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Density dependence in establishment, growth and worm fecundity in intestinal helminthiasis: the population biology of Trichuris muris (Nematoda) infection in CBA/Ca mice

Published online by Cambridge University Press:  06 April 2009

E. Michael
Affiliation:
Parasite Epidemiology Research Group, Department of Pure and Applied Biology, Imperial College, University of London, Prince Consort Road, London SW7 2BB
D. A. P. Bundy
Affiliation:
Parasite Epidemiology Research Group, Department of Pure and Applied Biology, Imperial College, University of London, Prince Consort Road, London SW7 2BB

Summary

The results are presented of an experimental study of the population biology of chronic Trichuris muris (Nematoda) infection in cortisone-treated CBA/Ca mice. Attention is focused upon both the validity of the common use of faecal egg counts to demonstrate density dependence in helminth fecundity, and the identification of other possible density-dependent mechanisms that may regulate worm numbers in chronic trichuriasis. The results show that faecal egg counts, although demonstrating high daily variation, are not an artefact of host faecal output but a significant density-dependent function of worm burden. This finding contrasts with the observations on Heligmosomoides polygyrus infection in outbred MF1 mice, but accords with similar studies in a wide variety of host - helminth systems. Worm establishment in the murine host is found to be a density related function of infection dose. This is attributed to the probable existence of a physical gut-carrying capacity in the murine host for T. muris. Worm distribution in the gut is also shown to be density dependent, with worms being displaced from the caecum to the colon at increasing intensities of infection. The sex ratio of the adult parasites, however, is found to be both unitary and independent of worm burden. Evidence for a significant density-dependent decline in female T. muris growth or size is presented. The results also show a significant positive association between female T. muris weight and per capita fecundity. These findings indicate that the stunted growth of individual worms at high parasite densities may be a potential mechanism underlying density dependence in helminth fecundity.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

