Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-30T16:03:20.709Z Has data issue: false hasContentIssue false

Studies on gut ultrastructure and digestive physiology in Rhabdias bufonis and R. sphaerocephala (Nematoda: Rhabditida)

Published online by Cambridge University Press:  06 April 2009

J. Barry Colam
Affiliation:
Department of Zoology, The University, Leeds, LS2 9JT

Extract

Histological, histochemical and ultrastructural methods have been used to study gut structure and digestive physiology in the parasitic nematodes Rhabdias bufonis (Schrank, 1788) and R. sphaerocephala (Goodey, 1924). Both species are parasitic in the lungs of their amphibian hosts and feed entirely upon blood drawn from the lung capillaries.

Three gland cells are present in the oesophagus, one in each sector. The two subventral ducts open, by way of ampullae, into the lumen of the oesophagus about a quarter of its length from the anterior end. The dorsal gland opens similarly into the base of the buccal capsule. It is suggested that the glands produce a B-esterase, in an histochemically inactive form in situ, which is responsible for haemolysis and the bulk of extracellular digestion. Only one cell type is present in the intestine and this is entirely absorptive in function.

The major part of haemoglobin digestion is extracellular, partly by a process of contact digestion involving the B-esterase and acid phosphatase which are present in association with the microvilli. Haematin results from this process and is precipitated in the gut lumen. A smaller proportion of haemoglobin is taken up by the gut cells and is broken down intracellularly by lysosomes, originating in Golgi in the basal gastrodermis. These show endopeptidase activity and later acid phosphatase in some of the bodies of the lysosomal sequence and only at the light microscope level. The iron-containing pigment haemosiderin resulting from digestion is retained in the lysosome residues and forms the pigment granules in the gastrodermis. The products of extracellular digestion absorbed by the gastrodermis are synthetized into lipid by a lipase, probably produced by GER.

This investigation was supported in part by Research Grant AI 06295 of the United States Public Health Service. The final manuscript was prepared during the tenure of a Postdoctoral Fellowship from the British Egg Marketing Board. I wish to extend my gratitude to Dr J. B. Jennings for advice and encouragement throughout this work.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1971

