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Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review

Published online by Cambridge University Press:  06 April 2009

D. J. Shaw  and
A. P. Dobson
D. J. Shaw
Affiliation:
Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK
A. P. Dobson
Affiliation:
Department of Ecology and Evolutionary Biology, Eno Hall, Princeton University, Princeton, New Jersey, USA
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Summary

In this paper we review the published literature on patterns of abundance and aggregation of macroparasites in wildlife host populations. We base this survey on quantitative analyses of mean burden and a number of measures of the degree of aggregation of parasite burdens between hosts. All major parasite and vertebrate host taxa were represented in the database. Mean parasite burden was found to be log-normally distributed, indicating that all parasite burdens are regulated to some degree. In addition, all but one of the parasitic infections were aggregated with respect to their hosts, and the relationship between log mean parasite burden and log variance was found to be very strong (R2 = 0·87). That is, for a given mean parasite burden there are constraints on the degree of variation in individual host burdens. The aggregated nature of the parasitic infections is also apparent from other measures of the degree of aggregation: prevalence – mean relationships, and the negative binomial parameter, k. Using a relatively new technique for parasitological infection data – tree-based models, as well as traditional linear models – a number of the parasitic infections was found to be associated with systematically lower or higher parasite burdens. Possible biological explanations for these and other patterns are proposed.

Keywords

macroparasitesaggregationnegative binomialdistributionworm burdenpopulation dynamics

Information

Type
Research Article
Information
Parasitology , Volume 111 , Supplement S1: Ecology of wildlife host-parasite interactions , January 1995 , pp. S111 - S133
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Allison, F. R. (1979). Life cycle of Curtuteria australis m. sp. (Digenea: Echinostomatidae: Himasthlinae), intestinal parasite of the South Island pied oystercatcher. New Zealand Journal of Zoology 6, 13–20.CrossRefGoogle Scholar
Amin, O. M. (1975). Host and seasonal associations of Acanthocephalus parksidei Amin 1974, (Acanthocephala: Echinorhynchidae) in Wisconsin fishes. Journal of Parasitology 61, 318–29.CrossRefGoogle ScholarPubMed
Amin, O. M. (1981). The seasonal distribution of Echinorhynchus salmonis (Acanthocephala: Echinorhynchidae) among rainbow smelt, Osmerus mordax Mitchell, in Lake Michigan. Journal of Fish Biology 19, 467–74.CrossRefGoogle Scholar
Anderson, R. M. (1976). Seasonal variation in the population dynamics of Caryophyllaeus laticeps. Parasitology 72, 281–305.CrossRefGoogle ScholarPubMed
Anderson, R. M. (1978). The regulation of host population growth by parasitic species. Parasitology 76, 119–57.CrossRefGoogle ScholarPubMed
Anderson, R. M. (1980). The dynamics and control of direct life cycle helminth parasites. Lecture Notes in Biomathematics 39, 278–322.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., Gordon, D. M., Crawley, M. J. & Hassell, M. P. (1982). Variability in the abundance of animal and plant-species. Nature 296, 245–8.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, 219–47.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1979 a). Population biology of infectious diseases: Part I. Nature 280, 361–7.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1979 b). Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology 79, 63–94.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985 a). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1–101.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985 b). Herd immunity to helminth infection and implications for parasite control. Nature 315, 493–6.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans: dynamics and Control. Oxford: Oxford University Press.CrossRefGoogle Scholar
