Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T12:35:53.608Z Has data issue: false hasContentIssue false

Intestinal migration in the life-cycle of Pseudodiplorchis americanus (Monogenea)

Published online by Cambridge University Press:  06 April 2009

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

Summary

Adults of Pseudodiplorchis americanus occur in the host's urinary bladder, the typical habitat of polystomatid monogeneans in amphibians. However, larvae which invade the respiratory tract via the nostrils then migrate to the bladder through the stomach and intestine, a route which is without precedent amongst monogeneans. Parasite transmission is correlated with the spawning of the desert toad Scaphiopus couchii (June/July in Arizona, USA) and the gut migration, which takes as little as 5 min, occurs after 26 days post-infection (p.i.). Migration occurs during the host's feeding season, and therefore the parasites normally encounter maximum digestive activity along their path. Worms transferred experimentally from respiratory tract to the digestive fluids in the gut are killed within 60 s. However, natural migration is stimulated by an unidentified host factor which triggers protective adaptations, enabling parasite survival for up to 4 h in these lethal conditions. Without this essential stimulus, migration may be delayed for over 1 year and juveniles remaining in the respiratory tract undergo no development beyond that reached at 4 weeks p.i. Rapid reproductive development is resumed immediately after migration, leading to maturation around 1 month later and progressive accumulation of embryos in utero in preparation for transmission during the next summer's rains.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1986

