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The diet and gastrodermal ultrastructure of polystomatid monogeneans infecting chelonians

Published online by Cambridge University Press:  06 April 2009

K. M. Allen
Affiliation:
School of Biological Sciences, Queen Mary College, London University, Mile End Road, London, E1 4NS
R. C. Tinsley
Affiliation:
School of Biological Sciences, Queen Mary College, London University, Mile End Road, London, E1 4NS

Summary

All polyopisthocotylean monogeneans previously studied, including representatives of the Polystomatidae infecting anuran amphibians, feed on host blood. However, the present analysis of species of Polystomoides, Polystomoidella and Neopolystoma, polystomatids which infect chelonian reptiles, has shown that this group has diverged nutritionally from related parasites. Histochemical tests failed to demonstrate haemoglobin in the gut caeca, and X-ray microanalysis confirmed the absence of haematin (or high concentrations of bound iron) in the gastrodermis. The chelonian poly-stomatids (and also the single monogenean which infects a mammal, Oculotrema hippopotami) feed on epithelial cells and mucus, the diet typical of monopisthocotyleans. Transmission electron microscopy revealed the same gastrodermal architecture in representatives of Polystomoides from Africa, N. America and S.E. Asia. The organization of the caecal epithelium conforms with that of blood-feeding polyopisthocotyleans, with two components: lamellated cells responsible for intracellular digestion interspersed with elements of a non-lamellated connecting syncytium. In other polyopistho-cotyleans, the syncytium probably has a skeletal, supportive role, related to the problems of intracellular accumulation of haematin, but in polystomatids infecting chelonians the syncytium is extremely reduced and its presence probably reflects an ancestry amongst blood-feeding relatives. The utilization of the presumably more primitive monogenean diet of epithelial cells and mucus by chelonian polystomatids may be related to the scarcity of superficial blood vessels in their oral and urinary bladder habitats.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

REFERENCES

Fournier, A. (1978). Euzetrema knoepffleri: evidence for a synchronous cycle of gastrodermal activity and an ‘apocrine-like’ release of the residues of digestion. Parasitology 77, 1926.Google Scholar
Fried, B. (1965). Transplantation of a monogenetic trematode, Polystomoides sp., to the chick chorioallantois. Journal of Parasitology 51, 983–6.CrossRefGoogle Scholar
Halton, D. W. (1967). Observations on the nutrition of digenetic trematodes. Parasitology 57, 639–60.CrossRefGoogle ScholarPubMed
Halton, D. W. (1974). Hemoglobin absorption in the gut of a monogenetic trematode, Diclidophora merlangi. Journal of Parasitology 60, 5966.CrossRefGoogle Scholar
Halton, D. W. (1975). Intracellular digestion and cellular defecation in a monogenean, Diclidophora merlangi. Parasitology 70, 331–40.CrossRefGoogle Scholar
Halton, D. W. (1976). Diclidophora merlangi: sloughing and renewal of haematin cells. Experimental Parasitology 40, 4171CrossRefGoogle ScholarPubMed
Halton, D. W. (1982). X-ray microanalysis of pigment granules in the gut of Diclidophora merlangi (Monogenoidea). Zeitschrift für Parasitenkunde 68, 113–15.CrossRefGoogle Scholar
Halton, D. W., Dermott, E. & Morris, G. P. (1968). Electron microscope studies of Diclidophora merlangi (Monogenea: Polyopisthocotylea). 1. Ultrastructure of the cecal epithelium. Journal of Parasitology 54, 909–16.CrossRefGoogle Scholar
Halton, D. W. & Jennings, J. B. (1965). Observations on the nutrition of monogenetic trematodes. Biological Bulletin 129, 257–72.CrossRefGoogle ScholarPubMed
Halton, D. W. & Stranock, S. D. (1976). The fine structure and histochemistry of the caecal epithelium of Calicotyle kroyeri (Monogenea: Monopisthocotylea). International Journal for Parasitology 6, 253–63.CrossRefGoogle ScholarPubMed
Jackson, H. C. (1987). The role of blood in helminth nutrition. Helminthological Abstracts (Series A) 56, 427–34.Google Scholar
Jennings, J. B. (1959). Studies on digestion in the monogenetic trematode Polystoma integerrimum. Journal of Helminthology 33, 197204.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1963). Feeding in some monogenean skin parasites: Entobdella solea on Solea solea and Acanthocotyle sp. on Raia clavata. Journal of the Marine Biological Association of the United Kingdom 43, 749–66.CrossRefGoogle Scholar
Lewis, P. R. & Knight, D. P. (1977). Staining methods for sectioned material. In Practical Methods in Electron Microscopy (ed. Glauert, A. M.), vol. 5 part I. Amsterdam: North Holland Publishing Company.Google Scholar
Llewellyn, J. (1954). Observations on the food and gut pigment of the Polyopisthocotylea (Trematoda: Monogenea). Parasitology 44, 428–37.CrossRefGoogle ScholarPubMed
Paul, A. A. (1938). Life history studies of North American freshwater Polystomes. Journal of Parasitology 24, 489510.CrossRefGoogle Scholar
Pearse, A. G. E. (1961). Histochemistry, Theoretical and Applied. 2nd Edn. London: J. & A. Churchill Ltd.Google Scholar
Rohde, K. (1973). Ultrastructure of the caecum of Polystomoides malayi Rohde and P. renschii Rohde (Monogenea: Polystomatidae). International Journal for Parasitology 3, 461–6.CrossRefGoogle Scholar
Rohde, K. (1974). Light- and electron-microscopic studies of the pharynx and the anterior and posterior glands of Polystomoides (Monogenea: Polystomatidae). Zoologischer Jahrbucher, Abteilung fur Anatomie und Ontogenie der Tiere 92, 117.Google Scholar
Rohde, K. (1975). Fine structure of the Monogenea, especially Polystomoides Ward. Advances in Parasitology 13, 133.CrossRefGoogle Scholar
Smyth, J. D. & Halton, D. E. (1983). The Physiology of Trematodes, 2nd Edn. Cambridge: Cambridge University Press.Google Scholar
Thurston, J. P. (1970). Haemoglobin in a monogenean Oculotrema hippopotami. Nature, London 228, 578–9.Google Scholar
Tinsley, R. C. (1973 a). Ultrastructural studies on the form and function of the gastrodermis of Protopolystoma xenopi (Monogenoidea: Polyopisthocotylea). Biological Bulletin 144, 541–55.CrossRefGoogle Scholar
Tinsley, R. C. (1973 b). Observations on Polystomatidae (Monogenoidea) from East Africa with a description of Polystoma makereri n.sp. Zeitschrift für Parasitenkunde 42, 251–63.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1974). The gut ultrastructure of the Polystomatidae (Monogenea). Parasitology 69, iiiii.Google ScholarPubMed
Tinsley, R. C. (1983). Ovoviviparity in platyhelminth life-cycles. Parasitology 86, 161–96.CrossRefGoogle ScholarPubMed
Uspenskaya, A. V. (1962). Nutrition of monogenetic trematodes [in Russian]. Doklady Akademii Nauk SSSR 142, 1212–5.Google Scholar