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Relationships between Bucephalus sp. and Crassostrea virginica: a histochemical study of some carbohydrates and carbohydrate complexes occurring in the host and parasite*

Published online by Cambridge University Press:  06 April 2009

Thomas C. Cheng  and
Richard W. Burton
Thomas C. Cheng
Affiliation:
Northeast Shellfish Sanitation Research Centre Public Health Service, U.S. Department of Health, Education, and Welfare, Narragansett, Rhode Island, U.S.A.
Richard W. Burton
Affiliation:
Northeast Shellfish Sanitation Research Centre Public Health Service, U.S. Department of Health, Education, and Welfare, Narragansett, Rhode Island, U.S.A.
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Extract

Six different histochemical techniques were employed to study the sites of deposition of glycogen, other carbohydrates, and carbohydrate complexes in uninfected Crassostrea virginica and those parasitized by the larvae of the trematode Bucephalus sp. The carbohydrate and carbohydrate complexes occurring in the parasites were also studied.

In uninfected oysters, glycogen is stored in the digestive diverticula, in Leydig cells located between the diverticula in the digestive gland, in the matrices of the palps, mantle, and gills, in walls of blood vessels, and in ova. There is a marked reduction of stored glycogen at these sites in infected oysters. In addition, the glycogen-storing diverticular cells and the interdiverticular Leydig cells are ruptured and/or lysed and the enclosed glycogen is expelled to the exterior.

Glycogen is found in the sporocysts; however, very little if any is present in cells comprising young germ balls. It is only after the elongate germ balls commence differentiating into cercariae that glycogen appears in their bodies.

In uninfected oysters, glucose deposits are present in the same Leydig cells in which stored glycogen is found. Glucose is believed to be the hexose from which the stored glycogen is synthesized. In infected oysters, the reduction of glucose in Leydig cells is almost complete.

There are histochemically demonstrable amounts of glucose in the blood vessels and sinuses of infected oysters while such is not the case in uninfected ones. This phenomenon is explained by the destruction of the sites of glycogen synthesis and storage in infected oysters, thus bringing about hyperglycaemia resulting from the accumulation of glucose taken in from the exterior.

The presence of glucose deposits adhering to the gill surfaces of infected oysters may represent the direct absorption of glucose from the environment and contribute to the hyperglycaemic conditions.

The absorption of glucose by sporocysts is suggested by the finding of this hexose adhering to the exterior and in the wall of certain sporocysts.

Gamma metachromatic globules are present in the digestive diverticula of uninfected oysters. Their number is increased in infected oysters. In addition, the connective tissue layers abutting the base of the epithelial lining of the stomach and intestine and the fibres at the base of the surface epithelium of the gills of uninfected and infected oysters are metachromatic. Metachromasia at these sites is believed to be due to acid mucopolysaccharides.

Acid mucopolysaccharides are present in certain cells intermingled among the ciliated epithelial lining of the gastric and intestinal walls and in secretory cells along the surface of the mantle, gills and palps. The histochemical reactions at these sites remain unaltered in infected oysters.

Only older sporocysts include acid mucopolysaccharides in the walls.

In older germ balls, acid mucopolysaccharides are present in the small somatic cells situated on the surface, beneath the enveloping membrane. These are believed to be cuticle-secreting cells.

In developing cercariae, acid mucopolysaccharides are found in the cuticle and certain parenchymal cells.

There is an increase in the number of ‘brown cells’ in infected oysters. The smallest and largest do not include acid mucopolysaccharides but those that measure between 0·006 and 0·012 mm are partially or totally positive for acid mucopolysaccharide. Slight metachromasia and sphingomyelins also are associated with certain ‘brown cells’ found in the digestive glands of infected oysters.

Large ‘brown cells’ in the intertubular spaces in the digestive glands of both uninfected and infected oysters have been observed to undergo division.

