Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-31T20:30:58.743Z Has data issue: false hasContentIssue false
  • English
  • Français

Optimal habitat selection by helminths within the host environment

Published online by Cambridge University Press:  07 April 2017

M. V. K. Sukhdeo  and
S. C. Sukhdeo
M. V. K. Sukhdeo
Affiliation:
Department of Animal Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ 08903 USA
S. C. Sukhdeo
Affiliation:
Department of Animal Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ 08903 USA
Get access Rights & Permissions [Opens in a new window]

Summary

Helminth parasites of vertebrates usually select very specific regions or habitats in their hosts, and this is often preceded by a tortuous migration through various host organs. However, the proximate mechanisms of migration and habitat selection have remained enigmatic despite considerable effort by parasitologists. In this paper, a new approach to studying helminth behaviour in the host is proposed. The core idea is that behaviour strategies must be considered from the perspective of the parasites and their perceptions of their environment. A guiding principle is that the environmental features to which an animal responds, and the actions which are required for responding to the environment, form a fundamental unit of behaviour. Thus, we can deduce an animal's behavioural strategy from the details of its response to environmental signals and from its sensory capabilities. The evidence presented suggests that helminth behaviours in the host often occur as fixed (or modal) action patterns which are usually seen in response to constant, or predictable environmental features. Thus, a working hypothesis is that the mechanisms of physiological and biochemical homeostasis within the host provide an extremely predictable environment for the parasite. Under these conditions, a parasite needs to perceive only small subsets of the total information available from the environment to respond appropriately. Studies on sensory and nervous systems of these organisms are critical to understanding parasite perception, but there are formidable technical obstacles that prevent easy access to parasite nervous systems. Therefore, a multidisciplinary approach, using ideas from parasitology, ecology, evolutionary biology and neuroethology, is considered requisite for reconstructing the parasites' behaviour strategies. It is suggested that future directions should pursue integration of studies on sensory physiology with the behavioural ecology of these organisms.

Keywords

Behaviourenvironmenthabitat selectionhelminth parasites
Type
Research Article
Information
Parasitology , Volume 109 , supplement S1: Parasites and behaviour , 1994 , pp. S41 - S55
Copyright
Copyright © Cambridge University Press 1994

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

Alcock, J. (1979). Animal Behavior: An Evolutionary Approach. Sunderland: Sinauer Associates Inc.Google Scholar
Allee, W. C, Emerson, A. E., Park, O., Park, T. & Schmidt, K. P. (1949). Principles of Animal Ecology. Philadelphia: W. B. Saunders, Co.Google Scholar
Al-Saffar, A. (1984). Analysis of the control of intestinal motility in fasted rats with special reference to neurotensin. Scandinavian Journal of Gastroenterology 19, 422–8.CrossRefGoogle ScholarPubMed
Arai, H. P. (1980). Migratory activity and related phenomena in Hymenolepis diminuta. In Biology of the tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 615–32. New York: Academic Press.CrossRefGoogle Scholar
Arms, K. & Camp, P. (1987). Biology. (3rd edn.) Philadelphia: Saunders College Publishing.Google Scholar
Bansemir, A. D. & Sukhdeo, M. V. K. (1994). The food resource of adult Heligmosomoides polygyrus in the small intestine. Journal of Parasitology 79, 24–8.CrossRefGoogle Scholar
Barlow, G. W. (1977). Modal action patterns. In How Animals Communicate (ed. Sebeok, T. A.), pp. 87–100. Bloomington: Indiana University Press.Google Scholar