Anderson, R. M., Whitfield, P. J. & Dobson, A. P. (1978). Experimental studies of infection dynamics: infection of the definitive host by the cercariae of Transverostrema patialense. Parasitology 77, 189–200.CrossRefGoogle ScholarPubMed
Andrews, C. (1979). Host specificity of the parasite fauna of perch Perca fluviatilis L. from the British Isles, with special reference to a study at Llyn Tegid (Wales). Journal of Fish Biology 15, 195–209.CrossRefGoogle Scholar
Awachie, J. B. E. (1966). Observations on Cyathocephalus truncatus Pallas, 1781 (Cestoda: Spathebothriidea) in its intermediate and definitive hosts in a trout stream, North Wales. Journal of Helminthology 40, 1–10.CrossRefGoogle Scholar
Bailey, N. T. J. (1959). Statistical Methods in Biology. Cambridge: Cambridge University Press.Google Scholar
Bartlett, M. S. (1956). Deterministic and stochastic models for recurrent epidemics. In Proceedings of the Third Berkeley Symposium on Mathematical Statistics and Probability, vol. 4, pp. 81–109. California: University of California Press.Google Scholar
Behnke, J. M. (1975). Aspiculuris tetraptera in wild Mus musculus. The prevalence of infection in male and female mice. Journal of Helminthology 49, 85–90.CrossRefGoogle ScholarPubMed
Bliss, C. I. & Fisher, R. A. (1953). Fitting the negative binomial distribution to biological data. Biometrics 9, 176–99.CrossRefGoogle Scholar
Booth, M. & Bundy, D. A. P. (1992). Comparative prevalences of Ascaris lumbricoides, Trichuris trichiura and hookworm infections and the prospects for combined control. Parasitology 105, 151–7.CrossRefGoogle ScholarPubMed
Bowers, E. A. & James, B. L. (1967). Studies on the morphology, ecology and life-cycle of Meiogymnophallus minutus (Cobbold, 11859) comb. nov. (Trematoda: Gymnophallidae). Paraistology 57, 281–300.CrossRefGoogle Scholar
Boxshall, G. A. (1974). The population dynamics of Lepeophtheirus pectoralis (Muller): dispersion pattern. Parasitology 69, 373–90.CrossRefGoogle ScholarPubMed
Brattey, J. (1988). Life history and population biology of adult Acanthocephalus lucii (Acanthocephala: echinorhynchidae). Journal of Parasitology 74, 72–80.CrossRefGoogle ScholarPubMed
Breiman, L., Friedman, J. H., Olshen, R. & Stone, C. J. (1984). Classification and Regression Trees. Belmont, California: Wadsworth International Group.Google Scholar
Breyev, K. A. (1973 a). On the nature of relation between the incidence of infection in host population and the men density of parasite. Folia Parasitologica (Praha) 20, 227–34.Google Scholar
Breyev, K. A. (1973 b). Some general principles of the control of parasitic arthropods as exemplified by the control of warble flies. Entomological Review 52, 142–51.Google Scholar
Breyev, K. A. & Minar, J. (1976). On the regularities of distribution of Hypoderma bovis De Geer larvae parasitising cattle herds in different parts of the range of this warble fly. Folia Parasitological (Praha) 23, 343–56.Google Scholar
Brown, N. S. (1971). A survey of the arthropod parasites of pigeons (Columba livia) in Boston. Journal of Parasitology 57, 1379–80.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. & Medley, G. F. (1992). Epidemiology and population dynamics of helminth infection. In Allergy and Immunity to Helminths: Common Mechanisms or Divergent Pathways? (ed. Hoqbel, R.), pp. 17–37. London: Taylor & Francis.Google Scholar
