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The population dynamics of competition between parasites

Published online by Cambridge University Press:  06 April 2009

A. P. Dobson
Affiliation:
Department of Pure and Applied Biology, Imperial College, Prince Consort Road, London SW7 2BB

Extract

A number of published studies of competition between parasite species are examined and compared. It is suggested that two general levels of interaction are discernible: these correspond to the two levels of competition recognized by workers studying free-living animals and plants: ‘exploitation’ and ‘interference’ competition. The former may be defined as the joint utilization of a host species by two or more parasite species, while the latter occurs when antagonistic mechanisms are utilized by one species either to reduce the survival or fecundity of a second species or to displace it from a preferred site of attachment. Data illustrating both levels of interaction are collated from a survey of the published literature and these suggest that interference competition invariably operates asymmetrically. The data are also used to estimate a number of population parameters which are important in determining the impact of competition at the population level. Theoretical models of host-parasite associations for both classes of competition are used to examine the expected patterns of population dynamics that will be exhibited by simple two-species communities of parasites that utilize the same host population. The analysis suggests that the most important factor allowing competing species of parasites to coexist is the statistical distribution of the parasites within the host population. A joint stable equilibrium should be possible if both species are aggregated in their distribution. The size of the parasite burdens at equilibrium is then determined by other life-history parameters such as pathogenicity, rates of resource utilization and antagonistic ability. Comparison of these theoretical expectations with a variety of sets of empirical data forms the basis for a discussion about the importance of competition in natural parasite populations. The models are used to assess quantitatively the potential for using competing parasite species as biological control agents for pathogens of economic or medical importance. The most important criterion for identifying a successful control agent is an ability to infect a high proportion of the host population. If such a parasite species also exhibits an intermediate level of pathology or an efficient ability to utilize shared common resources, antagonistic interactions between the parasite species contribute only secondarily to the success of the control. Competition in parasites is compared with competition in free-living animals and plants. The comparison suggests further experimental tests which may help to assess the importance of competition in determining the structure of more complex parasite-host communities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1985

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References

REFERENCES

Aarssen, L. W. (1983). Ecological combining abilities and competitive combining ability in plants: Towards a general evolutionary theory of coexistence in systems of competition. American Naturalist 122, 707–31.CrossRefGoogle Scholar
Anderson, R. M. (1978). The regulation of host population growth by parasitic species. Parasitology 76, 119–57.CrossRefGoogle ScholarPubMed
Anderson, R. M. (1979). Parasite pathogenicity and the depression of host population equilibria. Nature, London 279, 150–2.CrossRefGoogle Scholar
Anderson, R. M. & Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–98.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host-parasite interactions. I Regulatory processes. Journal of Aminal Ecology 47, 219–47.Google Scholar
Anderson, R. M. & May, R. M. (1979). Population biology of infectious diseases: Part I. Nature, London 280, 361–7.CrossRefGoogle ScholarPubMed
