Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-26T00:38:46.075Z Has data issue: false hasContentIssue false

The relative roles of the intestines and external surfaces in the nutrition of monogeneans, digeneans and nematodes

Published online by Cambridge University Press:  23 August 2011

P. W. Pappas
Affiliation:
Department of Zoology, The Ohio State University, Columbus, OH 43210–1293, USA

Summary

Several major groups of parasitic helminths (Monogenea, Digenea and Nematoda) possess two surfaces that are potentially absorptive in nature. These are an external surface, a tegument in the platyhelminths and cuticle in the nematodes, and the intestine. This paper discusses the relative contributions of these absorptive surfaces in the nutrition of these parasitic helminths. There are many factors that determine the availability of, and a parasite's ability to absorb nutrients via either of these surfaces, and this review discusses individually some of the more important morphological, physiological and environmental factors affecting the potential nutritional roles of these surfaces. It is clear from such a summary of previous studies that the intestines and teguments (cuticles) of helminth parasites can each serve an important nutritional role. However, insufficient data make it impossible at this time to determine the relative nutritional roles of these surfaces in any single parasitic helminth.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

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

Ammerman, J. W. & Azam, F. (1981). Dissolved cyclic adenosine monophosphate (cAMP) in the sea and uptake of cAMP by marine bacteria. Marine Ecology Progress Series 5, 85–9.CrossRefGoogle Scholar
Ando, K., Mitsuhashi, J. & Kitamura, S. (1980). Uptake of amino acids and glucose by microfilaria of Dirofilaria immitis in vitro. American Journal of Tropical Medicine and Hygiene 29, 213–16.CrossRefGoogle ScholarPubMed
Abme, C. (1982). Nutrition. In Modern Parasitology (ed. Cox, F. E. G.), pp. 148172. Oxford: Blackwell Scientific Publications.Google Scholar
Asch, H. L. & Read, C. P. (1975 a). Tegumental absorption of amino acids by male Schistosoma mansoni. Journal of Parasitology 61, 378–9.CrossRefGoogle Scholar
Asch, H. L. & Read, C. P. (1975 b). Membrane transport in Schistosoma mansoni: transport of amino acids in adult males. Experimental Parasitology 38, 123–35.CrossRefGoogle ScholarPubMed
Azam, F. & Hodson, R. E. (1977). Dissolved ATP in the sea and its utilization by marine bacteria. Nature, London 267, 696–8.CrossRefGoogle ScholarPubMed
Basch, P. F. & Diconza, J. J. (1974). The miracidium – sporocyst transition in Schistosoma mansoni: surface changes in vitro with ultrastructure correlation. Journal of Parasitology 60, 935–41.CrossRefGoogle ScholarPubMed
Bauer, C. (1986). Ciliates as possible food source for adult Oxyuris equi Schrank 1788. Zeitschrifi für Parasitenkunde 72, 279–80.CrossRefGoogle ScholarPubMed
Beckett, E. B. & Boothroyd, B. (1970). Mode of nutrition of the larvae of the filarial nematode Brugia pahangi. Parasitology 60, 21–6.CrossRefGoogle ScholarPubMed
Bennett, C. E. & Threadgold, L. T. (1975). Fasciola hepatica: development of tegument during migration in the mouse. Experimental Parasitology 38, 3855.CrossRefGoogle Scholar
Bird, A. F. (1980). The nematode cuticle and its surface. In Nematodes as Biological Models, vol. 2 (ed. Zuckerman, B. M.), pp. 213–36. New York: Academic Press.Google Scholar
Bone, L. W. & Bottjer, K. P. (1985). Stimulation of ingestion in Trichostrongylus colubriformis (Nematoda). Proceedings of the Helminthological Society of Washington 52, 80–4.Google Scholar