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

Ackert, J. E. & Whitlock, J. H. (1937). Feeding habits of nematode parasites of vertebrates. In An Introduction to Nematology, eds. Chitwood, B. G. and Chitwood, M. B.. Baltimore: Monumental Printing Company.Google Scholar
Andreassen, J. (1968). Fine structure of the intestine of the nematodes, Ancylostoma caninum and Phocanema decipiens. Zeitschrift für Parasitenkunde 30, 318–36.CrossRefGoogle ScholarPubMed
Bowen, I. D. (1968). Electron-cytochemical localization of acid phosphatase activity in the digestive caeca of the desert locust. Journal of the Royal Microscopical Society 88, 279–89.CrossRefGoogle ScholarPubMed
Bruce, R. G. (1966). The fine structure of the intestine and hind gut of the larva of Trichinella spiralis. Parasitology 56, 359–65.CrossRefGoogle ScholarPubMed
Burstone, M. S. (1958). Histochemical demonstration of acid phosphatase with naphthol AS-phosphates. Journal of the National Cancer Institute 21, 523–39.Google ScholarPubMed
Burstone, M. S. & Folk, J. E. (1956). Histochemical demonstration of aminopeptidase. Journal of Histochemistry and Cytochemistry 4, 217–26.CrossRefGoogle ScholarPubMed
Carpenter, M. F. P. (1952). The digestive enzymes of Ascaris lumbricoides var suis; their properties and distribution in the alimentary canal. Dissertation, University of Michigan.Google Scholar
Colam, J. B. (1970 a). Studies on gut ultrastructure and digestive physiology in Cyathostomalari (Nematoda: Strongylida). Parasitology 62, 273–83.Google Scholar
Colam, J. B. (1970 b). Studies on gut ultrastructure and digestive physiology in Cosmocerca ornata (Nematoda: Ascaridida). Parasitology 62, 259–72.Google Scholar
Diem, K. (Ed.) (1962). Documenta Geigy, Scientific Tables. Sixth edition. Manchester: Geigy Pharmaceutical Company Ltd.Google Scholar
De Duve, C. & Wattiaux, R. (1966). Functions of lysosomes. Annual Review of Physiology 28, 435–92.CrossRefGoogle ScholarPubMed
Gomori, G. (1952). Microscopic Histochemistry. Chicago: University of Chicago Press.Google Scholar
Halton, D. W. (1967). Observations on the nutrition of digenetic trematodes. Parasitology 57, 639–60.CrossRefGoogle ScholarPubMed
Halton, D. W. & Jennings, J. B. (1965). Observations on the nutrition of monogenetic trematodes. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass. 129, 257–72.CrossRefGoogle ScholarPubMed
Hausler, G. (1958). Zur Technik und Spezifität des Histochemischen Carboanhydrasenack-weises im Modellversuch und im Gewebsschnitten von Rattennieren. Histochemie 1, 2947.CrossRefGoogle Scholar
Hirumi, H., Chen, T. A., Lee, K. J. & Maramorosch, K. (1968). Ultrastructure of the feeding apparatus of the nematode Trichodorus christiei. Journal of Ultrastructural Research 24, 434–53.CrossRefGoogle ScholarPubMed
Hobson, A. D. (1948). The physiology and cultivation in artificial media of nematodes parasitic in the alimentary tract of animals. Parasitology 38, 183227.CrossRefGoogle ScholarPubMed
Holt, S. J. (1958). Studies in enzyme histochemistry. Proceedings of the Royal Society 148, 465532.Google Scholar
Hyman, L. H. (1961). The Invertebrata 3: Acanthocephala, Aschelminthes and Entoprocta. New York: McGraw-Hill Book Company Inc.Google Scholar
Jamuar, M. P. (1966). Cytochemical and electron microscope studies on the pharynx and intestinal epithelium of Nippostrongylus brasiliensis. Journal of Parasitology 52, 1116–28.CrossRefGoogle ScholarPubMed
Jenkins, T. (1965). Histochemical and electron microscope studies on Trichuris suis. Parasitology 55, 2223P.Google Scholar
Jenkins, T. & Erasmus, D. A. (1969). The ultrastructure of the intestinal epithelium of Metastrongylus sp. (Nematoda: Strongyloidea). Parasitology 59, 335–42.CrossRefGoogle ScholarPubMed
Jennings, J. B. (1959). Studies on digestion in the monogenetic trematode Polystoma integerrimum. Journal of Helminthology 33, 197204.CrossRefGoogle ScholarPubMed
Jennings, J. B. & Colam, J. B. (1970). Gut structure, digestive physiology and food storage in Pontonema vulgaris (Nematoda: Enoplida). Journal of Zoology, London 161, 211–21.CrossRefGoogle Scholar
Jeon, K. W. (1965). Simple method for staining and preserving epoxy-resin embedded animal tissue sections for light microscopy. Life Sciences 4, 1839–42.CrossRefGoogle ScholarPubMed
Lee, D. L. (1958). Digestion in Leidynema appendiculata (Leidy, 1850) a nematode parasitic in cockroaches. Parasitology 48, 437–47.CrossRefGoogle ScholarPubMed
Lee, D. L. (1962a). The distribution of esterase enzymes in Ascaris lumbricoides. Parasitology 52, 241–60.CrossRefGoogle Scholar
Lee, D. L. (1962 b). The histochemical localization of leucine aminopeptidase in Ascaris lumbricoides. Parasitology 52, 533–6.CrossRefGoogle Scholar
Lee, D. L. (1965). The Physiology of Nematodes. Edinburgh and London: Oliver and Boyd.Google Scholar
Lee, D. L. (1968). The ultrastructure of the alimentary tract of the skin-penetrating larva of Nippostrongylus brasiliensis. Journal of Zoology, London 154, 918.CrossRefGoogle Scholar
Lee, D. L. (1969). Nippostrongylus brasiliensis: some aspects of the fine structure and biology of the infective larva and adult. ‘Nippostrongylus and Toxoplasma. Symposia of the British Society for Parasitology 7, 316.Google Scholar
Lee, D. L. & Anya, A. O. (1968). Studies on the movement, the cytology and the associated micro-organisms of the intestine of Aspiculuris tetraptera (Nematoda). Journal of Zoology, London 156, 914.CrossRefGoogle Scholar
Lemberg, R. & Legge, J. W. (1949). Hematin Compounds and Bile Pigments. Their Constitution, Metabolism, and Function. New York and London: Interscience Publishers, Inc.Google Scholar
Llewellyn, J. (1954). Observations on the food and the gut pigment of the Polyopistho-cotylea (Trematoda: Monogenea). Parasitology 44, 428–37.CrossRefGoogle ScholarPubMed
Mazia, D., Brewer, P. A. & Alfert, M. (1953). The cytological staining and measurement of protein with mercuric bromophenol blue. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass. 104, 5767.CrossRefGoogle Scholar
Miller, J. H. (1967). Fine structure of the striated border of the intestinal cells of Ancylostoma caninum. Journal of Parasitology 53, 9499.CrossRefGoogle ScholarPubMed
Nimmo-Smith, R. H. & Keeling, J. E. D. (1960). Some hydrolytic enzymes of the parastic nematode Trichuris muris. Experimental Parasitology 10, 337–55.CrossRefGoogle Scholar
Pearse, A. G. E. (1961). Histochemistry, Theoretical and Applied. Second edition. London: Churchill.Google Scholar
Pickworth, F. A. (1934). A new method of study of the brain capillaries and its application to the regional localization of brain disorder. Journal of Anatomy 69, 6271.Google Scholar
Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208–12.CrossRefGoogle ScholarPubMed
Rogers, W. P. (1940). Digestion in parasitic nematodes. I. The digestion of carbohydrates. Journal of Helminthology 18, 183–92.CrossRefGoogle Scholar
Rogers, W. P. (1941 a). Digestion in parasitic nematodes. II. The digestion of fats. Journal of Helminthology 19, 3546.CrossRefGoogle Scholar
Rogers, W. P. (1941 b). Digestion in parasitic nematodes. III. The digestion of proteins. Journal of Helminthology 19, 4758.CrossRefGoogle Scholar
Ugolev, A. M. (1965). Membrane (contact) digestion. Physiological Reviews 45, 555–95.CrossRefGoogle ScholarPubMed
Weinstein, P. P. (1966). The in vitro cultivation of parasitic nematodes with reference to morphorgenesis. In Biology of Parasites, ed. Soulsby, E. J. L.. New York: Academic Press Inc.Google Scholar
Wright, K. A. (1963). The cytology of the intestine of the parasitic nematode Capillaria hepatica (Bancroft, 1893). Journal of Ultrastructural Research 9, 143–55.CrossRefGoogle Scholar
Wright, K. A. (1965). The histology of the oesophageal region of Xiphinema index Thorne and Allen, 1950, as seen with the electron microscope. Canadian Journal of Zoology 43, 690700.CrossRefGoogle ScholarPubMed
Yuen, P. H. (1967). Electron microscopical studies on Ditylenchus dipsaci (Kuhn) I. Stomatal region. Canadian Journal of Zoology 45, 1019–33.CrossRefGoogle Scholar
Yuen, P. H. (1968). Electron microscopical studies on Ditylenchus dipsaci. II. Oesophagus. Nematologica 14, 385–94.CrossRefGoogle Scholar