Antonovics, J. & Levin, D. A. (1980). The ecological and genetic consequences of density-dependent regulation in plants. Annual Reviews of Ecology and Systematics 11, 411–52.CrossRefGoogle Scholar
Arme, C. (1982). Nutrition. In Modern parasitology, (ed. Cox, F. E. G.). Oxford: Blackwell Scientific Publications.Google Scholar
Atkinson, W. D. & Shorrocks, B. (1981). Competition on a divided and ephemeral resource: a Simulation model. Journal of Animal Ecology 50, 461–71.CrossRefGoogle Scholar
Basch, P. F. (1970). Relationships of some larval strigeids and echinostomes (Trematoda): hyper-parasitism, antagonism and ‘immunity’ in the snail host. Experimental parasitology 27, 193216.CrossRefGoogle Scholar
Boddington, M. J. & Mettrick, D. F. (1981). Production and reproduction in Hymenolepis diminuta (Platyhelminthes: Cestoda). Canadian journal of zoology 59, 1962–72.CrossRefGoogle Scholar
Brassard, P., Rau, M. E. & Curtis, M. A. (1982). Parasite-induced susceptibility to predation in diplostomiasis. Parasitology 85, 495501.CrossRefGoogle Scholar
Bremmernan, H. J. (1980). Sex and polymorphism as strategies in host‐pathogen interactions. Journal of Theoretical Biology 87, 671702.CrossRefGoogle Scholar
Bristol, J. R., Pinon, A. J. & Mayberry, L. F. (1983). Interspecific interactions between Nippo‐ strongylus brasiliensis and Eimeria nieschulzi in the rat. Journal of Parasitology 69, 372–4.CrossRefGoogle Scholar
Broek, W. L. F. van den (1979 a). Infection of estuarine fish populations by Cryptocotyle lingua (Creplin). Journal of fish biology 14, 395402.CrossRefGoogle Scholar
Broek, W. L. F. (1979 b). Copepod ectoparasites of Merlangius merlangus and Platichthys flesus. Journal of Fish Biology 14, 371–80.CrossRefGoogle Scholar
Brooks, D. R. (1980 a). Allopatric speciation and non-interactive parasite community structure. Systematic Zoology 29, 192203.CrossRefGoogle Scholar
Brooks, D. R. (1980 b). Brooks' response to Holmes and Price. Systematic Zoology 29, 214–15.CrossRefGoogle Scholar
Bruna, C. D. & Xenia, B. (1976). Nippostrongylus brasiliensis in mice: reduction of worm burden and prolonged infection induced by the presence of Nematospiroides dubius. Journal of parasitology 62, 490–1.CrossRefGoogle ScholarPubMed
Burrough, R. J. (1978). The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata, in roach and rudd. Journal of Fish Biology 13, 1932.CrossRefGoogle Scholar
Cannon, L. R. G. (1972). Studies on the ecology of the papillose allocreadid trematodes of the yellow perch in Algonquin Park, Ontario. Canadian Journal of Zoology 50, 1231–9.CrossRefGoogle ScholarPubMed
Chappell, L. H. (1969). Competitive exclusion between two intestinal parasites of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Parasitology 55, 775–8.CrossRefGoogle Scholar
Combes, C. (1982). Trematodes: antagonism between species and sterilizing effects on snails in biological control. Parasitology 84, 151–75.CrossRefGoogle Scholar
Connell, J. H. (1983). On the prevalence and relative importance of interspecific competition: evidence from field experiments. American naturalist 122, 661–96.CrossRefGoogle Scholar
Cox, F. E. G. (1979). Concomitant infections. In Rodent Malaria (ed. Killick-kendrick, R. and Peters, W.). 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, 2783.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. (1985). Nutrition and parasitic infection. Federation proceedings (in the press).Google Scholar
Cross, S. X. (1934). A probable case of non-specific immunity between two parasites of ciscoes of the Trout Lake Region of Northern Wisconsin. Journal of Parasitology 20, 244–5.CrossRefGoogle Scholar
Crowden, A. E. & Broom, D. M. (1980). Effects of the eyefluke, Diplostomum spathaceum, on the behavior of dace (Leuciscus leuciscus.) Animal Behavior 28, 287–94.CrossRefGoogle Scholar
Dash, K. M. (1981). Interaction between Oesphagostomum columbianum and Oesophagostomum venu-losum in sheep. International Journal for Parasitology 11, 210–17.CrossRefGoogle Scholar
Evans, N. A. (1977). The site preferences of two digeneans, Asymphylodora kubanicum and Sphaero‐stoma bramae, in the intestine of the roach. Journal of Helminthology 51, 197204.CrossRefGoogle ScholarPubMed