Bone, L. W. & Bottjer, K. P. (1986). Nippostrongylus brasiliensis: effect of host hormones on helminth ingestion in vivo. International Journal for Parasitology 16, 7780.CrossRefGoogle ScholarPubMed
Bottjer, K. P. & Bone, L. W. (1985). Nippostrongylus brasiliensis: in vitro feeding activity. International Journal for Parasitology 15, 1519.CrossRefGoogle ScholarPubMed
Bottjer, K. P. & Bone, L. W. (1986 a). Effect of combined feeding stimuli on ingestion by the nematode Trichostrongylus colubriformis. Journal of Chemical Ecology 12, 147–54.CrossRefGoogle Scholar
Bottjer, K. P. & Bone, L. W. (1986 b). In vitro ingestion by Trichostrongylus colubriformis (Nematoda) in sera, bacteria, and media. Proceedings of the Helminthological Society of Washington 53, 134–6.Google Scholar
Bottjer, K. P., Klesius, P. H. & Bone, L. W. (1985). Effects of host serum of feeding in Trichostrongylus colubriformis (Nematoda). Parasite Immunology 7, 19.CrossRefGoogle ScholarPubMed
Brand, T. Von (1979). Biochemistry and Physiology of Endoparasites. Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
Castro, G. A. & Fairbairn, D. (1969 a). Comparison of cuticular and intestinal absorption of glucose by adult Ascaris lumbricoides. Journal of Parasitology 55, 1316.CrossRefGoogle ScholarPubMed
Castro, G. A. & Fairbairn, D. (1969 b). Effect of immune serum on glucose absorption and infectivity of Trichinella spiralis. Journal of Parasitology 55, 5966.CrossRefGoogle ScholarPubMed
Castro, G. A. & Roy, S. A. (1974). Disaccharidases in the nutrition of Trichinella spiralis. Journal of Parasitology 60, 887–9.CrossRefGoogle ScholarPubMed
Chappell, L. H. (1974). Methionine uptake by larval and adult Schistosoma mansoni. International Journal for Parasitology 4, 361–9.CrossRefGoogle ScholarPubMed
Chappell, C. L. & Dresden, M. H. (1986). Schistosoma mansoni: ‘hemoglobinase’ proteinase activity in material from the digestive tract of adult worms. Experimental Parasitology 61, 160–7.CrossRefGoogle ScholarPubMed
Chen, S. N. & Howells, R. E. (1979). The uptake in vitro of dyes, monosaccharides and amino acids by the filarial worm Brugia pahangi. Parasitology 78, 343–54.CrossRefGoogle ScholarPubMed
Colam, J. B. (1971 a). Studies on gut ultrastructure and digestive physiology in Rhabdias bufonis and R. sphaerocephala (Nematoda: Rhabditida). Parasitology 62, 247–58.CrossRefGoogle Scholar
Colam, J. B. (1971 b). Studies on gut ultrastructure and digestive physiology in Cosmocerca ornata (Nematoda: Ascaridida). Parasitology 62, 259–72.CrossRefGoogle ScholarPubMed
Colam, J. B. (1971 c). Studies on gut ultrastructure and digestive physiology in Cyathostoma lari (Nematoda: Strongylida). Parasitology 62, 273–83.CrossRefGoogle ScholarPubMed
Collin, W. K. (1971). Ultrastructural morphology of the esophageal region of the infective larvae of Brugia pahangi (Nematoda: Filarioidea). Journal of Parasitology 57, 449–68.CrossRefGoogle Scholar
Comley, J. C. W. & Mendis, A. H. W. (1986). Advances in the biochemistry of filariae. Parasitology Today 2, 34–7.CrossRefGoogle ScholarPubMed
Cornford, E. M. (1986). Influence of mating on surface nutrient exchange in schistosomes. Journal of Chemical Ecology 12, 1777–96.CrossRefGoogle ScholarPubMed
Cornford, E. M. & Fitzpatrick, A. M. (1985). The mechanism and rate of glucose transfer from male to female schistosomes. Molecular and Biochemical Parasitology 17, 131–41.CrossRefGoogle ScholarPubMed
Cornford, E. M. & Oldendorf, W. H. (1979). Transintegumental uptake of metabolic substrates in male and female Schistosoma mansoni. Journal of Parasitology 65, 357–63.CrossRefGoogle ScholarPubMed
Croll, N. A. (1976). The location of parasites within their hosts: the influence of host feeding and diet on the dispersion of adults of Nippostrongylus brasiliensis in the intestine of the rat. International Journal for Parasitology 6, 441–8.CrossRefGoogle ScholarPubMed
