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Behavioural adaptation of the tapeworm Hymenolepis diminuta to its environment

Published online by Cambridge University Press:  06 April 2009

M. V. K. Sukhdeo
Affiliation:
Department of Animal Sciences, Rutgers University, New Brunswick, New Jersey 08903, USA
M. S. Kerr
Affiliation:
Department of Preventive Medicine, University of Toronto, Toronto, Ontario, M5S 1A1, Canada

Summary

Hymenolepis diminuta migrates up the small intestine in response to feeding the host 1 g of glucose. Locomotion during migration may result from fixed patterns of retrograde peristaltic-like waves in the strobila of the tapeworm which propel the organism against the normal expulsive forces in the small intestine. The peristaltic-like locomotory waves occur in a gradient along the strobila with a frequency of 24·9±0·9 cycles/min in the anterior segments of the worm, decreasing linearly to 6·6±1·4 cycles/min in the posterior segments of the worm. Chemical signals, isolated from the small intestine of fed hosts, which stimulate migration behaviour in vivo do not alter the behaviour of the scolex or strobila in vitro. Removal of the scolex containing the cerebral ganglia does not alter the frequency or pattern of locomotory activity in the strobila. After the worm is cut into pieces, each region generates the pattern of locomotory activity that is appropriate for that region. These data suggest that the peripheral nervous system, and not the central nervous system, is responsible for the coordination of the fixed patterns of locomotory activity in these tapeworms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Alcock, J. (1979). Animal Behaviour: an Evolutionary Approach. Sunderland: Sinauer Associates Inc.Google Scholar
Al-Saffar, A. (1984). Analysis of the control of intestinal motility in fasted rats with special reference to neurotensin. Scandinavian Journal of Gastroenterology 19, 422–8.CrossRefGoogle ScholarPubMed
Al-Saffar, A., Hellstrom, P. M., Nylander, G. & Rosell, S. (1984). Influence of fasting and bombesin-induced myoelectric activity on the transit of small-intestinal contents in the rat. Scandinavian Journal of Gastroenterology 19, 541–6.CrossRefGoogle ScholarPubMed
Arai, H. P. (1980). Migratory activity and related phenomena in Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 615632. New York: Academic Press.CrossRefGoogle Scholar
Arms, K. & Camp, P. S. (1987). Biology. New York: Saunders College Publishing Co.Google Scholar
Bertaccini, G. (1982). Mediators and Drugs in Gastrointestinal Motility. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Bailey, G. M. A. (1971). Hymenolepis diminuta: circadian rhythm in movement and body length in the rat. Experimental Parasitology 29, 285–91.Google Scholar
Braten, T. & Hopkins, C. A. (1969). The migration of Hymenolepis diminuta in the rat's intestine during normal development and following surgical transplantation. Parasitology 59, 891905.CrossRefGoogle ScholarPubMed
Chappell, L. G., Arai, H. P., Dike, S. C. & Read, C. P. (1970). Circadian migration of Hymenolepis (Cestoda) in the intestine. I. Observations on H. diminuta in the rat. Comparative Biochemistry and Physiology 34, 3446.Google Scholar
Crompton, D. W. T. (1973). The sites occupied by some parasitic helminths in the alimentary tract of vertebrates. Biological Reviews 48, 2783.Google Scholar
Davis, W. J. (1985). Central feedback loops and some implications for motor control. In Feedback and Motor Control in Invertebrates and Vertebrates. (ed. Barnes, W. J. P. & Gladden, M. H.), pp. 1333. London: Croon-Helm Publishing Company.Google Scholar
Delcomyn, F. (1980). Neural basis of rhythmic behavior in animals. Science 210, 492–8.CrossRefGoogle ScholarPubMed
Diamant, N. E. & Bortoff, A. (1969). Nature of intestinal slow-wave frequency gradient. American Journal of Physiology 216, 301–7.Google Scholar
Evans, D. S. & Wickham, M. G. (1971). The migratory behavior of Hymenolepis diminuta in rats. Proceedings of the West Virginia Academy of Science 43, 99102.Google Scholar
