Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-19T17:09:57.370Z Has data issue: false hasContentIssue false

Density-dependent mechanisms in the regulation of intestinal helminth populations

Published online by Cambridge University Press:  06 April 2009

Anne Keymer
Affiliation:
Molteno Institute, Department of Parasitology, University of Cambridge, Downing Street, Cambridge CB2 3EE

Extract

The regulation of helminth populations tends to occur primarily as a result of limitations imposed on the build up of parasite subpopulations within individual hosts (Anderson & May, 1979; May & Anderson, 1979). Considering the relevance of these factors to the success or otherwise of intestinal helminth control programmes, it is perhaps surprising that more information is not yet available concerning the particular mechanisms which may be responsible, and in particular, the population consequences of the immune responses which such parasites may precipitate. Density-dependence in a single rate parameter, if operative over the naturally observed numerical range, is sufficient to regulate parasite population flow throughout the life-cycle, whether direct or indirect (Anderson, 1976). For the genera given in Table 1, this could be provided by the observed pattern of parasite mortality and/or fecundity. It is of interest to note, however, that circumstantial evidence cited in the Table suggests that each of the 6 genera is also potentially able to induce host mortality under certain conditions. Whether this acts in a density-dependent manner in natural infections is almost entirely unknown. Rapid reproduction may be of great selective advantage to intestinal helminths, even if it is necessarily accompanied by pathogenicity (see Anderson, 1981). If the manner in which this pathogenicity acts in any way enhances the stability of the host-parasite interaction, then perhaps it may have contributed to the selection pressures which have led so many genera to continue to break the rules of the ‘well-adapted’ parasite (see, for example, Noble & Noble, 1971).

Type
Trends and Perspectives
Copyright
Copyright © Cambridge University Press 1982

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

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). 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., (1976). Dynamic aspects of parasite population ecology. In Ecological Aspects of Parasitology, (ed. Kennedy, C. R.), North-Holland Publishing Company, Amsterdam.Google Scholar
Anderson, R. M., (1978). The regulation of host population growth by parasitic species. Parasitology 76, 119–57.CrossRefGoogle ScholarPubMed
Anderson, R. M., (1979). The influence of parasitic infection on the dynamics of host population growth. In Population Dynamics, (ed. Anderson, R. M., Turner, B. D. and Taylor, L. R.), Blackwell Scientific Publications, Oxford.Google Scholar
Anderson, R. M., (1980). The dynamics and control of direct life-cycle helminth parasites. Lecture Notes in Biomathematics 39, 278322.CrossRefGoogle Scholar
Anderson, R. M., (1981). Population ecology of infectious disease agents. In Theoretical Ecology: Principles and Applications (2nd Edition), (ed. May, R. M.), Blackwell Scientific Publications, Oxford.Google Scholar
Anderson, R. M., & May, R. M., (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–47.Google Scholar
Anderson, R. M., & May, R. M., (1979). Population biology of infectious diseases: Part I. Nature 280, 361–7.CrossRefGoogle ScholarPubMed
Anderson, R. M., & Michel, J. F., (1977). Density-dependent survival in populations of Ostertagia ostertagi. International Journal for Parasitology 7, 321–9.CrossRefGoogle ScholarPubMed
Arme, C., & Owen, R. W., (1967). Infections of the three-spined stickleback, Gasterosteus aculeatus L., with special reference to pathological effects. Parasitology 57, 301–14.Google Scholar
Beaver, P. C., (1980). Parasite factors influencing pathogenicity, mortality and morbidity of human intestinal infections. WHO scientific group on intestinal protozoan and helminthic infections. Int. Par. SG/WP/80. 3.Google Scholar
