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The regulation of host population growth by parasitic species

Published online by Cambridge University Press:  06 April 2009

R. M. Anderson
R. M. Anderson
Affiliation:
Department of Zoology, King's College, London University, London WC2R 2LS
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Summary

The nature of parasitism at the population level is defined in terms of the parasite's influence on the natural intrinsic growth rate of its host population. It is suggested that the influence on this rate is related to the average parasite burden/host and hence to the statistical distribution of parasites within the host population.

Theoretical models of host–parasite associations are used to assess the regulatory influence of parasitic species on host population growth. Model predictions suggest that three specific groups of population processes are of particular importance: over-dispersion of parasite numbers/host, density dependence in parasite mortality or reproduction and parasite-induced host mortality that increases faster than linearly with the parasite burden. Other population mechanisms are shown to have a destabilizing influence, namely: parasite-induced reduction in host reproductive potential, direct parasite reproduction within the host and time delays in the development of transmission stages of the parasite.

These regulatory and destabilizing processes are shown to be commonly observed features of natural host-parasite associations. It is argued that interactions in the real world are characterized by a degree of tension between these regulatory and destabilizing forces and that population rate parameter values in parasite life-cycles are very far from being a haphazard selection of all numerically possible values. It is suggested that evolutionary pressures in observed associations will tend to counteract a strong destabilizing force by an equally strong regulatory influence. Empirical evidence is shown to support this suggestion in, for example, associations between larval digeneans and molluscan hosts (parasite-induced reduction in host reproductive potential counteracted by tight density-dependent constraints on parasite population growth), and interactions between protozoan parasites and mammalian hosts (direct parasite reproduction counteracted by a well-developed immunological response by the host).

The type of laboratory and field data required to improve our understanding of the dynamical properties of host–parasite population associations is discussed and it is suggested that quantitative measurement of rates of parasite-induced host mortality, degrees of over-dispersion, transmission rates and reproductive and mortality rates of both host and parasite would provide an important first step. The value of laboratory work in this area is demonstrated by reference to studies which highlight the regulatory influence of parasitic species on host population growth.

Type
Research Article
Information
Parasitology , Volume 76 , Issue 2 , April 1978 , pp. 119 - 157
Copyright
Copyright © Cambridge University Press 1978