REFERENCES

Anderson, R. M. (1982). The population dynamics and control of hookworm and roundworm infections. In Population Dynamics of Infectious Diseases, (ed. Anderson, R. M.), pp. 67108. London: Chapman and Hall.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–48.CrossRefGoogle Scholar
Anderson, R. M.&May, R. M. (1982). Population dynamics of human helminth infections: control by chemotherapy. Nature, London 297, 557–63.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985). Helminth infections of humans: mathematical models, population dynamics and control. Advances in Parasitology 24, 1101.CrossRefGoogle ScholarPubMed
Anderson, R. M. & Medley, G. F. (1985). Community control of helminth infections in man by mass and selective chemotherapy. Parasitology 90, 629–60.CrossRefGoogle Scholar
Anderson, R. M. & Schad, G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812–25.CrossRefGoogle ScholarPubMed
Beaver, P. C. (1980). Parasite factors influencing pathogenicity, mortality and morbidity of human intestinal infections. WHO scientific group on intestinal protozoan and helminthic infections. International Journal for Parasitology. SG/WP/80.3.Google Scholar
Boray, J. C. (1969). Experimental fascioliasis in Australia. Advances in Parasitology 7, 95210.CrossRefGoogle ScholarPubMed
Brown, H. W. (1927). A study of the regularity of egg production of Ascaris lumbricoides, Necator americanus and Trichuris trichiura. Journal of Parasitology 14, 110–19.CrossRefGoogle Scholar
Bundy, D. A. P. & Cooper, E. S. (1988). Human Trichuris and trichuriasis. Advances in Parasitology (in the Press).Google ScholarPubMed
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Anderson, R. M. & Didier, J. M. (1987). Age-related prevalence and intensity of Trichuris trichiura infection in a St. Lucian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 8594.CrossRefGoogle Scholar
Bundy, D. A. P., Thompson, D. E., Cooper, E. S., Golden, M. H. N. & Anderson, R. M. (1985). Population dynamics and chemotherapeutic control of Trichuris trichiura infection of children in Jamaica and St. Lucia. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 759–64.CrossRefGoogle ScholarPubMed
Croll, N. A., Anderson, R. M., Gyorkos, T. W. & Ghadirian, E. (1982). The population biology and control of Ascaris lumbricoides in a rural community in Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 187–97.CrossRefGoogle Scholar
Elkins, D. B., Haswell-Elkins, M. & Anderson, R. M. (1986). The epidemiology and control of intestinal helminths in the Pulicat Lake region of Southern India. I. Study design and pre- and post-treatment observations on Ascaris lumbricoides infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 774–92.CrossRefGoogle Scholar
Elliot, J. M. (1977). Statistical Analysis of Samples of Benthic Invertebrates. Publication No. 25. 2nd Edn.Ambleside: Freshwater Biological Association.Google Scholar
Fahmy, M. A. M. (1954). An investigation on the life-cycle of Trichuris muris. Parasitology 44, 50–7.CrossRefGoogle ScholarPubMed
Hall, A. (1981). Quantitative variability of nematode egg counts in faeces: a study among rural Kenyans. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 682–7.Google Scholar
Hall, A. (1982). Intestinal helminths of man: the interpretation of egg counts. Parasitology 85, 605–13.Google Scholar
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–87.CrossRefGoogle ScholarPubMed
Keymer, A. E. & Hiorns, R. W. (1986). Faecal egg counts and nematode fecundity: Heligmosomoides polygyrus and laboratory mice. Parasitology 93, 189203.CrossRefGoogle ScholarPubMed
Keymer, A. E. & Slater, A. F. G. (1987). Helminth fecundity: density dependence or statistical illusion? Parasitology Today 3, 56–8.Google Scholar
Krupp, I. M. (1961). Effects of crowding and of superinfection on habitat selection and egg production in Ancylostoma caninum. Journal of Parasitology 47, 957–61.CrossRefGoogle ScholarPubMed
Lee, T. D. G. & Wakelin, D. (1983). Cortisone-induced immunotolerance to nematode infection in CBA/Ca mice. II. A model for human chronic trichuriasis. Immunology 48, 571–7.Google Scholar
Lloyd, S. & Soulsby, E. J. L. (1987). Immunobiology of gastrointestinal nematodes of ruminants. In Immune Responses in Parasitic Infections: Immunology, Immunopathology, and Immunoprophylaxis. Vol. 1: Nematodes, (ed. Soulsby, E. J. L.), pp. 141. Boca Raton: CRC Press.Google Scholar
Macdonald, G. (1965). The dynamics of helminth infections, with special reference to schistosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 489506.CrossRefGoogle ScholarPubMed
Martin, J., Keymer, A. E., Isherwood, R. J. & Wainwright, S. M. (1983). The prevalance and intensity of Ascaris lumbricoides in Moslem children from Nothern Bangladesh. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 702–6.CrossRefGoogle Scholar
May, R. M. (1977). Togetherness among schistosomes: its effects on the dynamics of the infection. Mathematical Biosciences 35, 301–43.Google Scholar
Medley, G. F. & Anderson, R. M. (1985). Density-dependent fecundity in Schistosoma mansoni infections in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 532–4.CrossRefGoogle ScholarPubMed
Michel, J. F. (1969). The regulation of egg output by Ostertagia Ostertagi in calves infected only once. Parasitology 59, 767–75.CrossRefGoogle Scholar
Moriya, S. (1954). The reliability of the current diagnostic methods for the identification of helminth eggs. Parasitology 44, 300–3.CrossRefGoogle ScholarPubMed
Panesar, T. S. (1981). The early phase of tissue invasion by Trichuris muris (Nematoda: Trichuroidea). Zeitschrift für Parasitenkunde 66, 163–6.CrossRefGoogle ScholarPubMed
Panesar, T. S. & Croll, N. A. (1980). The location of parasites within their hosts: site selection by Trichuris muris in the laboratory mouse. International Journal for Parasitology 10, 261–73.CrossRefGoogle ScholarPubMed
Scott, J. A. (1946). Simplified quantitative methods for hookworm control programs. American Journal of Tropical Medicine 26, 331–7.Google ScholarPubMed
Scott, J. A. & Headlee, W. H. (1938). Studies in Eygpt on the correction of helminth egg count data for the size and consistency of stools. American Journal of Hygiene 27, 176–95.Google Scholar
Sinniah, B. (1982). Daily egg production of Ascaris lumbricoides: the distribution of eggs in the faeces and the variability of egg counts. Parasitology 84, 167–75.CrossRefGoogle ScholarPubMed
Smith, G., Grenfell, B. T. & Anderson, R. M. (1987). The regulation of Ostertagia ostergagi populations in calves: density-dependent control of fecundity. Parasitology 95, 373–88.Google Scholar
Wakelin, D. (1967). Acquired immunity to Trichuris muris in the albino laboratory mouse. Parasitology 57, 515–24.Google Scholar
Wakelin, D. (1975). Genetic control of immune responses to parasites: selection for responsiveness and non-responsiveness to Trichuris muris in random-bred mice. Parasitology 71, 377–84.CrossRefGoogle ScholarPubMed
Wakelin, D. & Wilson, M. M. (1980). Immunity to Trichinella spiralis in irradiated mice. International Journal for Parasitology 10, 3741.Google Scholar