Bundy, D. A. P., Thompson, D. E., Golden, M. H., Cooper, E. S., Anderson, R. M. & Harland, P. S. (1985). Population distribution of Trichuris trichiura in a community of Jamaican children. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 232–7.CrossRefGoogle Scholar
Burreson, E. M. & Olson, R. E. (1974). Seasonal variation in the populations of two hemiurid trematodes from the Pacific Staghorn Sculpin, Leptocottus armatus Girard, in an Oregon estuary. Journal of Parasitology 60, 764–7.CrossRefGoogle Scholar
Butynski, T. M. (1982). Ecology of Physaloptera capensis (Nematoda: Spiruroidea) infecting the Springhare Pedetes capensis (Mammalia) in Botswana. Journal of Zoology, London 196, 233–54.CrossRefGoogle Scholar
Buxton, P. A. (1938). Studies on populations of head-lice (Pediculus humanus capitis: Anoplura). II. Parasitology 30, 851–10.CrossRefGoogle Scholar
Bye, K. (1987). Abomasal nematodes from three Norwegian wild reindeer populations. Canadian Journal of Zoology 65, 677–80.CrossRefGoogle Scholar
Bye, K., Halvorsen, O. & Nilssen, K. J. (1987). Immigration and regional distribution of abomasal nematodes of Svalbard reindeer. Journal of Biogeography 14, 451–8.CrossRefGoogle Scholar
Cassie, R. M. (1962). Frequency distributions models in the ecology of plankton and other organisms. Journal of Animal Ecology 31, 65–92.CrossRefGoogle Scholar
Chubb, J. C. (1963). Seasonal occurrence and maturation of Triaenophorus nodulosus (Pallas, 1781) (Cestoda: Pseuodphyllidea) in Pike Esox lucius L. of Llyn Tegid. Parasitology 55, 419–33.CrossRefGoogle Scholar
Chubb, J. C. (1964). Observations on the occurrence of the plerocercoids of Triaenophorus nodulosus (Pallas, 1781) (Cestoda: Pseudophyllidea) in the perch Perca fluviatilis L. of Llyn Tegid (Bala Lake), Merionethshire. Parasitology 54, 481–91.CrossRefGoogle ScholarPubMed
Ciampi, A., Chang, C.-H., Hogg, S. & McKinney, S. (1987). Recursive Partitioning: a versatile method for exploratory data analysis in Biostatistics. In Biostatistics (ed. Macneil, I. B. & Umphrey, G. J.). New York: D. Reidel Publishing.Google Scholar
Clark, L. A. & Pregibon, D. (1992). Tree-based models. In Statistical Models in S (ed. Chambers, J. M. & Hastie, T. J.), pp. 377–420, Wadsworth & Brooks/Cole Advanced Books & Software, California.Google Scholar
Cook, E. F. & Beer, J. R. (1955). The louse populations of some cricetid rodents. Parasitology 45, 409–19.CrossRefGoogle ScholarPubMed
Crofton, H. D. (1958). Nematode parasite populations in sheep on lowland farms. VI. Sheep behaviour and nematode infections. Parasitology 48, 251–60.CrossRefGoogle ScholarPubMed
Crofton, H. D. (1971 a). A quantitative approach to parasitism. Parasitology 62, 179–93.CrossRefGoogle Scholar
Crofton, H. D. (1971 b). A model of host-parasite relationships. Parasitology 63, 343–64.CrossRefGoogle Scholar
Crompton, D. W. T., Keymer, A. E. & Arnold, S. E. (1984). Investigating over-dispersion; Moniliformis (Acanthocephala) and rats. Parasitology 88, 317–31.CrossRefGoogle ScholarPubMed
Dawes, B. (1959). On Cercaria owreae (Hutton, 1954) from Sagitta hexaptera (d, Orbigny) in the Caribbean plankton. Journal of Helminthology 33, 209–22.CrossRefGoogle ScholarPubMed
Denny, M (1969). Life-cycles of helminth parasites using Grammarus lacustris as an intermediate host in a Canadian lake. Parasitology 59, 795–827.CrossRefGoogle Scholar