Frankland, H. M. T. (1959). The incidence and distribution in Britain of the trematodes of the mole Talpa europaea. Parasitology 49, 132–42.CrossRefGoogle Scholar
Gause, G. E. (1934). The Struggle For Existence. Baltimore: Williams & wilkins.CrossRefGoogle ScholarPubMed
Gordon, D. M. & Whitfield, P. J. (1984). Interactions of the cystercercoids of Hymenolepis diminuta and Raillietina cesticillus in their intermediate host, Tribolium confusum. Parasitology 90, 421–31.CrossRefGoogle Scholar
Grey, A. J. & Hayunga, E. G. (1980). Evidence for alternative site selection by Glaridacris laruei (Cestoidea: Caryophyllidea) as a result of interspecific competition. Journal of parasitology 66, 371–2.CrossRefGoogle Scholar
Halvorsen, O. (1976). Negative interaction amongst parasites. In Ecological Aspects of Parasitology (ed. Kennedy, C. R.). Amsterdam: North-Holland.Google Scholar
Halvorsen, O. & Macdosald, S. (1972). Studies of the helminth fauna of norway. XXVI. The distribution of Cyathocephalus truncatus (pallas) in the intestine of brown trout (Salmo irutta). Norwegian Journal of Zoology 20, 265–72.Google Scholar
Harper, J. L. (1982). After description. In The plant Community as a working mechanism (ed. Newman, E. I.), pp. 1125. Oxford: British Ecological Society. Blackwell Scientific.Google Scholar
Henricson, J. (1977). The abundance and distribution of Diphyllobothrium dendriticum (Nitzseh) and D. ditremum (Creplin) in the char Salvelinus alpinus (L.) In Sweden. Journal of Fish Biology 11, 231–48.CrossRefGoogle Scholar
Hobbs, R. P. (1980). Interspecific interactions among gastrointestinal helminths in Pikas of North America. American Midland Naturalist 103, 1525.CrossRefGoogle Scholar
Holland, C. (1984). Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88, 303–16.CrossRefGoogle ScholarPubMed
Holliman, R. B. (1971). Ecological observations on two species of spirorchid trematodes. American Midland Naturalist 86, 509–12.CrossRefGoogle Scholar
Holmes, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). 1. General effects and comparison with crowding. Journal Of Parasitology 47, 209–16.CrossRefGoogle Scholar
Holmes, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site aggregation, and their importance to the development of helminth communities. Canadian journal of Zoology 51, 337–47.CrossRefGoogle Scholar
Holmes, J. C. & Price, P. W. (1980). Parasite communities: the roles of phylogeny and ecology. Systematic Zoology 29, 203–13.CrossRefGoogle Scholar
Hominick, W. M. & Davey, K. G. (1972 a). The influence of the host stage and sex upon the size and Composition of the population of two species of thelastomatids parasitic in the hindgut of Periplaneta americana. Canadian Journal of Zoology 50, 947–54.CrossRefGoogle Scholar
Hominick, W. M. & Davey, k. G. (1972 b). Reduced nutrition as the factor controlling the population Of pinworms following endocrine gland removal in Periplaneta americana L. Canadian Journal of Zoology 50, 1421–32.CrossRefGoogle Scholar
Ives, A. R. & May, R. M. (1985). Competition within and between species in a patchy environment: relations between microscopic and macroscopic models. Journal of Theoretical Biology (in the press.)CrossRefGoogle Scholar
Jenkins, S. N. & Behnke, J. M. (1977). Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 71–8.CrossRefGoogle ScholarPubMed
Keeling, J. E. D. (1961). Experimental Trichuriasis. I. Antagonism between Trichuris muris and Aspicularis tetraptera in the albino mouse. Journal of parasitology 47, 641–6.CrossRefGoogle Scholar
Kennedy, C. R. (1981). Long term studies on the population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata (Digena: Diplostomatidae), concurrently infecting the eyes of perch, Perca fluviatilis. Journal of Fish Biology 19, 221–36.CrossRefGoogle Scholar
Kennedy, C. R. & Burroughs, R. J. (1977). The population biology of two species of eyefluke Diplostomum gasterostei and Tylodelphys clavata, in perch. Journal of Fish Biology 11, 619–33.CrossRefGoogle Scholar