Dargie, J. D. (1975). Applications of radioisotopic techniques to the study of red cell and plasma protein metabolism in helminth diseases of sheep. In Pathogenic Processes in Parasitic Infections. Symposia of the British Society of Parasitologists, vol. 13 (ed. Taylor, A. E. R. and Muller, R.), pp. 126. Oxford: Blackwell Scientific Publications.Google Scholar
Dass, P. D. & Donahue, M. J. (1986). γ-glutamyl transpeptidase activity in Ascaris suum. Molecular and Biochemical Parasitology 20, 233–36.CrossRefGoogle ScholarPubMed
Dawes, B. (1963). The migration of juvenile forms of Fasciola hepatica L. through the wall of the intestines in the mouse, with some observations on food and feeding. Parasitology 53, 109–22.CrossRefGoogle Scholar
Despommier, D. D., Kajima, M. & Wostmann, B. S. (1967). Ferritin-conjugated antibody studies on the larvae of Trichinella spiralis. Journal of Parasitology 53, 618–24.CrossRefGoogle ScholarPubMed
Dike, S. C. (1971). Ultrastructure of the esophageal region in Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 20, 552–68.CrossRefGoogle ScholarPubMed
Dresden, M. H., Rutledge, K. L. & Chappell, C. L. (1981). Properties of the acid thiol proteinase from Schistosoma mansoni adults. Molecular and Biochemical Parasitology 4, 61–6.CrossRefGoogle ScholarPubMed
Erasmus, D. A. (1967). The host – parasite interface of Cyathocotyle bushiensis Khan, 1962 (Trematoda: Strigeoidea). II. Electron microscope studies of the tegument. Journal of Parasitology 53, 703–14.CrossRefGoogle ScholarPubMed
Ernst, S. C. (1975). Biochemical and cytological studies of digestive – absorptive functions of esophagus, cecum, and tegument in Schistosoma mansoni: acid phosphatase and tracer studies. Journal of Parasitology 61, 633–47.CrossRefGoogle Scholar
Fetterer, R. H. & Wasiuta, M. (1987). Ascaris suum: partial isolation and characterization of hypodermis from adult female. Experimental Parasitology 63, 312–18.CrossRefGoogle ScholarPubMed
Fleming, M. W. & Fetterer, R. H. (1984). Ascaris suum: continuous perfusion of the pseudocoelom and nutrient absorption. Experimental Parasitology 57, 142–8.CrossRefGoogle ScholarPubMed
Foster, L. A. & Bogitsh, B. J. (1986). Utilization of the heme moiety of hemoglobin by Schistosoma mansoni schistosomules in vitro. Journal of Parasitology 72, 669–76.CrossRefGoogle ScholarPubMed
Franz, M. & Andrews, P. (1986). Fine structure of adult Litomosoides carinii (Nematoda: Filarioidea). Zeitschrift für Parasitenkunde 72, 537–47.CrossRefGoogle Scholar
Fripp, P. J. (1967). The sites of (1-14C) glucose assimilation in Schistosoma haematobium. Comparative Biochemistry and Physiology 23, 893–8.CrossRefGoogle ScholarPubMed
Halton, D. W. (1967 a). Studies on phosphatase activity in Trematoda. Journal of Parasitology 53, 4654.CrossRefGoogle ScholarPubMed
Halton, D. W. (1967 b). 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. (1976). Nutrition in monogeneans. Parasitology 73, xxi–xxiii.Google Scholar
Halton, D. W. (1978). Trans-tegumental absorption of L-alanine and L-leucine by a monogenean, Diclidophora merlangi. Parasitology 76, 2937.CrossRefGoogle ScholarPubMed
Halton, D. W. & Arme, C. (1971). In vitro technique for detecting tegument damage in Diclidophora merlangi: possible screening method for selection of undamaged tissues or organisms prior to physiological investigation. Experimental Parasitology 30, 54–7.CrossRefGoogle ScholarPubMed
Halton, D. W. & Jennings, J. B. (1965). Observations on the nutrition of monogenetic trematodes. Biological Bulletin 129, 257–72.CrossRefGoogle ScholarPubMed