Dietz, K. (1982). Overall population patterns in the transmission cycle of infectious agents. In Population Biology of Infectious Diseases (ed. Anderson, R. M. & May, R. M.), pp. 87–102. Berlin: Springer.CrossRefGoogle Scholar
Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317–47.CrossRefGoogle ScholarPubMed
Dobson, A. P. & Merenlender, A. (1991). Coevolution of macroparasites and their hosts. In Parasitism: Coexistence or Conflict? (ed. Toft, C. A. & Sihilmann, A. E.), pp. 83–101. Oxford: Oxford University Press.Google Scholar
Dronen, N. O. Jr (1978). Host-parasite population dynamics of Haematoloechus coloradensis Cort, 1915 (Digenea: Plagiorchiidae). American Midland Naturalist 99, 330–49.CrossRefGoogle Scholar
Durrett, R. & Levin, S. A. (1994). Stochastic spatial models: a user's guide to ecological applications. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 343, 329–50.CrossRefGoogle Scholar
Ekbaum, E. (1938). Notes on the occurrence of Acanthocephala in pacific fishes. I. Echinorhynchus gadi (Zoega) Müller in salmon and E. lageniformis Sp. Nov. and Corynosoma strumosum (Rudolphi) in two species of flounder. Parasitology 30, 267–73.CrossRefGoogle Scholar
Elliot, J. M. (1977). Statistical Analysis of Samples of Benthic Invertebrates, 2nd edn.Ambleside, UK: Freshwater Biological Association.Google Scholar
Ellis, C. & Williams, I. C. (1973). The longevity of some species of helminth parasites in naturally acquired infections of the lesser black-backed gull, Larus fuscus L. in Britain. Journal of Helminthology 47, 329–38.CrossRefGoogle ScholarPubMed
Evans, N. A. (1977). The occurrence of Sphaerostoma bramae (Digenea: Allocreadiidae) in the roach from the Worcester–Birmingham canal. Journal of Helminthology, 51, 189–96.CrossRefGoogle ScholarPubMed
Evans, N. A. (1978). The occurrence and life history of Asymphyldora kubanicum (Platyhelminthes: Digenea: Monorchidae) in the Worcester-Birmingham canal, with special reference to the feeding habits of the definitive host, Rutilus rutilus. Journal of Zoology, London 184, 143–53.CrossRefGoogle Scholar
Evans, N. A. (1983). The population biology of Hymenolepis tenerrima (Linstow, 1882) Fuhrmann 1906 (Cestoda, Hymenolepididae) in its intermediate host Herpetocypris reptans (Ostracoda). Zeitschrift für Parasitenkunde 69, 105–11.CrossRefGoogle ScholarPubMed
Evans, N. A., Whitfield, P. J., Bamber, R. N. & Espin, P. (1983). Lernaeocera lusci (Copepoda: Pennellidae) on bib (Trisopterus luscus) from Southampton Water. Paraistology 86, 161–73.CrossRefGoogle Scholar
Evans, N. A., Whitfield, P. J. & Dobson, A. P. (1981). Parasite utilization of a host community: the distribution and occurrence of metacercarial cysts of Echinoparyphium recurvatum (Digenea: Echinostomatidae) in seven species of mollusc at Harting Pond, Sussex. Parasitology 83, 1–12.CrossRefGoogle Scholar
Fisher, W. D. (1958). On grouping for maximum homogeneity. Journal of the American Statistical Association 53, 789–98.CrossRefGoogle Scholar
Folstad, I., Nilssen, A. C., Halvorsen, O. & Andersen, J. (1989). Why do male reindeer (Rangifer t. tarandus) have higher abundance of second and third instar larvae of Hypoderma tarandi than females? Oikos 55, 87–92.CrossRefGoogle Scholar
Folstad, I., Nilssen, A. C., Halvorsen, O. & Andersen, J. (1991). Parasite avoidance: the cause of post-calving migrations in Rangifer? Canadian Journal of Zoology 69, 2423–9.CrossRefGoogle Scholar
Grafen, A. & Woolhouse, M. E. J. (1993). Does the negative binomial distribution add up? Parasitology Today 9, 475–7.CrossRefGoogle ScholarPubMed
Gregory, R. D. & Woolhouse, M. E. J. (1993). Quantification of parasite aggregation: a simulation study. Acta Tropica 54, 131–9.CrossRefGoogle ScholarPubMed