Kennedy, M. W. (1980). Immunologically mediated non-specific interactions between intestinal Phases of Trichinella spiralis and Nippostrongylus brasiliensis in the mouse. Parasitology 80, 6172.CrossRefGoogle ScholarPubMed
Keymer, A. (1982 a). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–87.CrossRefGoogle ScholarPubMed
Keymer, A. (1982 b). Helminth population biology and host nutrition. Proceedings of the 5th International Congress of Parasitology, vol. 2, pp. 3235.Google Scholar
Keymer, A., Crompton, D. W. T. & Walters, D. E. (1983). Parasite population biology and host nutrition: dietary fructose and Moniliformis (Acanthocephala). Parasitology 87, 265–78.CrossRefGoogle ScholarPubMed
Kisielewska, K. (1970 a). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb). (Rodentia). IV. Spatial structure of a helminth grouping within the host population. Acta Parasitological Polonica 18, 177–96.Google Scholar
Kisielewska, K. (1970 b). Ecological organization of intestinal groupings in Clethrionomys glareolus (Schreb) (Rodentia). V. Some questions concerning helminth groupings in the host individuals. Acta Parasitologica Polonica 18, 197208.Google Scholar
Lang, B. Z. (1967). Fasciola hepatica and Hymenolepis microstoma in the laboratory mouse. Journal Of parasitology 53, 213‐14.CrossRefGoogle ScholarPubMed
Laurie, J. S. (1957). The in vitro fermentation of carbohydrate by two species of cestodes and one species of acanthocephala. Experimental parasitology 6, 245–60.CrossRefGoogle ScholarPubMed
Lawton, J. H. & Hassell, M. P. (1981). Asymmetrical competition in insects. Nature, london 289, 793–5.CrossRefGoogle Scholar
Levin, B. R. (1982). Evolution of parasites and hosts. Group report. In Population Biology of Infectious Diseases (ed. Anderson, R. M. and May, R. M.), pp. 213243. Berlin: Springer Verlag.CrossRefGoogle Scholar
Lie, K. J., Basch, P. F., Heyneman, D., Beck, A. J. & Audy, J. R. (1968). Implications for trematode control of interspecific larval antagonism within snail hosts. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 299319.CrossRefGoogle ScholarPubMed
Lim, H. K. & Heyneman, D. (1972). Intramolluscan inter-trematode antagonism: a review of factors influencing the host-parasite system and its possible role in biological control. Advances in Parasitology 10, 191268.CrossRefGoogle ScholarPubMed
Loach, C. D. (1962). Increased resistance to Trichinella spiralis in the laboratory rat following infections with Nippostrongylus muris. Journal of Parasitology 48, 24–6.CrossRefGoogle Scholar
Lotka, A. J. (1932). The growth of mixed populations; two species competing for a common food supply. Journal of the Washington Academy of Science 22, 461–9.Google Scholar
May, R. M. (1975). Stability and Complexity in Model Ecosystems, 2nd ed.Princeton: Princeton University Press.Google Scholar
May, R. M. & Anderson, R. M.(1978). Regulation and stability of host parasite population interactions. Two destabilizing processes. Journal of Animal Ecology 47, 249–67.CrossRefGoogle Scholar
May, R. M. & Anderson, R. M. (1979). Population biology of infectious diseases. II. Nature, London 280, 455–61.CrossRefGoogle Scholar
May, R. M. & Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society London B 219, 281313.Google ScholarPubMed
May, R. M. & Hassell, M. P. (1981). The dynamics of multiparasitoid-host interactions. American Naturalist 117, 234–61.CrossRefGoogle Scholar
McDonald, M. E. (1969). Catalogue of Helminths of Waterfowl (Anatidae). Bureau of Sport Fish and Wildlife, Special Scientific Report- Wildlife 126, 692 p.Google Scholar
Mead-Briggs, A. R. & Vaughn, J. R. (1973). The incidence of Anoplocephaline cestodes in a Population of rabbits in Surrey, England. Parasitology 67, 351–64.CrossRefGoogle Scholar
Miller, R. S. (1967). Pattern and process in competition. Advances in Ecological Research 4, 174.CrossRefGoogle Scholar
Moqbel, R. & Wakelin, D. (1979). Trichinella spiralis and Strongyloides ratti. Immune interaction in adult rats. Experimental Parasitology 47, 6572.CrossRefGoogle ScholarPubMed