Haseeb, M. A., Eveland, L. K. & Fried, B. (1985). The uptake, localization and transfer of [4-14C]-cholesterol in Schistosoma mansoni males and females maintained in vitro. Comparative Biochemistry and Physiology 82A, 421–3.CrossRefGoogle Scholar
Henrichs, S. M. & Farrington, J. W. (1979). Amino acids in interstitial waters of marine sediments. Nature, London 279, 319–22.CrossRefGoogle Scholar
Hockley, D. J. (1973). Ultrastructure of the tegument of Schistosoma. In Advances in Parasitology, vol. 11 (ed. Dawes, B.), pp. 233305. New York: Academic Press.Google Scholar
Hockley, D. J. & Mclaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 1325.CrossRefGoogle ScholarPubMed
Howells, R. E. & Chen, S. N. (1981). Brugia pahangi: feeding and nutrient uptake in vitro and in vivo. Experimental Parasitology 51, 4258.CrossRefGoogle ScholarPubMed
Hulinska, D., Grim, M. & Shaikenov, B. (1985). The feeding mechanism of intracellular muscle larvae, Trichinella nativa Britov et Boev, 1972 and T. pseudospiralis Garkavi, 1972. Folia Parasitologica 32, 61–6.Google Scholar
Isseroff, H., Bonta, C. Y. & Levy, M. G. (1972). Monosaccharide absorption by Schistosoma mansoni. I. Kinetic characteristics. Comparative Biochemistry and Physiology 43A, 849–58.CrossRefGoogle Scholar
Isseroff, H. & Read, C. P. (1974). Studies on membrane transport. VIII. Absorption of monosaccharides by Fasciola hepatica. Comparative Biochemistry and Physiology 47A, 141–52.CrossRefGoogle Scholar
Isseroff, H. & Walczak, I. M. (1971). Absorption of acetate, pyruvate and certain Krebs cycle intermediates by Fasciola hepatica. Comparative Biochemistry and Physiology 39B, 1017–21.Google Scholar
Jaffe, J. J. & Doremus, H. M. (1970). Metabolic patterns in Dirofilaria immitis microfilariae in vitro. Journal of Parasitology 56, 254–60.CrossRefGoogle ScholarPubMed
Jenkins, D. C. & Erasmus, D. A. (1971). The ultrastructure of the intestine of Ascaris suum larvae. Zeitschrift für Parasitenkunde 35, 173–87.Google ScholarPubMed
Kasschau, M. R. & Dresden, M. H. (1986). Schistosoma mansoni: characterization of hemolytic activity from adult worms. Experimental Parasitology 61, 201–9.CrossRefGoogle ScholarPubMed
Kasschau, M. R., Robinson, D. C. & Dresden, M. (1986). Schistosoma mansoni: activation of hemolytic activity in homogenates from live adult worms. Experimental Parasitology 62, 442–9.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1963). Feeding in some monogenean skin parasites; Entobdella soleae on Solea solea and Acanthocotyle sp. on Raia clavata. Journal of the Marine Biological Association of the United Kingdom 43, 749–66.CrossRefGoogle Scholar
Kennedy, M. W., Foley, M., Kuo, Y. -M., Kusel, J. R. & Garland, B. (1987). Biophysical properties of the surface lipid of parasitic nematodes. Molecular and Biochemical Parasitology 22, 233–40.CrossRefGoogle ScholarPubMed
Kharat, I. & Harinath, B. C. (1985). Uptake of 14C-labelled sugars and amino acids by Wuchereria bancrofti microfilariae in vitro. Indian Journal of Experimental Biology 23, 118–19.Google ScholarPubMed
Køie, M. (1987). Scanning electron microscopy of rediae, cercariae, metacercariae and adults of Mesorchis denticulatus (Rudolphi, 1802) (Trematoda, Echinostomitidae). Parasitology Research 73, 50–6.CrossRefGoogle ScholarPubMed
LaRue, G. R. (1927). A new species of Strigea from the herring gull, Larus argentatus (Pont.), with remarks on the function of the hold-fast organ. Journal of Parasitology 13, 226.Google Scholar
Lee, D. L. (1962). Studies on the function of the pseudosuckers and holdfast organ of Diplostomum phoxini Faust (Strigeida, Trematoda). Parasitology 52, 103–12.CrossRefGoogle Scholar
Lee, D. L. (1966). The structure and composition of the helminth cuticle. In Advances in Parasitology, vol. 4 (ed. Dawes, B.), pp. 187254. New York: Academic Press.Google Scholar