Goodchild, C. G. (1958). Transfaunation and repair of damage in the rat tapeworm Hymenolepis diminuta. Journal of Parasitology 44, 345–51.CrossRefGoogle ScholarPubMed
Harris-Warrick, R. M. & Jones, B. R. (1989). Motor pattern networks: flexible foundations for rhythmic pattern production. In Perspectives in Neural Systems and Behavior (ed. Carew, T. J. & Kelley, D. B.), pp. 5171. New York: Alan Liss.Google Scholar
Holmes, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333–47.Google Scholar
Kennedy, C. R. (1984). Host–parasite interrelationships: strategies of coexistence and coevolution. In Producers and Scroungers (ed. Barnard, C. J.), pp. 3460. New York: Chapman and Hall.Google Scholar
Kristan, W., Lockery, S., Wittenberg, G. & Cottrell, G. W. (1989). Behavioral choice – in theory and in practice. In The Computing Neuron (ed. Durbin, R., Miall, C. & Mitchisen, G), pp. 180204. Wokingham: Addison-Wesley Publishing Co.Google Scholar
Lorenz, K. Z. (1981). The Foundations of Ethology. New York: Springer-Verlag.Google Scholar
Lumsden, R. D. & Hildreth, M. B. (1983). The fine structure of adult tapeworms. In Biology of the Eucestoda, vol. 1 (ed. Arme, C. & Pappas, P. W.), pp. 177233. London: Academic Press.Google Scholar
Lumsden, R. D. & Specian, R. (1980). The morphology, histology and fine structure of the adult stage of the cyclophyllidean tapeworm Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 157280. New York: Academic Press.Google Scholar
Mettrick, D. F. (1971 a). Hymenolepis diminuta: effect of quantity of amino acid dietary supplement on growth. Experimental Parasitology 29, 1325.Google Scholar
Mettrick, D. F. (1971 b). Hymenolepis diminuta: pH changes in rat intestinal contents and worm migration. Experimental Parasitology 29, 386401.Google Scholar
Mettrick, D. F. (1971 c). Effect of host dietary constituents on intestinal pH and on migrational behaviors of the rat tapeworm Hymenolepis diminuta. Canadian Journal of Zoology 29, 1513–25.CrossRefGoogle Scholar
Mettrick, D. F. (1972). Changes in the distribution and chemical composition of Hymenolepis diminuta and the intestinal nutritional gradients of uninfected and parasitized rats following a glucose meal. Journal of Helminthology 46, 707–29.CrossRefGoogle ScholarPubMed
Mettrick, D. F. & Podesta, R. B. (1974). Ecological and physiological aspects of helminth–host interactions in the mammalian gastrointestinal canal. Advances in Parasitology 12, 183278.Google Scholar
Read, C. P. & Kilejian, A. Z. (1969). Circadian migratory behaviour of a cestode symbiote in the rat host. Journal of Parasitology 55, 492500.Google Scholar
Scott, L. D. & Summers, R. W. (1976). Correlation of contraction and transit in rat small intestine. American Journal of Physiology 230, 132–7.Google Scholar
Shepherd, G. M. (1983). Neurobiology. Oxford: Oxford University Press.Google Scholar
Sukhdeo, M. V. K. (1990). Habitat selection by helminths: a hypothesis. Parasitology Today 6, 234–7.Google Scholar
Sukhdeo, M. V. K. & Croll, N. A. (1981). The location of parasites in their hosts. Bile and site selection behaviour in Nematospiroides dubius. International Journal for Parasitology 11, 163–8.Google Scholar
Sukhdeo, M. V. K. & Mettrick, D. F. (1984). Migrational responses of Hymenolepis diminuta to surgical alterations of gastrointestinal secretions. Parasitology 88, 421–30.Google Scholar
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour. Understanding platyhelminth responses. Advances in Parasitology 26, 73144.Google Scholar
Sukhdeo, M. V. K., Hsu, S. C., Thompson, C. S. & Mettrick, D. F. (1984). The behavioral effects of 5-HT and Ach on Hymenolepis diminuta. Journal of Parasitology 70, 682–8.Google Scholar
Sukhdeo, M. V. K. & Sukhdeo, S. C. (1989). Gastrointestinal hormones: environmental cues for Fasciola hepatica? Parasitology 98, 239–43.CrossRefGoogle ScholarPubMed
Thompson, C. S. & Mettrick, D. F. (1989). The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 1257–62.CrossRefGoogle Scholar
Ulmer, M. J. (1971). Site finding behaviour in helminths in intermediate and definitive hosts. In Ecology and Physiology of Parasites (ed. Fallis, A. M.), pp. 123160. Toronto: University of Toronto Press.CrossRefGoogle Scholar