Type
Research Article
Information
Parasitology , Volume 56 , Issue 1 , February 1966 , pp. 111 - 122
Copyright
Copyright © Cambridge University Press 1966

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References

REFERENCES

axmann, M. C. (1947). Morphological studies on glycogen deposition in schistosomes and other flukes. J. Morph. 80, 321–34.CrossRefGoogle ScholarPubMed
Bargeton, M. (1941). Note sur les ‘cellules vésiculeuses a glycogène'. Étude de la distribution du glycogène chez les lombriciens et chez les ostréidés. Bull. Mus. Hist. nat., Paris, 13, 119–25.Google Scholar
Bargeton, M. (1942). Les variations saisonnières du tissu conjonctif vésiculeux de l'huître. Bull. biol. Fr. Belg. 76, 175–91.Google Scholar
Bargeton, M. (1945). Sur le teneur en glycogène des diverticules digestifs de l'huître. C.r. hebd. Séanc. Acad. Sci., Paris, 220, 623–5.Google Scholar
Bargeton, M. (1946). Variations du taux de glycogène dans différents organes de l'huître. Bull. Soc. zool. Fr. 71, 121–6.Google Scholar
Bernard, C. (1853). Recherches sur une nouvelle fonction du foie. Annls Sci. nat. Zool. 19, 282–340.Google Scholar
Best, A. (1903). Ueber Glykogen, inbesondere seine Bedeutung bei Entzündung und Eiterung. Beitr. path. Anat. 33, 585–605.Google Scholar
Bizio, J. (1866). Sur l'existence du glycogène dans les animaux invertèbrés. C.r. hebd. Séanc. Acad. Sci., Paris, 62, 675.Google Scholar
Bullock, W. L. (1948). Histochemical studies on the Acanthocephala: a contribution to helminth metabolism. Ph.D. Thesis, University of Illinois.Google Scholar
Cheng, T. C. (1960). Further studies on the parenchymal cells of digenetic trematodes. Proc. Pa. Acad. Sci. 34, 166–72.Google Scholar
Cheng, T. C. (1963 a). Biochemical requirements of larval trematodes. Ann. N.Y. Acad. Sci. 113, 289–321.CrossRefGoogle ScholarPubMed
Cheng, T. C. (1963 b). Histological and histochemical studies on the effects of parasitism of Musculium partumeium (Say) by the larvae of Gorgodera amplicava Looss. Proc. helminth Soc. Wash. 30, 101–7.Google Scholar
Cheng, T. C. (1963 c). The effects of Echinoparyphium larvae on the structure of and glycogen deposition in the hepatopancreas of Helisoma trivolvis and glycogenesis in the parasite larvae. Malacologia, 1, 291–303.Google Scholar
Cheng, T. C. (1965). On the structure and alteration of cellular polarity of the sporocysts of Bucephalus sp. as a function of age. Proc. Pa. Acad. Sci. (in the Press).Google Scholar
Cheng, T. C. & Burton, R. W. (1965). Relationships between Bucephalus sp. and Crassostrea virginica: histopathology and sites of infection. Chesapeake Sci. 6, 3–16.CrossRefGoogle Scholar
Cheng, T. C. & Provenza, D. V. (1960). Studies on cellular elements of the mesenchyma and of tissues of Haematoloechus confusus Ingles, 1932 (Trematoda). Trans. Am. microsc. Soc. 79, 170–9.CrossRefGoogle Scholar
Cheng, T. C. & Snyder, R. W. Jr. (1962). Studies on host-parasite relationships between larval trematodes and their hosts. I. A review. II. The utilization of the host's glycogen by the intramolluscan larvae of Glypthelmins pennsylvaniensis Cheng, and associated phenomena. Trans. Am. microsc. Soc. 81, 209–28.CrossRefGoogle Scholar
Cheng, T. C. & Snyder, R. W. Jr. (1963). Studies on host-parasite relationships between larval trematodes and their hosts. IV. A histochemical determination of glucose and its role in the metabolism of molluscan host and parasite. Trans. Am. microsc. Soc. 82, 343–46.CrossRefGoogle Scholar
Creighton, C. (1899). Microscopic Researches on the Formative Property of Glycogen. 2 pts. (1896–1899). Part. I. Physiological, 152 pp. Part II. Glycogen of Snails and Slugs in Morphological and Physiological Correspondence with the Lymph System of Vertebrates, 127 pp. London: Adam and Charles Black.Google Scholar