Lee, D. L. & Atkinson, H. J. (1977). Physiology of Nematodes, 2nd edn.New York: Columbia University Press.Google Scholar
Lee, D. L. & Wright, K. A. (1985). Aspects of cuticle structure and some membrane specializations in Trichinella spiralis as seen in freeze-fracture preparations. In Trichinellosis, Proceedings of the Sixth International Conference of Trichinellosis (ed. Kim, C. W.), pp. 168172. Albany: The State University of New York Press.Google Scholar
Levy, M. G. & Read, C. P. (1975). Relation of tegumentary phosphohydrolase to purine and pyrimidine transport in Schistosoma mansoni. Journal of Parasitology 61, 648–56..CrossRefGoogle ScholarPubMed
Lichtenfels, J. R., Pilitt, P. A. & Wergin, W. P. (1987). Dirofilaria immitis: fine structure of cuticle during development in dogs. Proceedings of the Helminthological Society of Washington 54, 133–40.Google Scholar
Llewellyn, J. (1954). Observations on the food and the gut pigment of the Polyopisthocotylea (Trematoda: Monogenea). Parasitology 44, 428–37.CrossRefGoogle ScholarPubMed
Lumsden, R. D. (1975). Surface ultrastructure and cytochemistry of parasitic helminths. Experimental Parasitology 37, 267339.CrossRefGoogle ScholarPubMed
Lyons, K. (1970). The fine structure and function of the adult epidermis of two parasitic monogeneans, Entobdella soleae and Acanthocotyle elegans. Parasitology 60, 3952.CrossRefGoogle ScholarPubMed
Lyons, K. M. (1973). The epidermis and sense organs of the Monogenea and some related groups. In Advances in Parasitology, vol. 11 (ed. Dawes, B.), pp. 193232. New York: Academic Press.Google Scholar
Maizels, R. M., De Savigny, D. & Ogilvie, B. M. (1984). Characterization of surface and excretory antigens of Toxocaris canis infective larvae. Parasite Immunology 6, 2337.CrossRefGoogle Scholar
Mansour, T. E. (1959). Studies on the carbohydrate metabolism of the liver fluke Fasciola hepatica. Biochimica et Biophysica Acta 34, 456–64.CrossRefGoogle ScholarPubMed
Martin, R. E., Foster, L. A., Kester, A. S. & Donahue, M. J. (1987). Ascaris lumbricoides suum: morphological characterization of apparent cuticular pores by ionic permeability and electron microscopy. Experimental Parasitology 63, 329–36.CrossRefGoogle ScholarPubMed
Martinez-Palomo, A. (1978). Ultrastructural characterization of the cuticle of Onchocerca volvulus microfilariae. Journal of Parasitology 64, 127–36.CrossRefGoogle Scholar
McManus, D. P. & James, B. L. (1975). The absorption of sugars and organic acids by the daughter sporocysts of Microphallus similis (Jag.). International Journal for Parasitology 5, 33–8.CrossRefGoogle Scholar
Mercer, J. G. & Chappell, L. H. (1985). Schistosoma mansoni: effect of maintenance in vitro on the uptake and incorporation of leucine by adult worms. Molecular and Biochemical Parasitology 15, 327–37.CrossRefGoogle ScholarPubMed
Mercer, J. G. & Chappell, L. H. (1986). The effect of maintenance in vitro on glucose uptake and the incorporation of glucose into glycogen by adult Schistosoma mansoni. International Journal for Parasitology 16, 253–61.CrossRefGoogle ScholarPubMed
Mettrick, D. F. & Podesta, R. B. (1974). Ecological and physiological aspects of helminth – host interactions in the mammalian gastrointestinal canal. In Advances in Parasitology, vol. 12 (ed. Dawes, B.), pp. 183279. New York: Academic Press.Google Scholar
Miller, F. H. Jr, Tulloch, G. S. & Kuntz, R. E. (1972). Scanning electron microscopy of integumental surface of Schistosoma mansoni. Journal of Parasitology 58, 693–8.CrossRefGoogle ScholarPubMed