Barton, R. A., Whiten, S.C., Strums, R. W., Byrne, R. W. & Simpson, A. J. (1992). Habitat use and resource availability in baboons. Animal Behavior 43, 831–44.CrossRefGoogle Scholar
Bates, R. M. & Kennedy, C. R. (1991). Site availability and density-dependent constraints on the acanthocephalan Pomphorhynchus laevis in rainbowtrout, Oncorhynchus mykiss (Walbaum). Parasitology 102, 405–10.CrossRefGoogle Scholar
Bawden, R. J. (1969). Some effects of the diet of mice on Nematospiroides dubius (Nematoda). Parasitology 59, 203–13.CrossRefGoogle Scholar
Beaver, P.C., Yoshida, Y. & Ash, L. R. (1964). Mating of Ancylostoma caninum in relation to blood loss in the host. Journal of Parasitology 50, 286–93.CrossRefGoogle ScholarPubMed
Blair, K. L. & Anderson, P. A. V. (1993). Properties of voltage-activated ionic currents in cells from the brains of the triclad flatworm Bdelloura Candida. Journal of Experimental Biology 185, 267–86.CrossRefGoogle Scholar
Bonner, T. P. & Etges, F. J. (1967). Chemically mediated sexual attraction in Trichinella spiralis. Experimental Parasitology 21, 53–60.CrossRefGoogle ScholarPubMed
Bullock, T. H. (1984). Comparative neuroethology of startle, rapid escape, and giant fiber-mediated responses. In Neural Mechanisms of Startle Behavior (ed. Eaton, R.C.), pp. 1–13. New York: Plenum Press.Google Scholar
Carter, M. C. & Dixon, A. F. G. (1982). Habitat quality and the foraging behavior of coccinellid larvae. Journal of Animal Ecology 51, 865–78.CrossRefGoogle Scholar
Chalfie, M. & White, J. (1988). The nervous system. In The Nematode Caenorhabditis elegans (ed. Wood, W. B.), pp. 337–391. Cold Spring Harbor: Cold Spring Harbor Laboratory.Google Scholar
Chernin, E. (1974). Some host-finding attributes of Schistosoma mansoni miracidia. American Journal of Tropical Medicine and Hygiene 23, 320–7.CrossRefGoogle ScholarPubMed
Cody, M. L. (1985). Habitat Selection in Birds. New York: Academic Press.Google Scholar
Croll, N. A. (1972). Behaviour of larval nematodes. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. V. & Wright, C. A.), pp. 31–52. London: Academic Press.Google Scholar
Crompton, D. W. T. (1973). The sites occupied by some parasitic helminths in the alimentary tract of vertebrates. Biological Reviews 48, 27–83.CrossRefGoogle ScholarPubMed
Dawes, B. (1963). The migration of juvenile forms of Fasciola hepatica L. through the wall of the intestine in the mouse, with some observations of food and feeding. Parasitology 53, 109–22.CrossRefGoogle Scholar
DAWes, B. & Hughes, D. L. (1964). Fascioliasis: the invasive stages of Fasciola hepatica in mammalian hosts. Advances in Parasitology 2, 97–165.CrossRefGoogle ScholarPubMed
Delcomyn, F. (1980). Neural basis of rhythmic behavior in animals. Science 210, 492–8.CrossRefGoogle ScholarPubMed
Dill, L. M. (1987). Animal decision making and its ecological consequences: The future of aquatic ecology and behavior. Canadian Journal of Zoology 65, 803–11.CrossRefGoogle Scholar
Doy, T. G. & Hughes, D. L. (1984). Early migration of immature Fasciola hepatica and associated liver pathology in cattle. Research in Veterinary Science 37, 219–22.CrossRefGoogle ScholarPubMed
Dusenbery, D. B. (1992). How Organisms Acquire and Respond to Information. NewYork: W. H. Freeman and Company.Google Scholar
Dyer, F. C. & Brockmann, H. J. (1994). Sensory processes, orientation, and communication: Biology of the Umwelt.In Foundations of Animal Behavior (ed. Houck, L. D., & Drickamer, L.C. ), in press. Chicago University Press.Google Scholar
Erasmus, D. A. (1958). Studies on the morphology, biology and development of a strigeoid cercaria (Cercaria X Baylis 1930). Parasitology 48, 312–35.CrossRefGoogle Scholar
Erasmus, D. A. (1959). The migration of Cercaria X Baylis (Strigeida) within the fish intermediate host. Parasitology 49, 173–90.CrossRefGoogle ScholarPubMed
