. Journal of Invertebrate Pathology 29, 118–25.CrossRefGoogle ScholarPubMed
Loker, E. S. & Bayne, C. J. (1986). Immunity to trematode larvae in the snail Biomphalaria. Symposium of the Zoological Society of London 56, 199220.Google Scholar
Loker, E. S., Bayne, C. J. & Yui, M. A. (1986). Echinostoma paraensei: Hemocytes of Biomphalaria glabrata as targets of echinostome mediated interference with host snail resistance to Schistosoma mansoni. Experimental Parasitology 62, 149–54.CrossRefGoogle ScholarPubMed
Loker, E. S., Bayne, C. J., Buckley, P. M. & Kruse, K. T. (1982). Ultrastructure of encapsulation of Schistosoma mansoni mother sporocysts by hemocytes of juveniles of the 10-R2 strain of Biomphalaria glabrata. Journal of Parasitology 68, 8494.CrossRefGoogle ScholarPubMed
Loker, E. S., Cimino, D. F., Stryker, G. A. & Hertel, L. A. (1987). The effect of size of M line Biomphalaria glabrata on the course of development of Echinostoma paraensei. Journal of Parasitology 73, 1090–8.CrossRefGoogle ScholarPubMed
Loker, E. S. & Hertel, L. A. (1987). Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. Journal of Parasitology 73, 503–13.CrossRefGoogle ScholarPubMed
Neter, J. & Wasserman, W. (1974). Applied Linear Statistical Methods. Richard D. Irwin, Homewood, III. 842 pp.Google Scholar
Schoenberg, D. A. & Cheng, T. C. (1981). The behaviour of Biomphalaria glabrata (Gastropoda: Pulmonata) hemocytes following exposure to lectins. Transactions of the American Microscopical Society 100, 345–54.CrossRefGoogle ScholarPubMed
Sminia, T. & Barendsen, L. (1980). A comparative morphological and enzyme histochemical study of blood cells of the freshwater snails Lymnaea stagnalis, Biomphalaria glabrata, and Bulinus truncatus. Journal of Morphology 165, 31–9.CrossRefGoogle ScholarPubMed
Stoltz, D. B. & Guzo, D. (1986). Apparent hemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria larvae. Journal of Insect Physiology 32, 377–88.CrossRefGoogle Scholar
Stumpf, J. L. & Gilbertson, D. E. (1980). Differential leukocytic responses of Biomphalaria glabrata to infection with Schistosoma mansoni. Journal of Invertebrate Pathology 32, 177–81.CrossRefGoogle Scholar
Ulmer, M. J. (1970). Notes on rearing snails in the laboratory. In Experiments and Techniques in Parasitology (ed. MacInnis, A. J. and Voge, M.), pp. 143–4. San Francisco: W. H. Freeman.Google Scholar
Van Der Knaap, W. P. W., Meuleman, E. A. & Sminia, T. (1987). Alterations in the internal defence system of the pond snail Lymnaea stagnalis induced by infection with the schistosome Trichobilharzia ocellata. Parasitology Research 73, 5765.CrossRefGoogle ScholarPubMed
Yoshina, T. O. (1981). Comparison of concanavalin A-reactive determinants on hemocytes of two Biomphalaria glabrata snail stocks: Receptor binding and redistribution. Developmental and Comparative Immunology 5, 229–39.CrossRefGoogle Scholar