Bradley, D. J., (1974). Stability in host-parasite systems. In Ecological Stability, (ed.Usher, M. B. and Williamson, M. H.), Chapman and Hall, London.Google Scholar
Camp, J. W., & Huizinga, H. W., (1980). Seasonal population interactions of Acanthocephalus dirus (Van Cleave, 1931) in the creek chub, Semotilus atromaculatus, and isopod, Asellus intermedius. Journal of Parasitology 66, 299304.CrossRefGoogle Scholar
Chandler, A. C., (1939). The effects of number and age of worms on development of primary and secondary infections with Hymenolepis diminuta in rats and an investigation into the true nature of ‘premunition’ in tapeworm infections. American Journal of Hygiene 29, 105–14.Google Scholar
Chappell, L. H., & Pike, A. W., (1976). Loss of Hymenolepis diminuta from the rat. International Journal for Parasitology 6, 333–9.Google Scholar
Crofton, H. D., (1971 a). A quantitative approach to parasitism. Parasitology 62, 179–94.Google Scholar
Crofton, H. D., (1971 b). A model of host-parasite relationships. Parasitology 63, 343–64.Google Scholar
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 (in the Press).CrossRefGoogle Scholar
Crompton, D. W. T., (1964). Studies on Acanthocephala, with special reference to Polymorphus minutus. Ph.D. dissertation, University of Cambridge.Google Scholar
Crompton, D. W. T., (1975). Relationships between acanthocephala and their hosts. Symposia of the Society for Experimental Biology XXIX, 467504.Google Scholar
Crompton, D. W. T., Arnold, S., & Barnard, D., (1972). The patent period and production of eggs of Moniliformis dubius (Acanthocephala) in the small intestine of male rats. International Journal for Parasitology 2, 319–26.CrossRefGoogle ScholarPubMed
Crompton, D. W. T., & Hall, A., (1981). Parasitic infection and host nutrition. Report of Workshop 2 at the 3rd European Multicolloquium of Parasitology. Parasitology 82, 3148.Google Scholar
Crompton, D. W. T., Keymer, A. E., Singhvi, A., & Nesheim, M. C., (1982). Rat-dietary fructose concentration and the intestinal distribution and growth of Moniliformis (Acanthocephala). (in the Press).Google Scholar
Crook, J. R., & Grundmann, A. W., (1964). The life history and larval development of Moniliformis clarki (Ward, 1917). Journal of Parasitology 50, 689–93.Google Scholar
Dobson, C., (1972). Immune responses to gastrointestinal helminths. In Immunity to Animal Parasites, (ed. Soulsby, E. J. L.), Academic Press, London.Google Scholar
Donald, A. D., Dineen, J. K., Turner, J. H., & Wagland, B. M., (1964). The dynamics of the host-parasite relationship. I. Nematodirus spathiger infection in sheep. Parasitology 54, 527–44.Google Scholar
Gandhi, B. P., (1965). Intestinal obstruction due to roundworms. East African Medical Journal 37, 124.Google Scholar
Gemmell, M. A., (1976). Immunology and regulation of the cestode zoonoses. In Immunology of Parasitic Infections, (ed. Cohen, S. and Sadun, E. H.), Blackwell, Oxford.Google Scholar
Gemmell, M. A., (1978). Perspective on options for Hydatidosis and Cysticercosis control. Veterinary Medical Review 1, 348.Google Scholar
Gemmell, M. A., & Johnstone, P. D., (1977). Experimental epidemiology of Hydatidosis and Cysticercosis. Advances in Parasitology 15, 312–69.Google ScholarPubMed
Gemmell, M. A., & MacNamara, F. N., (1972). Immune response to tissue parasites. II. Cestodes. In Immunity to Animal Parasites, (ed. Soulsby, E. J. L.), Academic Press, London.Google Scholar
Ghazal, A. M., & Avery, R. A., (1974). Population dynamics of Hymenolepis nana in mice: fecundity and the ‘crowding effect’. Parasitology 69, 403–15.Google Scholar
Hall, A., Latham, M. C, Crompton, D. W. T., & Stephenson, L. S., (1981). Taenia saginata (Cestoda) in Western Kenya: the reliability of faecal examinations in diagnosis. Parasitology 83, 91101.Google Scholar