Ewald, J. A. & Nichol, B. B. (1989). Availability of caecal habitat as a density-dependent limit on survivorship of Leptorhynchoides thecatus in green sunfish, Lepomis cyanellus. Parasitology 98, 447–50.CrossRefGoogle ScholarPubMed
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in platyhelminthes. Parasitology 102 (Suppl.), S77–S92.CrossRefGoogle Scholar
Ferguson, M. S. (1943). Migration and localization of an animal parasite within the host. Journal of Experimental Zoology 93, 375–401.CrossRefGoogle Scholar
Fretwell, S. D. & Lucas, H. L., Jr. (1970). On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheoretica 19, 16–36.CrossRefGoogle Scholar
Fried, B. (1994). Metacercarial excystment of trematodes. Advances in Parasitology 33, 91–144.CrossRefGoogle ScholarPubMed
Hair, J. D. & Holmes, J. C. (1975). The usefulness of measures of diversity, niche width and niche overlap in the analysis of helminth communities in waterfowl. Ada Parasitologica Polonica 23, 253–65.Google Scholar
Halton, D. W., Fairweather, I., Shaw, C. & Johnston, C. F. (1990). Regulatory peptides in parasitic platyhelminths. Parasitology Today 6, 284–90.CrossRefGoogle ScholarPubMed
Halton, D. W., Brennan, G. P., Maule, A. G., Shaw, C. F., Johnston, C. F., & Fairweather, I. (1991). The ultrastructure and immunogold-labelling of pancreatic polypeptide-like immunoreactive cells associated with the egg-forming apparatus of a monogenean parasite, Diclidophora merlangi. Parasitology 102, 429–36.CrossRefGoogle Scholar
Halton, D. W., Shaw, C., Maule, A. G., Johnston, C. F., & Fairweather, I. (1992). Peptidergic messengers: A new perspective of the nervous system of parasitic platyhelminths. Journal of Parasitology 78, 179–93.CrossRefGoogle ScholarPubMed
Harris-Warrick, R. M. & Johnson, B. R. (1989). Motor pattern networks: Flexible foundations for rhythmic pattern production. In Perspectives in Neural Systems and Behavior (ed. Carew, T. J. & Kelley, D. B.), pp. 51–71. New York: Alan Liss.Google Scholar
Haseeb, M. A. & Fried, B. (1988). Chemical communication in helminths. Advances in Parasitology 27, 169–207.CrossRefGoogle ScholarPubMed
Haslewood, G. A. D. (1978). The Biological Importance of Bile Salts.Frontiers in biology 47. Amsterdam: North Holland Publishing Co.Google Scholar
Holmes, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333–47.Google Scholar
Holmes, J. C. (1990). Competition, contacts, and other factors restricting niches of parasitic helminths. Annales de Parasitologie Humaine et Comparée 65 (Suppl.), S69–S72.CrossRefGoogle ScholarPubMed
Holmes, J.C., Hobbs, R. P. & Leong, T. S. (1977). Populations in perspective: community organisation and regulation of parasite populations. In Regulation of Parasite Populations (ed. Esch, G. W.), pp. 209–245. London and New York: Academic Press.Google Scholar
Holmes, J.C. & Price, P. W. (1985). Communities of parasites. In Community Ecology: Pattern and Process (ed. Anderson, D. J. & Kikkawa, J.), pp. 187–213. Oxford: Blackwell Scientific Publications.Google Scholar
Hoyle, G. (1984). The scope of neuroethology. Behavioral and Brain Sciences 7, 367–412.CrossRefGoogle Scholar
Huber, F. (1988). Invertebrate neuroethology: guiding principles. Experientia 44, 428–31.CrossRefGoogle Scholar
Kemp, W. M. & Devine, D. R. (1982). Behavioral cues in trematode life cycles. In Cues that Influence Behavior of Internal Parasites (ed. Bailey, W. S.), pp. 67–84. USDA.Google Scholar
Kennedy, C. R. (1984). Host-parasite interrelationships: strategies of coexistence and coevolution. In Producers and Scroungers (ed. Barnard, C. J.), pp. 34–60. New York: Chapman and Hall.CrossRefGoogle Scholar
Kennedy, C. R. (1985). Site segregation by species of Acanthocephala in fish, with special references to eels, Anguilla anguilla. Parasitology 90, 375–90.CrossRefGoogle Scholar
Keymer, A. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–87.CrossRefGoogle ScholarPubMed