Paperna, I. (1964). Competitive exclusion of Dactylogyvus extensus by Dactylogyvus vastator (Trema-Toda, Monogenea) on the gills of reared carp. Journal of Parasitology 50, 94–8.CrossRefGoogle Scholar
Pojmanska, T. (1982). The co-occurrence of three species of Diorchis Clere, 1903 (Cestoda: Hymeno-lepididae) in the European coot, Fulica atra L. Parasitology 84, 419–29.CrossRefGoogle Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton: Princeton University Press.Google ScholarPubMed
Read, C. P. (1951). The ‘crowding effect’ in tapeworm infections. Journal of Parasitology 37, 174–8.CrossRefGoogle ScholarPubMed
Read, C. P. (1956). Carbohydrate metabolism of Hymenolepis diminuta. Experimental Parasitology 5, 325–44.CrossRefGoogle ScholarPubMed
Read, C. P. & Phifer, K. (1959). The role of carbohydrates in the biology of cestodes. VII. Interactions between individual tape worms of the same and different species. Experimental Parasitology 8, 4650.CrossRefGoogle Scholar
Riley, J. & Owen, W. R. (1975). Competition between two closely related Tetrabothrius cestodes of the Fulmar (Fulmarus glacialis L.) Zeitschrift für Parasitenkunde 46, 221–8.CrossRefGoogle ScholarPubMed
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. (1982). Ecology of Marine Parasites. University of Queensland Press.Google Scholar
Roughgarden, J. (1979). Theory of Population Genetics and Evolutionary Ecology: An Introduction. New York: Macmillan.Google Scholar
Roughgarden, J. (1983). The theory of coevolution. In Coevolution (ed. Futuyma, D. J. and Slatkin, M.), pp. 3364. Sunderland, Ma: Sinauer.Google Scholar
Schad, G. A. (1963). Niche diversification in a parasite species flock. Nature, London 198, 404–6.CrossRefGoogle Scholar
Schad, G. A. (1966). Immunity, competition, and natural regulation of helminth populations. American Naturalist 100, 359–64.CrossRefGoogle Scholar
Schad, G. A. (1982). Resources, competition and the niches of helminth parasites. Proceedings of the 5th International Congress of Parasitology, vol. 2, pp. 4043.Google Scholar
Schoener, T. W. (1983). Field experiments on interspecific competition. American Naturalist 122, 240–85.CrossRefGoogle Scholar
Shorrocks, B., Rosewell, J., Edwards, K. & Atkinson, W. (1984). Interspecific competition is not a major organizing force in many insect communities. Nature, London 310, 310–12.CrossRefGoogle Scholar
Silver, B. B., Dick, T. A. & Welch, H. E. (1980). Concurrent infections of Hymendepis diminuta and Trichinella spiralis in the rat intestine. Journal of Parasitology 66, 786–91.CrossRefGoogle ScholarPubMed
Stahl, W. (1966). Experimental Aspiculuraisis II. Effects of concurrent helminth infection. Experimental Parasitology 18, 116–23.CrossRefGoogle ScholarPubMed
Tilman, D. (1982). Resource Competition and Community Structure. Princeton University Press.Google ScholarPubMed
Thomas, J. D. (1963). Studies on the growth of brown trout (Salmo trutta L.) from four contrasting habitats. Proceedings of the Zoological Society of London 142, 459509.CrossRefGoogle Scholar
Thomas, J. D. (1964). Studies on populations of helminth parasites in Brown Trout (Salmo trutta, L.) Journal of Animal Ecology 33, 8395.CrossRefGoogle Scholar
Turner, J. H., Kates, K. C. & Wilson, G. I. (1962). The interaction of concurrent infections of the abomasal nematodes, Haemonchus contortus, Ostertagia circumvata, and Trichostrongylus axei (Trichostrongylidae), in lambs. Proceedings of the Helminthological Society of Washington 29, 210–16.Google Scholar
Uglem, G. L. & Beck, S. M. (1972). Habitat specificity and correlated aminopeptidase activity in the acanthocephalans Neoechinorhynchus cristatus and N. Crassus. Journal of Parasitology 58, 911–20.CrossRefGoogle Scholar
Wakelin, D. (1978). Genetic control of susceptibility and resistance to parasitic infection. Advances in Parasitology 16, 219308.CrossRefGoogle ScholarPubMed
Wilson, C. B. (1916). Copepod parasites of fresh-water fishes and their economic relation to mussel glochidia. Bulletin of the U.S. Bureau of Fisheries 34, (1914) 131374.Google Scholar