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References

Ackert, J. E., Graham, G. L., Nolf, L. O. & Porter, D. A. (1931). Quantitative studies on the administration of variable numbers of nematode eggs (Ascaridia lineata) to chickens. Transactions of the American Microscopical Society 50, 206–14.CrossRefGoogle Scholar
Anderson, R. M. (1974 a). Population dynamics of the cestode Caryophyllaeus laticeps (Pallas, 1781) in the bream (Abramis brama L.). Journal of Animal Ecology 43, 305–21.CrossRefGoogle Scholar
Anderson, R. M. (1974 b). An analysis of the influence of host morphometric features on the population dynamics of Diplozoon paradoxum (Nordmann, 1832). Journal of Animal Ecology 43, 873–81.CrossRefGoogle Scholar
Anderson, R. M. (1976 a). Some simple models of the population dynamics of eucaryotic parasites. In Mathematical Models in Medicine, Lecture Notes in Biomathematics, vol. 11 (ed. Berger, J., Buhler, W., Repges, R. and Tautu, P.), pp. 16–57. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Anderson, R. M. (1976 b). Dynamic aspects of parasite population ecology. In Ecological Aspects of Parasitology (ed. Kennedy, C. R.). Amsterdam: North-Holland Publishing Com-pany.Google Scholar
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host–parasite population interactions: I. Regulatory processes. Journal of Animal Ecology (in the Press).CrossRefGoogle Scholar
Anderson, R. M. & Michel, J. F. (1978). Density dependent survival in populations of Ostertagia ostertagi. International Journal for Parasitology 7, 321–9.CrossRefGoogle Scholar
Anderson, R. M. & Whitfield, P. J. (1975). Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transvesotrema patialense (Soparker, 1924). Parasitology 70, 295–310.CrossRefGoogle Scholar
Anderson, R. M., Whitfield, P. J. & Mills, C. A. (1977). An experimental study of the population dynamics of an ectoparasite digenean Transversotrema patialense (Soparker): the cercarial and adult stages. Journal of Animal Ecology 46, 555–80.CrossRefGoogle Scholar
Anderson, R. M., Whitfield, P. J., Dobson, A. P. & Keymer, Anne E. (1978). Concomitant predation and infection: an experimental study. Journal of Animal Ecology (in the Press).CrossRefGoogle Scholar
Askew, R. R. (1971). Parasitic Insects. London: Heinemann.Google Scholar
Bailey, N. T. J. (1964). The Elements of Stochastic Processes. London: John Wiley.Google Scholar
Baker, J. R. (1969). Parasitic Protozoa. London: Hutchinson.Google Scholar
Beddington, J. R., Free, C. A. & Lawton, J. H. (1976). Concepts of stability and resilience in predator–prey models. Journal of Animal Ecology 45, 791–816.CrossRefGoogle Scholar
Berrie, A. D. (1970). Snail problems in African schistosomiasis. Advances in Parasitology 8, 43–98.CrossRefGoogle ScholarPubMed
Boray, J. C. (1969). Experimental fascioliasis in Australia. Advances in Parasitology 7, 95–210.CrossRefGoogle ScholarPubMed
Boxshall, G. A. (1974). The population dynamics of Lepeophtheirus pectoralis (Muller): dispersion pattern. Parasitology 69, 373–90.CrossRefGoogle ScholarPubMed
Bruce-Chwatt, L. J. & Bruce-Chwatt, J. M. (1974). Malaria in Mauritius as dead as the Dodo. Bulletin of the New York Academy of Medicine 50, 1069–80.Google ScholarPubMed
Buxton, P. A. (1940). Studies on populations of head-lice (Pediculus humanu8 capitis Anoplura). III. Material from South India. Parasitology 32, 296–302.CrossRefGoogle Scholar
Chu, K. Y., Sabbaghian, H. & Massoud, J. (1966). Host–parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. 2. Effect of exposure dosage of miracidia on the breeding of the snail host and the development of the parasite. Bulletin of the World Health Organization 34, 121–30.Google Scholar
Cole, L. C. (1949). The measurement of interspecific association. Ecology 30, 411–24.CrossRefGoogle Scholar
Crofton, H. D. (1971 a). A quantitative approach to parasitism. Parasitology 62, 179–94.CrossRefGoogle Scholar
Crofton, H. D. (1971 b). A model of host–parasite relationships. Parasitology 63, 343–64.CrossRefGoogle Scholar
Dogiel, V. A. (1964). General Parasitology. Edinburgh: Oliver and Boyd.Google Scholar