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

Allen, K. M. (1984). Ultrastructural adaptations of the host-parasite interface of polystomatid monogeneans. Ph.D. thesis, University of London.Google Scholar
Calow, P. & Jennings, J. B. (1974). Calorific values in the phylum Platyhelminthes: the relationship between potential energy, mode of life and the evolution of entoparasitism. Biological Bulletin 147, 8194.CrossRefGoogle ScholarPubMed
Combes, C. (1968). Biologie, écologie des cycles et biogéographiede Digènes et Monogènesd' Amphibiens dans l'Est des Pyrénées. Mémoires du Museum National l'Histoire Naturelle, Paris, Nouvelle série A 51, 1195.Google Scholar
Combes, C. (1981). Invasion strategies in parasites of amphibious hosts. Third European Multicolloquium of Parasitology, Parasitology 82 (4), 63–4.Google Scholar
Dimmitt, M. A. & Ruibal, R. (1980 a). Exploitation of food resources by spadefoot toads (Scaphiopus). Copeia 1980(4), 854–62.CrossRefGoogle Scholar
Dimmitt, M. A. & Ruibal, R. (1980 b). Environmental correlates of emergence in spadefoot toads (Scaphiopus). Journal of Herpetology 14, 21–9.CrossRefGoogle Scholar
Gallien, L. (1935). Recherches experiméntales sur la dimorphisme évolutif et la biologie de Polystoma integerrimum Fröhl. Traveaux du Station de Zoologie, Wimereux 12, 1181.Google Scholar
Gussev, A. V. & Fernando, C. H. (1973). Dactylogyridae (Monogenoidea) from the stomach of fishes. Folia Parasitologica, (Praha) 20, 207–12.Google Scholar
Halton, D. W. (1967). Studies on glycogen deposition in Trematoda. Comparative Biochemistry and Physiology 23, 113–20.CrossRefGoogle ScholarPubMed
Halton, D. W. (1974). Haemoglobin absorption in the gut of a monogenetic trematode, Diclidophora merlangi. Journal of Parasitology 60, 5966.Google 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.Google Scholar
Hillyard, S. D. (1975). The role of the antidiuretic hormones in the water economy of the spadefoot toad, Scaphiopus couchi. Physiological Zoology 48, 242–51.Google Scholar
Hobson, B. M. & Townsend, B. G. (1964). The anaesthetic action of di-ethyl ether, ethyl carbamate and tricaine methanesulfonate upon Xenopus laevis. In Small Animal Anaesthesia (ed. O., Graham-Jones), pp. 4758. London: Pergamon Press.Google Scholar
Jennings, J. B. (1959). Studies on digestion in the monogenetic trematode Polystoma integerrimum. Journal of Helminthology 33, 197204.CrossRefGoogle ScholarPubMed
Lawson, J. R. & Wilson, R. A. (1980). Metabolic changes associated with the migration of the schistosomulum of Schistosoma mansoni in the mammal host. Parasitology 81, 325–36.CrossRefGoogle ScholarPubMed
Llewellyn, J. (1965). The evolution of parasitic platyhelminths. In Third Symposium of the British Society for Parasitology (ed. Taylor, A. E. R.), pp. 4778. Oxford: Blackwell Scientific Publications.Google Scholar
McClanahan, L. JR. (1967) Adaptations of the spadefoot toad, Scaphiopus couchi, to desert environments. Comparative Biochemistry and Physiology 20, 7399.CrossRefGoogle Scholar
Mettrick, D. F. & Cho, C. H. (1981). Effect of electrical vagal stimulation on migration of Hymenolepis diminuta. Journal of Parasitology 67, 386–90.CrossRefGoogle ScholarPubMed
Mettrick, D. F. & Cho, C. H. (1982). Changes in tissue and intestinal serotonin (5-HT) levels in the laboratory rat following feeding and the effect of 5-HT inhibitors on the migratory response of Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 60, 790–7.CrossRefGoogle Scholar
Mettrick, D. F. & Podesta, R. B. (1982). Effect of gastrointestinal hormones and amines on intestinal motility and the migration of Hymenolepis diminuta in the rat small intestine. International Journal for Parasitology 12, 151–4.CrossRefGoogle ScholarPubMed
Middler, S. A., Kleeman, C. R. & Edwards, E. (1968). Influence of tricaine methane sulfonate anesthesia on fluid and salt metabolism of the toad, Bufo marinus. Comparative Biochemistry and Physiology 24, 1065–7.Google Scholar
Murith, D. (1982). Etude in vivo de la nature des relations hôte–parasite dans le complexe Amphibien-Polystome (Monogenea). Revue suisse de Zoologie 89, 957–65.CrossRefGoogle Scholar
Neminen, M., Laitinen, M. & Pasanen, P. (1982). Effects of anaesthesia with tricaine (MS 222) on the blood composition of the Splake (Salvelinus fontinalis x Salvelinus namaycush). Comparative Biochemistry and Physiology 73C, 271–6.Google Scholar
Paperna, I. (1963). Enterogyrus cichlidarum n.gen. n.sp., a monogenetic trematode parasitic in the intestine of a fish. Bulletin of the Research Council, Israel 11 (B), 183–7.Google Scholar
Ruibal, R., Tevis, L. & Roig, V. (1969). The terrestrial ecology of the spadefoot toad Scaphiopus hammondii. Copeia 1969(3), 571–84.Google Scholar
Seymour, R. S. (1973). Gas exchange in spadefoot toads beneath the ground. Copeia 1973(3), 452–60.CrossRefGoogle Scholar
Soivio, A., Nyholm, K. & Huhti, M. (1977). Effects of anaesthesia with MS 222, neutralised MS 222 and benzocaine on the blood constituents of rainbow trout, Salmo gairdneri. Journal of Fish Biology 10, 91101.CrossRefGoogle Scholar
Sommerville, R. I. (1977). Development of Haemonchus contortus in vitro and the stimulus from the host. Journal of Parasitology 63, 344–7.Google Scholar
Tinsley, R. C. (1973). Ultrastructural studies on the form and function of the gastrodermis of Protopolystoma xenopi (Monogenoidea: Polyopisthocotylea). Biological Bulletin 144, 541–55.Google Scholar
Tinsley, R. C. (1982 a). Pseudodiplorchis americanus (Monogenea): synchronisation of transmission with restricted host availability. Proceedings of the Fifth International Congress of Parasitology: Molecular and Biochemical Parasitology, Suppl. p. 459.Google Scholar
Tinsley, R. C. (1982 b). The reproductive strategy of a polystomatid monogenean in a desert environment. Parasitology 85, xv.Google Scholar
Tinsley, R. C. (1983). Ovoviviparity in platyhelminth life-cycles. Parasitology 86, 161–96.Google Scholar
Tinsley, R. C. (1984). Pulsed parasite transmission between desert-adapted amphibians. Parasitology 89, vi.Google Scholar
Tinsley, R. C. & Earle, C. M. (1983). Invasion of vertebrate lungs by the polystomatid monogeneans Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 86, 501–17.CrossRefGoogle Scholar
Wedemeyer, G. (1970). Stress of anesthesia with M.S. 222 and benzocaine in rainbow trout (Salmo gairdneri). Journal of the Fisheries Research Board of Canada 27, 909–14.Google Scholar