Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-18T11:19:42.048Z Has data issue: false hasContentIssue false

Thermal preferences of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to schistosoma mansoni (Trematoda)

Published online by Cambridge University Press:  06 April 2009

H. Lefcort
Affiliation:
Department of Zoology, Oregon State University, Corvallis, OR 97331, USA
C. J. Bayne
Affiliation:
Department of Zoology, Oregon State University, Corvallis, OR 97331, USA

Extract

The thermal preferences of two strains of the snail Biomphalaria glabrata, one resistant to, and one susceptible to, the parasite Schistosoma mansoni were determined in an aquatic thermal gradient. Snails were tested without exposure to the parasite, and 2 h and 5 weeks after exposure to trematode miracidia. The mean temperature selected by susceptible strain snails 2 h post-exposure tended to be lower than that of unexposed controls, although this was not statistically significant. In this strain, at 5 weeks post-exposure, the preferred temperature dropped by 1.9±0.5°C. The resistant strain displayed a significant drop of 1.8±0.6°C 2 h post-exposure. These results are consistent with the hypothesis that a drop in mean temperatures selected by snails is due to altered levels of endogenous cytokines such as IL-1 or TNF in association with parasite activation of the snail internal defense system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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

Atkins, E. (1982). Fever: its history, cause, and function. Yale Journal of Biological Medicine 55, 283–9.Google ScholarPubMed
Bayne, C. J. (1983). Molluscan immunobiology. In Biology Of The Mollusca. Vol. 5, Physiology Pt. 2 (ed. Saleuddin, A. S. M. & Wilbur, K. M.), pp. 407486. San Diego: Academic Press.Google Scholar
Besedovsky, H., Del Rey, A., Sorkin, E. & Dinarello, C. H. (1986). Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science 233, 652–4.CrossRefGoogle ScholarPubMed
Blankespoor, H. D., Babiker, S. M. & Blankespoor, C. L. (1989). Influence of temperature on the development of Schistosoma haematobium in Bulinus truncatus. Journal of Medical and Applied Malacology 1, 123–31.Google Scholar
Chernin, E. (1967). Behavior of Biomphalaria glabrata and of other snails in a thermal gradient. Journal of Parasitology 53, 1233–40.CrossRefGoogle Scholar
Dinarello, C. A. (1984). Interleukin-1 and the pathogenesis of the acute-phase response. New England Journal of Medicine 311, 1413–18.Google ScholarPubMed
Dinarello, C. A., Cannon, J. G., Wolff, S. M., Bernheim, H. A. & Beutler, B. (1986). Tumor necrosis factor (cachectin) is an endogenous pyrogen and induces production of interleukin 1. Journal of Experimental Medicine 163, 1433–50.CrossRefGoogle ScholarPubMed
Eiger, S. M. & Kluger, M. J. (1985). Cyanate and temperature regulation in anephric rabbits. American Journal of Physiology 249, F69–F73.Google ScholarPubMed
Fryer, S. E., DYKES-Hoberg, M. & Bayne, C. J. (1989). Changes in plasma opsonization of yeast after isolation of Biomphalaria glabrata in small volumes of water. Journal of Invertebrate Pathology 54, 275–6.CrossRefGoogle ScholarPubMed
Fryer, S. E. & Bayne, C. J. (1990). Schistosoma mansoni modulation of phagocytosis in Biomphalaria glabrata. Journal of Parasitology 76, 4252.CrossRefGoogle ScholarPubMed
Hughes, K. JR., Smith, E. M., Chin, R., Cadet, P., Sinisterra, J., Leung, M. K., Shipp, M. A., Scharrer, B. & Stefano, G. B. (1990). Interaction of immunoactive monokines (interleukin 1 and tumor necrosis factor) in the bivalve mollusc Mytilus edulis. Proceedings of the National Academy of Sciences, USA 87, 4426–9.CrossRefGoogle ScholarPubMed
Hurst, C. T. & Walker, C. R. (1935). Increased heat production in a poikilothermous animal in parasitism. American Naturalist 69, 461–6.CrossRefGoogle Scholar
Kluger, M. J. (1979). Phylogeny of fever. Federation Proceedings 38, 30–4.Google ScholarPubMed
Kluger, M. J. (1991). Fever: role of pyrogens and cryogens. Physiological Reviews 71, 93127.CrossRefGoogle ScholarPubMed
Kluger, M. J., Turnbull, A. J., Cranston, W. I., Wing, A. J., Gross, M. P. & Rothenburg, B. A. (1981). Endogenous cryogen secreted by the kidneys. American Journal of Physiology 281, R271–R276.Google Scholar