Halvorsen, O., & Andersen, K., (1974). Some effects of population density in infections of Diphyllobothrium dendriticum (Xitztsch) in golden hamster (Mesocricetusauratus Weiterhouse) and common gull (Larus canus L.). Parasitology 69, 149–60.Google Scholar
Hassell, M. P., Lawton, J. H., & Beddinoton, J. R., (1977). Sigmoid functional responses by invertebrate predators and parasitoids. Journal of Animal Ecology 46, 249–62.Google Scholar
Hassell, M. P., & May, R. M., (1973). Stability in insect host-parasite models. Journal of Animal Ecology 42, 693726.Google Scholar
Hayashi, S., (1980). A model for the evaluation and assessment of the effect of control of the soil transmitted helminthiasis. In The Proceedings of the Seminar on Parasite Control in the Prevention of Malnutrition. W.H.O., UNICEF, JOICFP, JAPC. Tokyo.Google Scholar
Hesselberg, C. A., & Andreassen, J., (1975). Some influences of population density on Hymenolepis diminuta in rats. Parasitology 71, 517–23.CrossRefGoogle ScholarPubMed
Hill, R. B., (1926). The estimation of the number of hookworm harboured by the use of the dilution egg count method. American Journal of Hygiene 6 (Suppl.): 1941.Google Scholar
Hine, P. M., & Kennedy, C. R., (1974). The population biology of the acanthocephalan Pomphorhynchus laevis (Muller) in the River Avon. Journal of Fish Biology 6, 665–79.Google Scholar
Holling, C. S., (1959 a). The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Canadian Entomologist 91, 293320.Google Scholar
Holling, C. S., (1959 b). Some characteristics of simple types of predation and parasitism. Canadian Entomologist 91, 385–98.CrossRefGoogle Scholar
Holmes, J. C., (1959). Interaction between dietary carbohydrate quality and quantity in nutrition of Hymenolepis diminuta. Journal of Parasitology (Suppl.) 45, 31.Google Scholar
Hopkins, C. R., (1980). Immunity and Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta, (ed. Arai, H. P.) Academic Press, London.Google 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.Google Scholar
Jarrett, E. E. E., Jarrett, W. F. H., & Urquahart, G. M., (1968). Quantitative studies on the kinetics of establishment and expulsion of intestinal nematode populations in susceptible and immune hosts. Nippostrongylus brasiliensis in the rat. Parasitology 58, 625–39.Google 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, 8893.CrossRefGoogle Scholar
Jorgensen, R. J., Nansen, P., Nielsen, K., Eriksen, L., & Andersen, S., (1975). Experimental Ascaris suum infection in the pig. Population kinetics following low and high levels of primary infection in piglets. Veterinary Parasitology 1, 151–7.Google Scholar
Kennedy, C. R., (1970). The population biology of helminths of British freshwater fish. In Aspects of Fish Parasitology, vol. 8. Symp. Brit. Soc. Parasitol., (ed. Taylor, A. E. R. and Muller, R.). Blackwell, Oxford.Google Scholar
Kennedy, C. R., (1974). The importance of parasite mortality in regulating the population size of the acanthocephalan Pomphorhynchus laevis in goldfish. Parasitology 68, 93101.CrossRefGoogle ScholarPubMed
Kennedy, C. R., (1976). Reproduction and dispersal. In Ecological Aspects of Parasitology, (ed. Kennedy, C. R.), North Holland Publishing Company, Amsterdam.Google Scholar
Kennedy, C. R., (1977). The regulation offish parasite populations. In Regulation of Parasite Populations, (ed. Esch, G. W.), Academic Press, New York.Google Scholar
Kennedy, C. R., & Rumpus, , (1977). Long-term changes in the size of the Pomphorynchus laevis (Acanthocephala) population in the River Avon. Journal of Fish Biology 10, 3542.Google Scholar
Keymer, A. E., (1980). The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81, 405–21.CrossRefGoogle ScholarPubMed
Keymer, A. E., (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 51, 941–50.Google Scholar
Keymer, A. E., (1982). The dynamics of tapeworm infections. In The Dynamics of Infectious Diseases, (ed. Anderson, R. M.), Chapman and Hall, London (in the Press).Google Scholar
Keymer, A. E., & Anderson, R. M., (1979). The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: the influence of infective-stage density and spatial distribution. Parasitology 79, 195207.CrossRefGoogle ScholarPubMed