Koopowitz, H. (1974). Some aspects of the physiology and organization of the nerve plexus in polyclad flatworms. In Biology of Turbellaria (ed. Riser, C. J. & Morse, C.J), pp. 198–212. McGraw-Hill Book, Co.Google Scholar
Koopowitz, H. (1982). Free-living platyhelminthes. In Electrical Conduction and Behavior in ‘Simple’ Invertebrates (ed. Shelton, G. A. B.), pp. 359–392. Oxford: Oxford University Press.Google Scholar
Koopowitz, H. & Keenan, L. (1982). The primitive brains of the platyhelminthes. Trends in Neuroscience 5, 77–9.CrossRefGoogle Scholar
Krebs, J. R. & Davies, N. B. (1989). Behavioral Ecology. An Evolutionary Approach. Oxford: Blackwell.Google Scholar
Lackie, A. M. (1975). The activation of infective stages of endoparasites of vertebrates. Biological Reviews 50, 285–323.CrossRefGoogle ScholarPubMed
Lee, T. D. G. & Wright, K. A. (1978). The morphology and probable feeding site of the nematode Trichuris muris (Schrank, 1788) Hall, 1916. Canadian Journal of Zoology 56, 1889–905.CrossRefGoogle ScholarPubMed
LI, H. C. (1933). On the mouth-spear of Trichocephalus trichuris and of a Trichocephalus sp. from monkey, Macacus rhesus. Chinese Medical Journal 47, 1343–6.Google Scholar
Lorenz, K. Z. (1981). The Foundations of Ethology. New York: Springer-Verlag.CrossRefGoogle Scholar
Lumsden, R. D. & Hildreth, M. B. (1983). The fine structure of adult tapeworms. In Biology of the Eucestoda, Vol.1 (ed. Arme, C. & Pappas, P. W.), pp. 177–233. London: Academic Press.Google Scholar
Lumsden, R. D. & Specian, R. (1980). The morphology, histology and fine structure of the adult stage of the cyclophyllidean tapeworm Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 157–280. New York: Academic Press.CrossRefGoogle Scholar
Macinnis, A. J. (1965). Responses of Schistosoma mansoni miracidia to chemical attractants. Journal of Parasitology 51, 731–46.CrossRefGoogle ScholarPubMed
Messner, R. (1988). All 14 Eight-Thousanders. Seattle: The Crowood Press.Google Scholar
Montgomerie, R. F. (1928). Observations of artificial infestation of sheep with Fasciola hepatica and on a phase in the development of the parasite. Journal of Helminthology 16, 71–130.Google Scholar
Morris, D. W. (1987 a). Ecological scale and habitat use. Ecology 68, 362–9.CrossRefGoogle Scholar
Morris, D. W. (1987 b). Spatial scale and the cost of density-dependent habitat selection. Evolutionary Ecology 1, 379–88.CrossRefGoogle Scholar
Morris, D. W. (1989). Density-dependent habitat selection: testing the theory with fitness data. Evolutionary Ecology 3, 80–94.CrossRefGoogle Scholar
Noble, E. R., Noble, G. A., Schad, G. A. & Macinnis, A. J. (1989). Parasitology: The Biology of Animal Parasites. Philadelphia: Lea & Febiger.Google Scholar
Orians, G. H. (1981). Foraging behavior and the evolution of discriminatory abilities. In Foraging Behavior: Ecological, Ethological and Psychological Approaches (ed. Kamil, A. C. & Sargent, T. D.), pp. 389–405. New York: Garland Stpm Press.Google Scholar
Orians, G. H. & Wittenberger, J. F. (1991). Spatial and temporal scales in habitat selection. American Naturalist 137 (Suppl.), S29–S49.CrossRefGoogle Scholar
Oster, G. F. & Wilson, E. O. (1978). Caste and Ecology, pp. 292–315. Princeton: Princeton Unviersity Press.Google ScholarPubMed
Partridge, L. (1978). Habitat selection. In Behavioral Ecology: An Evolutionary Approach (ed. Krebs, J. R. and Davies, N. B.), pp. 351–376. Massachusetts: Sinauer Associates Inc.Google Scholar
Pax, R. A. & Bennet, J. L. (1991). Neurobiology of parasitic platyhelminths: possible solutions to the problems of correlating structure with function. Parasitology 102 (Suppl.), S31–9.CrossRefGoogle Scholar
Pax, R. A. & Bennet, J. L. (1992). Neurobiology of parasitic flatworms: How much ‘neuro’ in the biology ? Journal of Parasitology 78, 194–205.CrossRefGoogle ScholarPubMed
Price, P. W. (1987). Evolution in Parasite Communities. International Journal for Parasitology 17, 209–14.CrossRefGoogle ScholarPubMed