Davenport, H. A. (1960). Histological and Histochemical Technics, 401 pp. Philadelphia: W. B. Saunders Co.Google Scholar
Fraser, J. R. & Holmes, D. C. (1961). The determination of glycogen in oysters. Analyst, Lond., 86, 131–2.Google Scholar
Ginecinskij, T. A. (1960). Glycogen in the body of cercariae and the dependence of its distribution upon the peculiarities of their biology. Dokl. Akad. Nauk. SSSR, 135, 1012–5. (In Russian.)Google Scholar
Ginecinskij, T. A. & Dobrovalskij, A. A. (1962). Glycogen and fat in the various phases of the life cycle of trematodes. Vest. Leningr. gos. Univ. No. 9, (Biol. Ser., 2, 67–81. (In Russian.)Google Scholar
Goldstein, L. C. (1940). The morphology and histology of the Virginia oyster, Ostrea virginica, Lister. M.S. Thesis, University of Richmond.Google Scholar
Grassé, P.-P. (ed.). (1960). Traité de zoologie: Anatomie, Systématique, Biologie. Vol. 5. Paris: Masson et Cie.Google Scholar
Haigler, S. A. (1964). A histochemical and cytological study of the ‘brown cells’ found in the ‘auricular pericardial gland’ and other tissues of the oyster, Crassostrea virginica (Gmelin). M.S. Thesis, University of Delaware.Google Scholar
Hess, M. & Hollander, F. (1947). Permanent metachromatic staining of mucus in tissue sections and smears. J. Lab. clin. Med. 32, 905–9.Google Scholar
Hopkins, S. H. (1957). Our present knowledge of the oyster parasite ‘Bucephalus’. Proc. Natn. Shellfish. Ass. 47, 58–61.Google Scholar
Humphrey, C. (1941). The determination of glycogen in oysters. Aust. J. exp. Biol. med. Sci. 19, 311–12.CrossRefGoogle Scholar
Kelly, J. W. (1956). The metachromatic reaction. In Protoplasmatologia. Band ii. Cytoplasma. 98 pp. Vienna: Springer-Verlag.Google Scholar
McManus, J. F. A. (1946). Histological demonstration of mucin after periodic acid. Nature, Lond. 158, 202.CrossRefGoogle ScholarPubMed
Monné, L. (1959). On the external cuticles of various helminths and their role in the host-parasite relationship. Ark. Zool. 12, 343–58.Google Scholar
Okamoto, K., Kadota, I & Aoyama, Z. (1948). Histochemical test-method of glucose and lactose. Taish. Gaku Zasshi. 14, 35–40. (In Japanese.)Google Scholar
Palm, V. (1962 a). Glykogen- und Fettstoffwechsel bei Cercaria limnaea ovata. Z. ParasitKde. 22, 261–6.Google Scholar
Palm, V. (1962 b). Glykogen und Fett bei Trematodenlarvenstadien am Beispiel von Delichosaccus rastellus and Haplometra cylindraceum (Plagiorchiida). Acta parasit. pol. 10, 117–23.Google Scholar
Pearse, A. G. E. (1961). Histochemistry, Theoretical and Applied. 998 pp. Boston: Little, Brown and Co.Google Scholar
Pekelharing, C. A. (1901). Le tissue conjonctif de l'huître (Hollandais). Petrus Camper ned. Bijdr. Anat. pp. 228–38.Google Scholar
Rinehart, J. F. & Abul-Haj, S. K. (1951). An improved method for histologic demonstration of acid mucopolysaccharides in tissues. Archs Path. 52, 189–94.Google ScholarPubMed
Russell, E. S. (1923). Report on seasonal variations in the chemical composition of oysters. Fishery Invest., Lond., (Ser. 2), 62, 1–24.Google Scholar
Snyder, R. W. Jr. & Cheng, T. C. (1961). The effect of the larvae of Glypthelmins pennsylvaniensis (Trematoda: Brachycoeliidae) on glycogen deposition in the heptatopancreas of Helisoma trivolvis (Say). J. Parasit. 47 (Sect. 2), 52.Google Scholar
Steedman, H. F. (1950). Alcian blue 8GS: a new stain for mucin. Q. Jl microsc. Sci. 91, 477–9.Google ScholarPubMed
Tennent, D. H. (1906). A study of the life-history of Bucephalus haimeanus; a parasite of the oyster. Q. Jl microsc. Sci. 49, 635–90.Google Scholar
White, K. M. (1942). The pericardial cavity and the pericardial gland of the Lamellibranchia. Proc. malac. Soc. Lond. 25, 37–88.Google Scholar
Yonge, C. M. (1926). Structure and physiology of the organs of feeding and digestion in Ostrea edulis. J. mar. biol. Ass. U.K. 14, 295–386.CrossRefGoogle Scholar