Grenfell, B. T. (1988). Gastrointestinal nematode parasites and the stability and productivity of intensive ruminant grazing systems. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 321, 541–63.Google ScholarPubMed
Grenfell, B. T. (1992). Parasitism and the dynamics of ungulate grazing systems. American Naturalist 139, 907–29.CrossRefGoogle Scholar
Grenfell, B. T., Das, P. K., Rajagopalan, P. K. & Bundy, D. A. P. (1990). Frequency distribution of lymphatic filariasis microfilariae in human populations: population processes and statistical estimation. Parasitology 101, 417–27.CrossRefGoogle ScholarPubMed
Grenfell, B. T. & Dobson, A. P. (1995). Ecology of Infectious Diseases in Natural Populations. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Grenfell, B. T., Smith, G. & Anderson, R. M. (1986). Maximum-likelihood estimates of the mortality and migration rates of the infective larvae of Ostertagia ostertagi and Cooperia oncophora. Parasitology 92 643–52.CrossRefGoogle ScholarPubMed
Grenfell, B. T., Smith, G. & Anderson, R. M. (1987). The regulation of Ostertagia ostertagi populations in calves: the effect of past and current experience of infection on proportional establishment and parasite survival. Parasitology 95, 363–72.CrossRefGoogle ScholarPubMed
Grundmann, A. W., Warnock, R. G. & Wassom, D. L. (1976). Some mechanisms of natural regulation of parasitic helminth populations. American Midland Naturalist 95, 347–60.CrossRefGoogle Scholar
Guyatt, H. L. & Bundy, D. A. P. (1991). Estimating prevalence of community morbidity due to intestinal helminths: prevalence of infection as an indicator of the prevalence of disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 778–82.CrossRefGoogle ScholarPubMed
Guyatt, H. L., Bundy, D. A. P., Medley, G. F. & Grenfell, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology 101, 139–43.CrossRefGoogle ScholarPubMed
Halvorsen, O. & Andersen, K. (1984). The ecolgical interaction between arctic charr, Salvenlinus alphinus (L.) and the plerocercoid stage of Diphyllobothrium ditremum. Journal of Fish Biology 25, 305–16.CrossRefGoogle Scholar
Hardin, E. L. & Janovy, J. (1988). Populations dynamics of Distoichometra bufonis (Cestoda: Nematotaeniidae) in Bufo woodhousii. Journal of Parasitology 74, 360–5.CrossRefGoogle Scholar
Harvey, P. H. & Godfray, H. C. J. (1987). How species divide resources. American Naturalist 129, 318–20.CrossRefGoogle Scholar
Hassell, M. P., Comins, H. N. & May, R. M. (1991). Spatial structure and chaos in insect population dynamics. Nature 353, 255–8.CrossRefGoogle Scholar
Haukisalmi, V., Henttonen, H. & Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–25.CrossRefGoogle Scholar
Helle, T. (1980). Abundance of warble fly (Oedemagena tarandi) larvae in semi-domestic reindeer (Rangifer tarandus) in Finland. Reports of Kevo Subarctic Research Statistics 16, 1–6.Google Scholar
Henricson, J. (1977). The abundance and distribution of Diphyllobothrium dendriticum (Nitzsch) and D. ditremum (Creplin) in the charr Salvelinus alpinus (L.) in Sweden. Journal of Fish Biology 11, 231–48.CrossRefGoogle Scholar
Heyneman, D. (1958). Effect of temperature on the rate of development and viability of the cestode, Hymenolepis nana in its intermediate host. Experimental Parasitology 7, 374–82.CrossRefGoogle ScholarPubMed
Hodasi, J. K. M. (1969). Comparative studies on the helminth fauna of native and introduced domestic fowls in Ghana. Journal of Helminthology 43, 35–52.CrossRefGoogle ScholarPubMed
Hominick, W. M., Dean, C. G. & Schad, G. A. (1987). Population biology of hookworms in West Bengal: analysis of numbers of infective larvae recovered from damp pads applied to the soil surface at defaecation sites. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 978–87.CrossRefGoogle Scholar