Keymer, A. E., Crompton, D. W. T., & Walters, D. E., (1982). Nippostrongylus brasiliensis (Nematoda) in protein-malnourished rats. Host mortality, morbidity and rehabilitation, (in the Press).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.Google Scholar
Lackie, J. M., (1972). The course of infection and growth of Moniliformis dubius (Acanthocephala) in the intermediate host, Periplaneta americana. Parasitology 64, 95106.Google Scholar
Leikina, E. S., Poletaeva, O. G., & Martsinovsky, E. I., (1980). Immunology of Ascariasis. WHO Scientific group on intestinal protozoan and helminthic infections. Int. Par. SG/WP/80. 15.Google Scholar
Li, S. Y., & Hsu, H. F., (1951). On the frequency distribution of helminths in their naturally infected hosts. Journal of Parasitology 37, 3241.CrossRefGoogle ScholarPubMed
Love, R. J., (1975). Nippostrongylus brasiliensis infections in mice; the immunological basis of worm expulsion. Parasitology 70, 1118.CrossRefGoogle ScholarPubMed
May, R. M., (1975). Stability and Complexity in Model Ecosystems, (2nd ed.). Princeton University Press.Google Scholar
May, R. M., (1977). Dynamical aspects of host-parasite associations: Crofton's model revisited. Parasitology 75, 259–76.Google Scholar
May, R. M., & Anderson, R. M., (1978). Regulation and stability of host-parasite population interactions. II. Destabilizing processes. Journal of Animal Ecology 47, 249–67.Google Scholar
May, R. M., & Anderson, R. M., (1979). Population biology of infectious diseases: Part II. Nature 280, 455–61.Google Scholar
Mello, D. A., (1974). A note on egg production of Ascaris lumbricoides. Journal of Parasitology 60, 380–1.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
Michel, J. F., (1974). Arrested development of nematodes and some related phenomena. Advances in Parasitology 12, 279366.CrossRefGoogle ScholarPubMed
Miller, G. C., (1981). Helminths and the transmammary route of infection. Parasitology 82, 335–42.Google Scholar
Miller, T. A., (1979). Hookworm infection in man. Advances in Parasitology 17, 315–84.CrossRefGoogle ScholarPubMed
Moss, G. E., (1971). The nature of the immune response of the mouse to the bile duct cestode Hymenolepis microstoma. Parasitology 62, 285–94.CrossRefGoogle Scholar
Muller, R., (1975). Worms and Disease: A Manual of Medical Helminthology. William Heinemann Ltd., London.Google Scholar
Murdoch, W. W., & Oaten, A., (1975). Predation and population stability. Advances in Ecological Research 9, 2131.Google Scholar
Nickol, B. B., (1977). Introductory remarks. In Regulation of Parasite Populations, (ed. Esch, G. W.), Academic Press, London.Google Scholar
Noble, E. R., & Noble, G. A., (1971). Parasitology, 3rd ed., Lea and Febiger, Philadelphia.Google Scholar
Ogilvie, B. M., & Jones, V. E., (1971). Nippostrongylus brasiliensis: a review of immunity and the host-parasite relationship in the rat. Experimental Parasitology 29, 138–77.Google Scholar
Pawlowski, Z. S., (1980). Ascariasis: host-pathogen biology. WHO Scientific group on helminthic infections. Int. Par. SG/WP/80. 16.Google Scholar
Pawlowski, Z. S., & Schultz, M. G., (1972). Taeniasis and cysticercosis (Taenia saginata). Advances in Parasitology 10, 269347.CrossRefGoogle ScholarPubMed
Pennycuick, L., (1971). Frequency distributions of parasites in a population of three-spined sticklebacks, Gasterosteus aculeatus, with particular reference to the negative binomial distribution. Parasitology 63, 389406.Google Scholar
Phillipson, R. S., (1969). Reproduction of Nippostrongylus brasiliensis in the rat intestine. Parasitology 59, 961–71.Google Scholar
Rau, M. E., (1979). The frequency distribution of Hymenolepis diminuta cysticercoids in natural, sympatric populations of Tenebrio molitor and T. obscurus. International Journal for Parasitology 9, 85–7.CrossRefGoogle Scholar
Rau, M. E., & Tanner, C. E., (1972). Echinococcus multilocularis in the cotton rat. Asexual proliferation following the intraperitoneal inoculation of graded doses of protoscolices. Canadian Journal of Zoology 50, 941–6.Google Scholar
