THE SITES OCCUPIED BY SOME PARASITIC HELMINTHS IN THE ALIMENTARY TRACT OF VERTEBRATES
Authors: CROMPTON D. W. T. 
Published: August 2010

1. The sites occupied by adult helminths in the alimentary tracts of vertebrates, the events leading to the establishment of the helminths in these sites and some of the factors involved in extensions or changes of site have been described and discussed in an attempt to summarize the present state of knowledge and stimulate more research into the ecology of helminths in the tract.

2. In an attempt to reduce confusion and ambiguity in the future literature on the ecology of helminths, definitions have been proposed for the terms site, emigration and migration.

3. Since it has been assumed that the distribution and survival of some species of helminth in the tract are related to phases of digestive activity or inactivity, the morphology, histology and physiology of the alimentary tract of vertebrates have been considered with emphasis on events and features which appear to be of significance to helminths.

4. Many phases of a helminth's association with its host appear to be related to the host's intestinal motility.

5. Digestion in vertebrates is considered to be an ordered sequence of events producing different conditions in different parts of the tract. These conditions, however, are not entirely predictable; digestion is affected by the nature of the diet, the feeding routine and the psychosomatic state of the animal in question.

6. An accurate description of a helminth's site is fundamental to our understanding of its ecology. The description should include information about (I) the helminth's linear distribution, (2) the helminth's radial distribution, (3) the length of time which passed between the death of the host and finding the parasites, (4) the time of day when the search was made, (5) the stage of digestion in progress on the death of the host, (6) the season of the year when the parasites were observed, (7) the parasite's reproductive state and (8) the worm burden and the other species of parasite present in the host's alimentary tract.

7. Special care must be taken when describing the site of a cestode because of the nature of the strobila and the degrees of independent existence shown by the proglot‐tids of certain species.

8. The distribution of sites occupied by the adults of 252 species of helminth in the alimentary tract of vertebrates is given in Tables 2–6, and some sites are illustrated diagrammatically in Figs. 36–57. The sites given in the tables should be accepted with caution, for not all the authors recognized the need for information of the type proposed in paragraph 6 above.

9. The adult stages of most species of Acanthocephala and of most species of Cestoda are confined to the lumen and paramucosal lumen of the small intestines of their hosts. Their mode of feeding and dependence on their hosts' digestive processes fit in with their observed distribution. Acanthocephalans and cestodes are likely to be competitors because their restriction to the small intestine and their feeding behaviour suggest that they may have similar ecological niches.

10. The adult stages of Nematoda can be found in most regions of the alimentary tract, from the mouth to the rectum and from the lumen to the serosa. They do not appear to be successful parasites of the biliary system. The occupation of so many sites in the tract by nematodes may be correlated with the small size of many species and the fact that many species feed independently of their hosts' digestive activity.

11. The co‐existence of various species of nematode in the same site may result from their varied dietary requirements and feeding habits.

12. Although the sites of adult digenetic Trematoda are to be found throughout the length of the alimentary tract, most species appear to be restricted to the paramucosal lumen and mucosal and epithelial tissues. Their limited radial distribution may be related to the conclusion that most species have become adapted to feeding on the mucosa and material associated with it.

13. The observation that some species of helminth occupy different sites in the tracts of related hosts shows that some helminths can tolerate conditions as varied as those in the anterior part of the small intestine of one host and those in the posterior part of another are believed to be. Thus, the fact that a helminth is usually found in a particular zone of the host's tract does not necessarily indicate that it is dependent upon the conditions prevailing there.

14. The events leading to the establishment of the adults of many species in their sites can be considered in three general categories; (I) the direct arrival of immature stages in the site of the adults, (2) emigration by the immature stages in the direction of gastro‐intestinal flow to the site of the adults, and (3) emigration by the immature stages against the direction of gastro‐intestinal flow.

15. Much of the evidence for emigrations is indirect, circumstantial and difficult to interpret.

16. Circumstantial evidence and the results of experiments involving the transplantation of helminths from one host to another indicate that both immature and adult stages of several species of helminth can orientate themselves in the alimentary tract and find their normal sites.

17. Extensions of site occur in response to both intra‐ and interspecific reactions. In the case of an intraspecific reaction, extension of site is usually indicative of an increase in population density.

18. What determines the populations of different helminths in the alimentary tract of vertebrates has been insufficiently investigated. More studies are needed if the ecology of helminths is to be understood.

19. In the case of interspecific reactions, some species of helminth change site or become confined to one part of their normal site when another species is present.

20. Some species of helminth appear to extend or change their site in response to an immunological reaction of the host.

21. In general, adult helminths emigrate less than their immature stages. Extensions and changes of site may ensure the survival of the infection during events which are deleterious to individual parasites.

22. The conclusions in paragraphs 9–21 are based on information recorded in the references cited in Tables 2, 3, 4 and 6. They may not apply to all the species of helminth known to live in the alimentary tract.

23. The cestode Hymenolepis diminuta undergoes an exogenous, circadian migration in the small intestine of rats. The migration is superimposed on the anterior emigration and involves the cestode's release of its hold on the mucosa and its attachment elsewhere. There is corresponding change in the position of the biomass, the migration being related in some way to the feeding and digestive activity of the host. Decisive experiments are needed to elucidate the nature of this relationship.

24. Some preliminary observations suggest that other species of helminth make periodic migrations in the tracts of their hosts.

In addition to the acknowledgements already made, I also thank the following publishers and copyright owners: Blackwell Scientific Publications for Figs. 1, 4, 6, 47, 56 and 57; Cambridge University Press for Figs. 36, 38 and 39, and Figs. 2, 40, 42, 52, 54 and 55 from Parasitology; Urban & Schwarzenberg for Figs. 3, 5 and 8; Company of Biologists Ltd. for Fig. 20; Prof. John Morton for Fig. 21; Mrs E. C. Greene for Fig. 23; Cornell University for Fig. 27; Dr P. M. Hine for Fig. 37; Marine Biological Association of the United Kingdom for Fig. 41; Academic Press for Figs. 43, 44 and 46 from Experimental Parasitology; Macmillan (Journals) Ltd. for Fig. 48 from Nature; American Society of Parasitologists for Fig. 49 from Journal of Parasitology; Pergamon Press Ltd. for Fig. 50 from International Journal for Parasitology; Editorial and publications section of C.S.I.R.O. for Fig. 53.