Mopper, K. & Lindroth, P. (1982). Diet and depth variations in dissolved free amino acids and ammonium in the Baltic Sea determined by shipboard HPLC analysis. Limnology and Oceanography 27, 336–47.CrossRefGoogle Scholar
Mukhopadhay, D. P., Maity, C. R., Sengupta, A., Majumdar, G. & Ghosal, S. K. (1985). Nutritional requirement of folic acid in Ascaris lumbricoides and the role of cuticle and gut in its absorption. Indian Journal of Medical Research 82, 311–15.Google Scholar
Nollen, P. M. (1968). Uptake and incorporation of glucose, tyrosine, leucine, and thymidine by adult Philophthalmus megalurus (Cort, 1914) (Trematoda) as determined by autoradiography. Journal of Parasitology 54, 295304.CrossRefGoogle ScholarPubMed
Nollen, P. M. & Nadakavukaren, M. J. (1974). Observations on ligated adults of Philophthalmus megalurus, Gorgoderina attenuata, and Megalodiscus temperatus by scanning electron microscopy and autoradiography. Journal of Parasitology 60, 921–4.CrossRefGoogle Scholar
Öhman, C. (1965). The structure and function of the adhesive organ in strigeid trematodes. II. Diplostomum spatheceum Braun, 1893. Parasitology 55, 481502.CrossRefGoogle Scholar
Ortega-Pierres, G., Clark, N. T. W. & Parkhouse, R. M. E. (1986). Regional specialization of the surface of nematodes. Parasite Immunology 8, 613–17.CrossRefGoogle Scholar
Pantelouris, E. M. & Gresson, R. A. R. (1960). Autoradiographic studies on Fasciola hepatica L. Parasitology 50, 165–9.CrossRefGoogle Scholar
Pappas, P. W. (1971). Haemotaloechus medioplexus: uptake, localization, and fate of tritiated arginine. Experimental Parasitology 30, 102–19.CrossRefGoogle ScholarPubMed
Pappas, P. W. & Read, C. P. (1975). Membrane transport in helminth parasites: a review. Experimental Parasitology 37, 469530.CrossRefGoogle ScholarPubMed
Parkening, T. A. & Johnson, A. D. (1969). Glucose uptake in Haematoloechus medioplexus and Gorgoderina trematodes. Experimental Parasitology 25, 358–67.CrossRefGoogle ScholarPubMed
Philipp, M., Parkhouse, R. M. E. & Ogilvie, B. M. (1980). Changing proteins on surface of parasitic nematodes. Nature, London 287, 538.CrossRefGoogle Scholar
Podesta, R. B. (1982). Membrane physiology of helminths. In Membrane Physiology of Invertebrates (ed. Podesta, R. B.), pp. 121177. New York: Marcel Dekker.Google Scholar
Poinar, G. O. Jr & Hess, R. (1972). Food uptake by the insect-parasitic nematode, Sphaerularia bombi (Tylenchida). Journal of Nematology 4, 270–7.Google ScholarPubMed
Poinar, G. O. Jr & Hess, R. (1977). Romanomermis culicivorax: morphological evidence of transcuticular uptake. Experimental Parasitology 42, 2733.CrossRefGoogle ScholarPubMed
Popiel, I. & Basch, P. F. (1984). Reproductive development of female Schistosoma mansoni (Digenea: Schistosomatidae) following bisexual pairing of worms and worm segments. Journal of Experimental Zoology 232, 141–50.CrossRefGoogle ScholarPubMed
Preston, C. M., Jenkins, T. & McLaren, D. J. (1986). Surface properties of developing stages of Trichuris muris. Parasite Immunology 8, 597611.CrossRefGoogle ScholarPubMed
Read, C. P. (1970). Parasitism and Symbiology. New York: The Ronald Press.Google Scholar
Riding, I. L. (1970). Microvilli on the outside of a nematode. Nature, London 226, 179–80.CrossRefGoogle ScholarPubMed
Riley, J. P., Robertson, D. E., Dutton, J. W. R., Mitchell, N. T. & Williams, R. J.Le, B. (1975). Analytical chemistry of sea water. In Chemical Oceanography, vol. 3, 2nd edn. (ed. Riley, J. P. and Skirrow, G.), pp. 193514. New York: Academic Press.Google Scholar
Roberts, L. S. & Fairbairn, D. (1965). Metabolic studies on adult Nippostrongylus brasiliensis (Nematoda: Trichostrongyloidea). Journal of Parasitology 51, 129–38.CrossRefGoogle ScholarPubMed
Roche, M. & Torres, C. M. (1960). A method for in vitro study of hookworm activity. Experimental Parasitology 9, 250–6.CrossRefGoogle ScholarPubMed