Rea, J. G. & Irwin, S. W. B. (1994). The ecology of hostfinding behaviour and parasite transmission: past and future perspectives. Parasitology 109 (Suppl.), S31–S39.CrossRefGoogle ScholarPubMed
Rhomberg, L. (1984). Inferring habitat selection by aphids from the dispersion of their galls over the tree. American Naturalist 124, 751–6.CrossRefGoogle Scholar
Roberts, T. M. (1982). From receptor to response: prospects of research in behavioral parasitology. In Cues that Influence Behavior of Internal Parasites (ed. Bailey, W. S.), pp. 166–179. Usda.Google Scholar
Roberts, T. M. & Thorson, R. E. (1977). Chemical attraction between adults of Nippostrongylus brasiliensis: characterization of the substance which attracts females. Journal of Parasitology 63, 849–53.CrossRefGoogle ScholarPubMed
Roche, M. (1966). Influence of male and female Ancyclostoma caninum on each others distribution in the intestine of the dog. Experimental Parasitology 19, 327–31.CrossRefGoogle Scholar
Rohde, K. (1977). A non-competitive mechanism responsible for restricting niches. Zoologischer Anzeiger 199, 164–72.Google Scholar
Rohde, K. (1979). A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114, 648–71.CrossRefGoogle Scholar
Rohde, K. (1994). Niche restriction in parasites: proximate and ultimate causes. Parasitology 109 (Suppl.), S69–S84.CrossRefGoogle ScholarPubMed
Rosenzweig, M. L. (1981). A theory of habitat selection. In Proceedings of the \st International Congress in Ecology, pp. 401–404. Wagenigen, The Netherlands: Centre for Agricultural Publishing and Documentation.Google Scholar
Ross, E. M. & Gilman, A. G. (1985). Pharmacodynamics: Mechanisms of drug action and the relationship between drug concentration and effect. In The Pharmacological Basis of Therapeutics (ed. Gilman, A. G., Goodman, L. S., Tall, T. W., & Furad, F.), pp. 35–48. New York: Macmillan Publishing Company.Google Scholar
Scott, L. D. & Summers, R. W. (1976). Correlation of contraction and transit in rat small intestine. American Journal of Physiology 230, 132–7.CrossRefGoogle ScholarPubMed
Shepherd, G. M. (1988). Neurobiology. Oxford: Oxford University Press.Google Scholar
Smith, G. (1984). Density-dependent mechanisms in the regulation of Fasciola hepatica populations in sheep. Parasitology 88, 449–61.CrossRefGoogle ScholarPubMed
Stephens, D. W. & Krebs, J. R. (1986). Foraging Theory. Princeton: Princeton University Press.Google Scholar
Stretton, A.O. W., Cowden, C., Sithigorngul, P., & Davis, R. E. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102 (Suppl.), S107–16.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. (1990). Habitat selection by helminths: a hypothesis. Parasitology Today 6, 234–7.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. (1991). The relationship between intestinal location and fecundity in Trichinella spiralis. International Journal for Parasitology 21, 855–8.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. (1992 a). Behavior of flatworms in vivo. The role of the brain. Journal of Parasitology 78, 231–42.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. (1992 b). Intestinal contractions and migration behavior in Hymenolepis diminuta. International Journal for Parasitology 22, 813–17.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. (1992 c). Hymenolepis diminuta: The effects of decerebration of Hymenolepis diminuta on thermal responses. Experimental Parasitology 74, 300–6.CrossRefGoogle Scholar