Kluger, M. J., Conn, C. A., Franklin, B., Freter, R. & Abrams, G. D. (1990). Effects of gastrointestinal flora on body temperature of rats and mice. American Journal of Physiology 258, R552–R557.Google ScholarPubMed
Lee, O. F. & Cheng, T. C. (1971). Schistosoma mansoni infection in Biomphalaria glabrata: alterations in heart rate and thermal tolerance of the host. Journal of Invertebrate Pathology 18, 412–18.CrossRefGoogle ScholarPubMed
Lemay, L. G., Vander, A. J. & Kluger, M. J. (1990) The effects of psychological stress on plasma interleukin-6 activity in rats. Physiology and Behavior 47, 957–61.CrossRefGoogle ScholarPubMed
Lillywhite, H. B., Licht, P. & Chelgren, P. (1973). The role of behavioral thermoregulation in the growth energetics of the toad Bufo boreas. Ecology 52, 375–83.CrossRefGoogle Scholar
Loker, E. S. (1979). Pathology and host responses induced by Schistosomatium douthitti in the freshwater snail Lymnaea catascopium. Journal of Invertebrate Pathology 33, 265–73.CrossRefGoogle ScholarPubMed
Long, N. C., Vander, A. J., Kunkel, S. L. & Kluger, M. J. (1990 a). Antiserum against tumor necrosis factor increases stress hyperthermia in rats. American Journal of Physiology 258, R591–R595.Google ScholarPubMed
Long, N. C., Otterness, I., Kunkel, S. L., Vander, A. J. & Kluger, M. J. (1990 b). Roles of interleukin 1B and tumor necrosis factor in lipopolysaccharide fever in rats. American Journal of Physiology 259, R724–R728.Google Scholar
Pan, C. (1963). Generalized and focal tissue response in the snail, Australorbus glabratus, infected with Schistosoma mansoni. Annals of the New York Academy of Sciences 113, 475–85.CrossRefGoogle ScholarPubMed
Pan, C. (1965). Studies on the host–parasite relationship between Schistosoma mansoni and the snail Australorbus glabratus. American Journal of Tropical Medicine and Hygiene 14, 931–76.CrossRefGoogle ScholarPubMed
Regal, P. M. (1966). Thermophilic responses following feeding in certain reptiles. Copeia 1966, 588–90.CrossRefGoogle Scholar
Shiff, C. J. (1964). Studies on Bulinus (Physopsis) globosus in Rhodesia. 1. The influence of temperature on the intrinsic rate of natural increase. Annals of Tropical Medicine and Parasitology 58, 94105.CrossRefGoogle Scholar
Shiff, C. J. & Husting, E. L. (1966). An application of the concept of intrinsic rate of natural increase to studies on the ecology of freshwater snails of the genera Biomphalaria and Bulinus (Physopsis). Proceedings and Transactions of the Rhodesian Science Association 51, 28.Google Scholar
Sodeman, W. A. JR. & Dowda, M. C. (1974). Behavioral responses of Biomphalaria glabrata. Physiological Zoology 47, 198206.CrossRefGoogle Scholar
Standen, O. D. (1952). Experimental infection of Australorbis glabratus with Schistosoma mansoni. I. Individual and mass infection of snails, and the relationship of infection to temperature and season. Annals of Tropical Medicine and Parasitology 46, 4853.CrossRefGoogle ScholarPubMed
Stibbs, H. H., Owczarzak, A., Bayne, C. J. & Dewan, P. C. (1979). Schistosome sporocyst-killing amebae isolated from Biomphalaria glabrata. Journal of Invertebrate Pathology 33, 159–70.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1954). Effect of maintenance temperatures on development of Schistosoma mansoni. Experimental Parasitology 3, 504–16.CrossRefGoogle ScholarPubMed
Sturrock, B. M. & Sturrock, R. F. (1970). Laboratory studies of the host–parasite relationship of Schistosoma mansoni and Biomphalaria glabrata from St Lucia, West Indies. Annals of Tropical Medicine and Parasitology 64, 357.CrossRefGoogle ScholarPubMed
Sturrock, R. F. & Sturrock, B. M. (1971). Shell abnormalities in Biomphalaria glabrata infected with Schistosoma mansoni and their significance in field transmission studies. Journal of Helminthology 45, 201–10.CrossRefGoogle ScholarPubMed
Sturrock, R. F. & Sturrock, B. M. (1972). The influence of temperature on the biology of Biomphalaria glabrata (Say), intermediate host of Schistosoma mansoni on St Lucia, West Indies. Annals of Tropical Medicine and Parasitology 66, 385–90.CrossRefGoogle Scholar
Van Der Knaap, W. P. W. & Loker, E. S. (1990). Immune mechanisms in trematode–snail interactions. Parasitology Today 6, 175–82.CrossRefGoogle ScholarPubMed
Webbe, G. & James, C. (1972). Host–parasite relationships of Bulinus globosus and B. truncatus with strains of Schistosoma haematobium. Journal of Helminthology 46, 185–99.CrossRefGoogle Scholar