Dogiel, V. A. (1965). General Protozoology. London: Oxford University Press.Google Scholar
Forrester, D. J. (1971). Heligmosomoides polygyrus (=Nematospiroides dubius) from wild rodents of Northern California: natural infections, host specificity, and strain characteristics. Journal of Parasitology 57, 498–503.CrossRefGoogle ScholarPubMed
Foster, R. (1958). The effects of the trematode metacercariae (Brachylaemidae) on the slug Milax Sowerbii Férussac and Agriolimax reticulatus Muller. Parasitology 48, 261–8.CrossRefGoogle ScholarPubMed
Frankland, H. M. T. (1954). The life history and binomics of Diclidophora denticulata (Trematoda: Monogenea). Parasitology 45, 313–51.CrossRefGoogle Scholar
Ghazal, A. M. & Avery, R. A. (1974). Population dynamics of Hymenolepis nana in mice: fecundity and the crowding effect. Parasitology 69, 403–15.CrossRefGoogle ScholarPubMed
Hassell, M. P., Lawton, J. H. & Beddington, J. R. (1976). The components of arthropod predation: I. The prey death rate. Journal of Animal Ecology 45, 135–64.CrossRefGoogle Scholar
Hassell, M. P., Lawton, J. H. & May, R. M. (1976). Patterns of dynamical behaviour in single-species populations. Journal of Animal Ecology 45, 471–86.CrossRefGoogle Scholar
Hayes, T. J., Bailer, J. & Mitrovic, M. (1973). The pattern of mortality in mice experimentally infected with Fasciola hepatica. International Journal for Parasitology 3, 665–9.CrossRefGoogle ScholarPubMed
Hesselberg, C. A. & Andreassen, G. (1975). Some influences of population density on Hymenolepis diminuta in rats. Parasitology 71, 517–23.CrossRefGoogle ScholarPubMed
Hodasi, J. K. (1972). The effects of Fasciola hepatica on Lymnaea truncatula. Parasitology 64, 359–69.CrossRefGoogle Scholar
Hunter, G. C. & Leigh, L. C. (1961). Studies on the resistance of rats to the nematode Nippostrongylus muris (Yokogawa, 1920). Parasitology 51, 347–51.CrossRefGoogle Scholar
Jones, A. W. & Tan, B. D. (1971). Effect of crowding upon growth and fecundity in the mouse bile duct tapeworm Hymenolepis microstoma. Journal of Parasitology 57, 88–93.CrossRefGoogle Scholar
Krebs, C. J. (1972). Ecology: The Experimental Analy8is of Distribution and Abundance. New York: Harper and Row.Google Scholar
Lancinani, C. A. (1975). Parasite induced alterations in host reproduction and survival. Ecology 56, 689–95.CrossRefGoogle Scholar
Lim, H. K. & Lie, K. J. (1969). The redial population of Paryphostomum segregatum (Trematoda: Echinostomatidae) in the snail Biomphalaria glabrata. Zeitschrift f¨r Parasitenkunde 32, 112–19.Google ScholarPubMed
MacDonald, G. (1961). Epidemiologic models in studies of vector-borne diseases. Public Health Reports, Washington D.C. 76, 753–64.CrossRefGoogle Scholar
Massoud, J. (1974). The effect of variation in miracidial exposure dose on laboratory infections of Ornithobilharzia turkestanicum in Lymnaea gedrosiana. Journal of Helminthology 48, 139–44.CrossRefGoogle ScholarPubMed
May, R. M. (1975). Stability and Complexity in Model Ecosystems, 2nd edition. Princeton: Princeton University Press.Google Scholar
May, R. M. (1976). Models for single species populations. In Theoretical Ecology (ed. May, R. M.), pp. 4–25. Oxford: Blackwell Scientific Publications.Google Scholar
May, R. M. (1977). Dynamical aspects of host–parasite associations: Crofton's Model revisited. Parasitology 75, 259–76.CrossRefGoogle Scholar
May, R. M. & Anderson, R. M. (1978). Regulation and stability of host–parasite population interactions: II. Destabilising processes. Journal of Animal Ecology (in the Press).Google Scholar
May, R. M., Conway, G. R., Hassell, M. P. & Southwood, T. R. E., (1974). Time delays, density dependence and single species oscillations. Journal of Animal Ecology 43, 747–70.CrossRefGoogle Scholar
McClelland, G. & Bourns, T. K. R. (1968). Effects of Trichobilharzia ocellata on growth, reproduction and survival of lymnaea stagnalis. Experimental Parasitology 24, 137–46.CrossRefGoogle Scholar
Michel., J. F. (1969). The regulation of egg output by Ostertagia Ostertagi in calves infected only once. Parasitology 59, 767–75.CrossRefGoogle Scholar