Hopkins, C. A. (1959). Seasonal variations in the incidence and development of the cestode Proteocephalus filicollis (Rud. 1810) in Gasterosteus aculeatus (L. 1766). Parasitology 49, 529–42.CrossRefGoogle ScholarPubMed
Hudson, P. J., Dobson, A. P. & Newborn, D. (1992). Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology 61, 681–92.CrossRefGoogle Scholar
Ignoffo, C. M. (1959). Louse populations of some rodents of the Great Salt Lake Desert. Parasitology 49, 511–18.CrossRefGoogle ScholarPubMed
Jacobs, D. E. & Dunn, A. M. (1969). Helminths of Scottish pigs: Occurrence, age incidences and seasonal variation. Journal of Helminthology 43, 327–40.CrossRefGoogle Scholar
James, B. L. & Llewellyn, L. C. (1967). A quantitative analysis of helminth infestation in some Passerine birds found dead on the island of Skomer. Journal of Helminthology 41, 19–44.CrossRefGoogle Scholar
Jarroll, E. L. Jr (1970). Population biology of Bothriocephalus rarus Thomas (1937) in the red-spotted newt, Notophthalmus viridescens Raf. Parasitology 79, 183–93.CrossRefGoogle Scholar
Jarroll, E. L. Jr (1980). Population dynamics of Bothriocephalus rarus (Cestoda) in Notophthalmus viridescens. American Midland Naturalist 103, 360–6.CrossRefGoogle Scholar
Kennedy, C. R. (1969). Seasonal incidence and development of the cestode Caryophyllaeus laticeps (Pallas) in the River Avon. Parasitology 59, 783–94.CrossRefGoogle ScholarPubMed
Kennedy, C. R. (1981). The establishment and population biology of th eye-fluke Tylodelphys podicipina (Digenea: Diplostomatidae) in perch. Parasitology 82, 245–55.CrossRefGoogle Scholar
Kennedy, C. R. (1984). The dynamics of a declining population of the acanthocephalan Acanthocephalus clavula in eels Enguilla anguilla in a small river. Journal of Fish Biology 25, 665–77.CrossRefGoogle Scholar
Kennedy, C. R. & Moriarty, C. (1987). Co-existence of congenic species of Acanthocephala: Acanthocephalus lucii and Acanthocephalus anguillae in eels Anguilla anguilla in Ireland. Parasitology 95, 301–10.CrossRefGoogle Scholar
Keymer, A. E. (1982 a). Tapeworm infections. In Population Dynamics of Infectious Diseases: Theory and Applications (ed. Anderson, R. M.), pp. 109–138. London: Chapman and Hall.CrossRefGoogle Scholar
Keymer, A. E. (1982 b). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–87.CrossRefGoogle ScholarPubMed
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, 195–207.CrossRefGoogle ScholarPubMed
Keymer, A. E. & Dobson, A. P. (1987). The ecology of helminths in populations of small mammals. Mammal Review 17, 105–16.CrossRefGoogle Scholar
Lee, R. L. G. (1981). Ecology of Acanthocephalus lucii (Müller, 1776) in perch, Perca fluviatilis, in the Serpentine, London, UK. Journal of Helminthology 55, 149–54.CrossRefGoogle Scholar
Lees, E. (1962). The incidence of helminth parasites in a particular frog population. Parasitology 52, 95–102.CrossRefGoogle Scholar
Lewis, J. W. (1966). Maritrema apodemicum sp. nov. (Digenea: Microphallidae) from the Long Tailed Field Mouse Apodemus sylvaticus sylvaticus (L.) on Skomer Island. Journal of Helminthology 40, 363–74.CrossRefGoogle Scholar
Lewis, J. W. (1978). A population study of the metastrongylid nematode Skrjabingylus nasicola in the weasel Mustela nivalis. Journal of Zoology, London 184, 225–9.CrossRefGoogle Scholar
Li, S. Y. & Shu, H. F. (1951). On the frequency distribution of helminths in their naturally infected hosts. Journal of Parasitology 37, 32–41.CrossRefGoogle ScholarPubMed