Read, C. P., (1951). The ‘crowding effect’ in tapeworm infections. Journal of Parasitology 37, 174–8.CrossRefGoogle ScholarPubMed
Read, C. P., (1959). The role of carbohydrates in the biology of cestodes. VIII. Some conclusions and hypotheses. Experimental Parasitology 8, 365–82.CrossRefGoogle ScholarPubMed
Read, C. P., & Phifer, K., (1959). The role of carbohydrates in the biology of cestodes. I. The effect of dietary carbohydrate quality on the size of Hymenolepis diminuta. Experimental Parasitology 6, 17.CrossRefGoogle Scholar
Rees, G., (1967). Pathogensis of adult cestodes. Helminthological Abstracts 36, 123.Google Scholar
Roberts, L. S., (1961). The influence of population density on patterns and physiology of growth in Hymenolepis diminuta (Cestoda: Cyclophyllidea) in the definitive host. Experimental Parasitology 11, 332–71.Google Scholar
Roberts, L. S., & Mono, F. N., (1968). Developmental physiology of cestodes. III. Development of Hymenolepis diminuta in superinfections. Journal of Parasitology 54, 5562.Google Scholar
Rogers, D. J., (1972). Random search and insect population models. Journal of Animal Ecology 41, 369–83.Google Scholar
Russell, S. W., Baker, N. F., & Raizes, G. S., (1966). Experimental Obeliscoides cunicul infections in rabbits: comparison with Trichostrongylus and Ostertagia infections in cattle and sheep. Experimental Parasitology 19, 163–73.Google Scholar
Sarles, M. P., (1929). The effect of age and size of infestation on the egg production of the dog hookworm, Ancylostoma caninum. American Journal of Hygiene 10, 658–66.Google Scholar
Schad, G. A., (1977). The role of arrested development in the regulation of nematode populations. In Regulation of Parasite Populations, (ed. Esch, G. W.), Academic Press, London.Google Scholar
Schad, G. A., Soulsby, E. J. L., Chowdhury, A. B., & Gilles, H. M., (1975). Epidemiological and serological studies of hookworm infection in India and West Africa. In Nuclear Techniques in Helminthology Research. International Atomic Energy Agency, Vienna.Google Scholar
Seidenberg, A. J., (1973). Ecology of the acanthocephalan, Acanthocephalus dirus (Van Cleave, 1931), in its intermediate host, Asellus intermedius Forbes (Crustacea: Isopoda). Journal of Parasitology 59, 957–62.Google Scholar
Stephenson, L. S., (1980 a). The contribution of Ascaris lumbricoides to malnutrition in children. Parasitology 81, 221–33.Google Scholar
Stephenson, L. S., (1980 b). Nutritional and economic implications of soil-transmitted helminths with special reference to Ascariasis. In Clinical Disorders in Pediatric Gastroenterology and Nutrition (ed. by Lifshitz, F.), Marcel Dekker, Inc: New York.Google Scholar
Stoll, N. R., (1929). Studies with the Strongyloid nematode, Haemonchus contortus. I. Acquired resistance of hosts under natural reinfection conditions out-of-doors. American Journal of Hygiene 10, 384418.Google Scholar
Sweatman, G. K., Williams, R. J., Moriarty, K. M., & Henshall, T. C., (1963). On acquired immunity to Echinococcus granulosus in sheep. Research in Veterinary Science 4, 187–98.Google Scholar
Uznanski, R. L., & Nickol, B. B., (1980). Parasite population regulation: lethal and sublethal effects of Leptorhynchoides thecatus (Acanthocephala: Rhadinorhynchidae) on Hyalella azteca (Amphipoda). Journal of Parasitology 66, 121–6.CrossRefGoogle Scholar
Van Dobben, W. H., (1952). The food of the cormorants in the Netherlands. Ardea 40, 163.Google Scholar
Walkey, M., (1967). The ecology of Neoechinorhynchus rutili (Muller). Journal of Parasitology 53, 795804.Google Scholar
Wamba, J. R., (1974). Intestinal obstruction in Kenya. East African Journal of Medical Research, 1, 265–72.Google Scholar
Who Chronicle, (1968). Volume 22, pages 155–59.Google Scholar
Winfield, G. F., (1932). Quantitative studies on the rat nematode Heterakis spurnosa (Schneider, 1866). American Journal of Hygiene 17, 168228.Google Scholar