MurdocH, W. W. & Oaten, A. (1975). Predation and population stability. Advances in Ecological Research 9, 1–131.CrossRefGoogle Scholar
Noble, E. R. & Noble, G. A. (1971). Parasitology: The Biology of Animal Parasites, 3rd edition. Philadephia: Lea and Febiger.Google Scholar
Northam, J. I. & Rocha, U. F. (1958). On the statistical analysis of worm counts in chickens. Experimental Parasitology 7, 428–38.CrossRefGoogle Scholar
Pan, C. (1965). Studies on the host–parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. Annals of Tropical Medicine and Hygiene 14, 931–75.CrossRefGoogle ScholarPubMed
Park, T. (1948). Experimental studies of interspecies competition. I. Competition between populations of the flour beetles, Tribolium confusum Duval and Tribolium casteneum Herbst. Ecological Monographs 18, 265–308.CrossRefGoogle Scholar
Pennycuick, L. (1971). Frequency distributions of parasites in a population of three spined sticklebacks, Gasterosteus aculeatus L., with particular reference to the negative binomial distribution. Parasitology 63, 389–406.CrossRefGoogle Scholar
Randolph, S. E. (1975). Patterns of distribution of the tick Ixodes trianguliceps Birula on its hosts. Journal of Animal Ecology 44, 451–74.CrossRefGoogle Scholar
Rose, J. H. (1956). The bionomics of the free living larvae of Dictyocaulus viviparus. Journal of Comparative Pathology and Therapeutics 66, 228–40.CrossRefGoogle ScholarPubMed
Schmid, W. D. & Robinson, E. J. (1972). The pattern of a host-parasite distribution. Journal of Parasitology 57, 907–10.CrossRefGoogle Scholar
Smyth, J. D. (1976). Introduction to Animal Parasitology, 2nd edition. London: Hodder and Stoughton.Google Scholar
Southwood, T. R. E. (1976). Bionomic strategies and population parameters. In Theoretical Ecology (ed. May, R. M.), pp. 26–48. Oxford: Blackwell Scientific Publications.Google Scholar
Southwood, T. R. E. (1977). Habitat, the templet for ecological strategies? Journal of Animal Ecology 46, 337–66.CrossRefGoogle Scholar
Starr, M. P. (1975). A generalised scheme for classifying organismic associations. In Symbiosis (ed. Jennings, D. H. and Lee, D. L.), pp. 1–20. London: Cambridge University Press.Google Scholar
Stromberg, P. C. & Crites, J. L. (1974). Survival, activity and penetration of the first stage larvae of Cammallanus oxycephalus Ward and Magath, 1916. International Journal for Parasitology 4, 417–21.CrossRefGoogle ScholarPubMed
Sturrock, B. M. (1966). The influence of infection with Schistosoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 60, 187–97.CrossRefGoogle ScholarPubMed
Targett, G. A. T. & Viens, P. (1975). Ablastin: control of Trypanosoma musculi infections in mice. Experimental Parasitology 38, 309–16.CrossRefGoogle ScholarPubMed
Viens, P., Targett, G. A. T., Leuchars, E. & Davies, A. J. S. (1974). The immunological response of CBA mice to Trypanosoma musculi. I. Initial control of the infection and the effect of T-cell deprivation. Clinical and Experimental Immunology 16, 279–94.Google ScholarPubMed
Watkins, C. V. & Harvey, L. A. (1942). On the parasites of silver foxes on some farms in the South West. Parasitology 34, 155–79.CrossRefGoogle Scholar
Weatherly, N. (1971). Effects on litter size and litter survival in Swiss mice infected with Trichinella spiralis during gestation. Journal of Parasitology 57, 298–301.CrossRefGoogle ScholarPubMed
Whittaker, R. H. (1975). Communities and Ecosystems, 2nd edition. New York: Macmillan.Google Scholar
Williams, C. B. (1944). Some applications of the logarithmic series and the index of diversity to ecological problems. Journal of Ecology 32, 1–44.CrossRefGoogle Scholar
Williams, I. C. (1963). The infestations of the redfish Sebastes marinus (L.) and S. mentella Travin (Scleroparei: Scorpaenidea) by the copepods, Peniculus clavatus (Müller), Sphyrion lumpi (Krøyer) and Chondracanthopsis nodosus (Müller) in the eastern North Atlantic. Parasitology 53, 501–25.CrossRefGoogle Scholar
Winfield, G. F. (1932). Quantitative studies on the rat nematode Heterakis spumosa (Schneider, 1866). American Journal of Hygiene 17, 168–228.Google Scholar
Wright, C. A. (1971). Flukes and Snails. London: Allen and Unwin.Google Scholar