Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-12-01T00:08:24.869Z Has data issue: false hasContentIssue false

Unique ultrastructural adaptations of Pseudodiplorchis americanus (Polystomatidae: Monogenea) to a sequence of hostile conditions following host infection

Published online by Cambridge University Press:  06 April 2009

J. Cable
Affiliation:
School of Biological Sciences, Queen Mary and Westfield College, University of London, Mile End Road, London E1 4NS
R. C. Tinsley
Affiliation:
School of Biological Sciences, Queen Mary and Westfield College, University of London, Mile End Road, London E1 4NS

Summary

The polystomatid Pseudodiplorchis americanus occupies a wider range of habitats and experiences more diverse physiological conditions than any other monogenean. It initially invades the respiratory system of an anuran, Scaphiopus couchii, and then migrates along the alimentary tract while the host is actively feeding, resulting in exposure to digestive enzymes and the surfactant action of bile. Whilst in the urinary bladder, parasites are exposed to wide osmotic fluctuations. This ultrastructural study reveals a set of adaptations unknown elsewhere in platyhelminth biology. During development within the respiratory tract, pre-migratory worms accumulate two types of electron-dense tegumental vesicle. Migration through the gut is accompanied by mass secretion of vesicles which appear to provide protection against digestion. Pre-migrants transferred experimentally to digestive fluids die within minutes unless they have received a specific cue which is responsible for triggering vesicle secretion. Migrants stimulated by this trigger factor can tolerate the same conditions for up to 8 h by continually releasing vesicles to form a protective surface coat. No specific structural adaptations were evident for survival in the lungs or bladder of the host.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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

Adamson, I. Y. R. & Bowden, D. H. (1970). The surface complexes of the lung. A cytochemical partition of phospholipid surfactant and mucopolysaccharide. American Journal of Pathology 61, 359–76.Google Scholar
Allen, K. M. (1984). Ultrastructural adaptations of the host-parasite interface of polystomatid monogeneans. Ph.D. thesis, University of London.Google Scholar
Bennett, C. E. & Threadgold, L. T. (1975). Fasciola hepatica: development of tegument during migration in the mouse. Experimental Parasitology 38, 3855.CrossRefGoogle Scholar
Bychowsky, B. E., Korotajeva, V. D. & Nagibina, L. F. (1970). [Montchadskyella intestinale gen. & sp.n – a new member of the endoparasitic monogeneans (Monogenoidea)]. Parasitologiya 4, 451–7. (In Russian.) English Abstract.Google Scholar
Cable, J. (1989). Ultrastructural adaptations of parasites exposed to extreme environmental conditions. Ph.D. thesis, University of London.Google Scholar
Cable, J. & Tinsley, R. C. (1991). Intra-uterine larval development of the polystomatid monogeneans, Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 103, 253–66.CrossRefGoogle ScholarPubMed
Cable, J. & Tinsley, R. C. (1992). Tegumental ultrastructure of Pseudodiplorchis americanus larvae (Polystomatidae: Monogenea). International Journal for Parasitology (in the Press.)CrossRefGoogle Scholar
Combes, C. (1980). Invasion strategies in parasites of amphibious hosts. Parasitology 82 (4), 63–4.Google Scholar
Cone, D. K., Gratzek, J. B. & Hoffman, G. L. (1987). A study of Enterogyrus sp. (Monogenea) parasitizing the foregut of captive Pomacanthus paru (Pomacanthidae) in Georgia. Canadian Journal of Zoology 65, 312–16.CrossRefGoogle Scholar
Dimmitt, M. A. & Ruibal, R. (1980). Exploitation of food resources by Spadefoot toads (Scaphiopus). Journal of Herpetology 14, 21–9.CrossRefGoogle Scholar
Fournier, A. (1979). Evolution du tégument des Polystoma (Monogènes: Polystomatidae) au cours du cycle. Persistance de l'épiderme embryonaire nucléé chez les oncomiracidiums. Zeitschrift für Parasitenkunde 59, 169–85.CrossRefGoogle Scholar
Fournier, A. (1980). Les monogènes d'amphibiens. Approche ultrastructurale des modifications adaptatives au cours du cycle et des relations phyletiques. Thèse Doct., Université de Perpignan, France.Google Scholar
Gussev, A. V. & Fernando, C. H. (1973). Dactylogyridae (Monogenoidea) from the stomach of fishes. Folia Parasitologica 20, 207–12.Google Scholar
Haselwood, G. A. D. (1978). The Biological Importance of Bile Salts. Frontiers in Biology. Amsterdam: North Holland Publishing Company.Google Scholar
Hayat, M. A. (1975). Positive Staining for Electron Microscopy. New York: Van Nostrand Reinhold.Google Scholar
Meban, C. (1972). An electron microscopic study of the acid mucosubstance lining the alveoli of hamster lung. Histochemical Journal 4, 18.CrossRefGoogle ScholarPubMed
Paperna, I. (1963). Enterogyrus cichlidarum n.gen. n.sp., a monogenetic trematode parasitic in the intestine of a fish. Bulletin of the Research Council of Israel, B 11, 183–7.Google Scholar
Perrin, D. D. & Dempsey, B. (1979). Buffers for pH and Metal Ion Control. New York: Chapman & Hall.CrossRefGoogle Scholar
Reader, W. R. (1964). The digestive system. In Physiology of the Amphibia (ed. Moore, J. A.), pp. 99142. New York: Academic Press.Google Scholar
Rieger, R. M. (1981). Morphology of the Turbellaria at the ultrastructural level. Hydrobiologia 84, 213–30.CrossRefGoogle Scholar
Shoemaker, V. H., McClanahan, L. & Ruibal, R. (1969). Seasonal changes in body fluids in a field population of spadefoot toads. Copeia 1969, 585–91.CrossRefGoogle Scholar
Smyth, J. D. & Haselwood, G. A. D. (1963). The biochemistry of bile as a factor in determining host specificity in intestinal parasites, with particular reference to Echinococcus granulosus. Annals of the New York Academy of Sciences 113, 234–60.CrossRefGoogle Scholar
Tinsley, R. C. (1990). The influence of parasite infection on mating success in spadefoot toads, Scaphiopus couchii. American Zoologist 30, 313–24.CrossRefGoogle Scholar
Tinsley, R. C. & Earle, C. M. (1983). Invasion of vertebrate lungs by the polystomatid monogeneans Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 86, 501–7.CrossRefGoogle Scholar
Tinsley, R. C. & Jackson, H. C. (1986). Intestinal migration in the life-cycle of Pseudodiplorchis americanus (Monogenea). Parasitology 93, 451–69.CrossRefGoogle Scholar
Wattel, W. (1974). PA-TCH-SP: A PAS-type staining method for polysaccharide in electron microscopy. LKB Application Note 147.Google Scholar