Sukhdeo, M. V. K. & Croll, N. A. (1981). The location of parasites within their hosts: bile and the site selection behavior of Nematospiroides dubius. International Journal for Parasitology 11, 157–62.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K., Keith, S., & Mettrick, D. F. (1988). Effects of bile on the locomotory cycle of Fasciola hepatica. Journal of Parasitology 74, 283–5.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. & Kerr, M. S. (1992). Behavioral adaptation of the tapeworm Hymenolepis diminuta to its environment. Parasitology 104, 331–6.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. & Mettrick, D. F. (1986). The behavior of juvenile Fasciola hepatica. Journal of Parasitology 72, 492–7.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour: Understanding platyhelminth responses. Advances in Parasitology 26, 73–144.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K., O'Grady, R. T., & Hsu, S. C. (1984). The site selected by the larvae of Heligmosomoides polygyrus. Journal of Helminthology 58, 19–23.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. & Sukhdeo, S. C. (1989). Gastrointestinal hormones: Environmental cues for Fasciola hepatica. Parasitology 98, 239–43.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C. & Sukhdeo, M. V. K. (1988). Neurocytology of the cerebral ganglia of Fasciola hepatica (Platyhelminthes). Journal of Comparative Neurology 278, 337–43.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C. & Sukhdeo, M. V. K. (1994 a). FMRFamide related peptides in Hymenolepis diminuta: Immunohistochemistry and radioimmunoassay. Parasitology Research, in press.CrossRefGoogle Scholar
Sukhdeo, S. C. & Sukhdeo, M. V. K. (1994 b). Mesenchyme cells in Fasciola hepatica (Platyhelminthes): primitive glia? Tissue and Cell 26, 123–31.CrossRefGoogle ScholarPubMed
Sukhdeo, S.C., Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Site-finding behavior of Fasciola hepatica (Trematoda), a parasitic flatworm. Behaviour 103, 174–86.CrossRefGoogle Scholar
Sukhdeo, S.C., Sukhdeo, M. V. K. & Mettrick, D. F. (1988). Neurocytology of the cerebral ganglia of Fasciola hepatica (Platyhelminthes). Journal of Comparative Neurology 278, 337–43.CrossRefGoogle ScholarPubMed
Szidat, L. (1969). Structure, development and behaviour of new strigeatoid metacercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada 26, 753–86.CrossRefGoogle Scholar
Tinbergen, N. (1951). The Study of Instinct. New York: Oxford University Press.Google Scholar
Tinbergen, N. & Perdeck, A. C. (1950). On the stimulus situations releasing the begging response in the newly hatched herring gull (Larus argentatus Pont.). Behaviour 3, 1–39.CrossRefGoogle Scholar
Tudge, C. (1988). The Environment of Life. New York. Oxford University Press.Google Scholar
Uetz, G. W. & Hodge, M. A. (1990). Influence of habitat and prey availability on special organization and behavior of colonial web-building spiders. National Geographic Research 6, 22–40.Google Scholar
Uexküll., J. Von. (1934). Streifzge durch die Umwelten von Tieren und Menschen. Berlin: Springer-Berlag. Translated as: A stroll through the worlds of animal and men. In Instinctive Behavior (ed. Schiller, C. H.), pp. 5–80. New York: International Universities Press (1957).Google Scholar
L'Lmer, M. J. (1971). Site finding behaviour in helminths in intermediate and definitive hosts. In Ecology and Physiology of Parasites (ed. Fallis, A. M.), pp. 123–160. Toronto: University of Toronto Press.Google Scholar
Unsworth, W. (1989). Everest. Seattle: Cloudcap.Google Scholar
Wilson, P. A. G. (1994). Doubt and certainty about the pathways of invasive juvenile parasites inside hosts. Parasitology 109 (Suppl.), S57–S67.CrossRefGoogle ScholarPubMed
Wine, J. J. (1984). The structural basis of an innate behavioural pattern. Journal of Experimental Biology 112, 283–319.CrossRefGoogle Scholar
Wright, K. A. (1974). The feeding site and probable feeding mechanism of the parasitic nematode Capillaria hepatica (Bancroft, 1893). Canadian Journal of Zoology 52, 1215–20.CrossRefGoogle ScholarPubMed
Yokogawa, S., Cort, W. W. & Yokogawa, M. (1960). Paragonimus and paragonimiasis. Experimental Parasitology 10, 81–205.CrossRefGoogle Scholar
Young, D. (1989). Nerve Cells and Animal Behaviour. Cambridge: Cambridge University Press.Google Scholar