Rogers, S. H. & Bueding, E. (1975). Anatomical localization of glucose uptake by Schistosoma mansoni adults. International Journal for Parasitology 5, 369–71.CrossRefGoogle ScholarPubMed
Rogers, W. P. & Lazarus, M. (1949). The uptake of radioactive phosphorus from host tissue and fluids by nematode parasites. Parasitology 39, 245–50.CrossRefGoogle ScholarPubMed
Roy, T. K. (1982). Hydrolytic enzymes and membrane digestion in parasitic platyhelminths. Journal of Scientific and Industrial Research 41, 439–54.Google Scholar
Rutherford, T. A. & Webster, J. M. (1974). Transcuticular uptake of glucose by the entomophilic nematode, Mermis nigrescens. Journal of Parasitology 60, 804–8.CrossRefGoogle ScholarPubMed
Rutherford, T. A., Webster, J. M. & Barlow, J. S. (1977). Physiology of nutrient uptake by the entomophilic nematode Mermis nigrescens (Mermithidae). Canadian Journal of Zoology 55, 1773–81.CrossRefGoogle Scholar
Smyth, J. D. & Halton, D. W. (1983). The Physiology of Trematodes, 2nd edn.Cambridge: Cambridge University Press.Google Scholar
Southgate, V. R. (1970). Observations on the epidermis of the miracidium and on the formation of the tegument of the sporocyst of Fasciola hepatica. Parasitology 61, 177–90.CrossRefGoogle ScholarPubMed
Stewart, G. L. & Giannini, S. H. (1982). Sarcocystis, Trypanosoma, Toxoplasma, Brugia, Ancylostoma, and Trichinella spp.: a review of the intracellular parasites of striated muscle. Experimental Parasitology 53, 406–47.CrossRefGoogle ScholarPubMed
Stewart, G. L., Raines, K. M. & Kilgore, M. W. (1986). Glucose absorption in vitro by the enteric stages of Trichinella spiralis. Parasitology 93, 581–6.CrossRefGoogle ScholarPubMed
Threadgold, L. T. (1984). Parasitic platyhelminths. In Biology of the Integument, vol. 1 (ed. Bereiter-Hahn, J.Matoltsy, A. G. and Richards, K. S.), pp. 132191. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Todd, J. R. & Ross, J. G. (1966). Origin of hemoglobin in the cecal contents of Fasciola hepatica. Experimental Parasitology 19, 151–4.CrossRefGoogle ScholarPubMed
Uglem, G. L. (1980). Sugar transport by larval and adult Proterometra macrostoma (Digenea) in relation to environmental factors. Journal of Parasitology 66, 748–58.CrossRefGoogle ScholarPubMed
Uglem, G. L. (1987). Environmental sodium regulates cutaneous sugar transport in a digenean fluke. Parasitology 94, 16.CrossRefGoogle Scholar
Uglem, G. L. & Lee, K. J. (1985). Proterometra macrostoma (Trematoda: Azygiidae): functional morphology of the tegument of redia. International Journal for Parasitology 15, 61–4.CrossRefGoogle ScholarPubMed
Uglem, G. L. & Read, C. P. (1975). Sugar transport and metabolism in Schistosoma mansoni. Journal of Parasitology 61, 390–7.CrossRefGoogle ScholarPubMed
Uglem, G. L., Lewis, M. C. & Larson, O. R. (1985). Niche segregation and sugar transport capacity of the tegument in digenean flukes. Parasitology 91, 121–7.CrossRefGoogle Scholar
Voge, M., Price, Z. & Bruckner, D. A. (1978). Changes in tegumental surface during development of Schistosoma mansoni. Journal of Parasitology 64, 585–92.CrossRefGoogle ScholarPubMed
Watts, S. D. M. (1972). Amino acid flux in the sporocysts of Cercaria emasculans Pelsener, 1906 in vitro. Parasitology 64, 114.CrossRefGoogle ScholarPubMed
Weatherly, N. F., Hansen, M. F. & Moser, H. C. (1963). In vitro uptake of C14-labelled alanine and glucose by Ascaridia galli (Nematoda) of chickens. Experimental Parasitology 14, 3748.CrossRefGoogle Scholar
Zussman, R. A., Bauman, P. M. & Petruska, J. C. (1970). The role of ingested hemoglobin in the nutrition of Schistosoma mansoni. Journal of Parasitology 56, 75–9.CrossRefGoogle ScholarPubMed