Liat, L. B. & Pike, A. W. (1980). The incidence and distribution of Profilicollis botulus (Acanthocephala) in the eider duck, Somateria mollissima, and its intermediate host the shore crab, Carcinus maenas, in north east Scotland. Journal of Zoology, London 190, 39–51.CrossRefGoogle Scholar
Lloyd, M. (1967). Mean crowding. Journal of Animal Ecology 36, 1–30.CrossRefGoogle Scholar
Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F. & Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797–805.CrossRefGoogle ScholarPubMed
May, R. M. (1975). Patterns of species abundance and diversity. In Ecology and Evolution of Communities (ed. Cody, M. L. & Diamond, J. M.), pp. 81–120. Cambridge, Massachusetts: Harvard University Press.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, 248–67.CrossRefGoogle Scholar
Mayfield, R. B. (1938). Ratfleas in Plymouth. Parasitology 30, 314–19.CrossRefGoogle Scholar
Mead-Briggs, A. R. & Page, R. J. C. (1975). Records of anoplocephaline cestodes from wild rabbits and hares colected throughout Great Britain. Journal of Helminthology 49, 49–56.Google Scholar
Mead-Briggs, A. R. & Vaughan, J. A. (1973). The incidence of Anoplocephaline cestodes in a population of rabbits in Surrey, England. Parasitology 67, 351–64.CrossRefGoogle Scholar
Medley, G. F. (1992). Which came first in host-parasite systems: density dependence or parasite distribution? Parasitology Today 8, 321–2.CrossRefGoogle ScholarPubMed
Medley, G. F., Guyatt, H. L. & BUNDY, D. A. P. (1993 a). A quantitative framework from evaluating the effect of community treatment on the morbidity due to ascariasis. Parasitology 106, 211–21.CrossRefGoogle ScholarPubMed
Medley, G. F., Sinden, R. E., Fleck, S., Billingsley, P. F., Tirawanchai, N. & Rodriguez, M. H. (1993 b). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441–9.CrossRefGoogle ScholarPubMed
Michel, J. F. (1963). The phenomena of host resistance and the course of infection of Ostertagia ostertagi in calves. Parasitology 53, 63–84.CrossRefGoogle Scholar
Milne, A. (1943). The comparison of sheep-tick populations (Ixodes ricinus L.). Annals of Applied Biology 30, 240–53.CrossRefGoogle Scholar
Mykytowycz, R. (1964). A survey of the endoparasites of the Red Kangaroo Megaleia rufa (Desmarest). Parasitology 54, 677–93.CrossRefGoogle ScholarPubMed
Nee, S., Harvey, P. H. & May, R. M. (1991). Lifting the veil on abundance patterns. Proceedings of the Royal Society of London Series B-Biological Sciences 243, 161–3.Google Scholar
Neyman, J. (1939). On a new class of ‘contagious’ distributions, applicable in entomology and bacteriology. Annals of Mathematical Statistics 10, 35–57.CrossRefGoogle Scholar
Nuorteva, P. (1966). Corynosoma strumosum (Rud.) and C. semerne (Forssell) (Acanthocephala) as pathogenic parasites of farmed minks in Finland. Journal of Helminthology 40, 77–80.CrossRefGoogle Scholar
Pacala, S. W. & Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle ScholarPubMed
Pemberton, R. T. (1963). Helminth parasites of three species of British gulls, Larus argentatus Pont., L. fuscus L. and L. ridibundus L. Journal of Helminthology 37, 57–88.CrossRefGoogle Scholar
Pence, D. B. & Windberg, L. A. (1984). Population dynamics across selected habitat variables of the helminth community in coyotes, Canis latrans, from South Texas. Journal of Parasitology 70, 733–46.CrossRefGoogle ScholarPubMed
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
Pielou, E. C. (1969). An Introduction to Mathematical Ecology. New York: Wile Interscience.Google Scholar
Pojmanska, T. (1982). The co-occurrence of three species of Diorchis Clerc, 1903 (Cestoda: Hymenolepididae) in the European coot Fulica atra L. Parasitology 84, 419–29.CrossRefGoogle Scholar
Pölya, G. (1931). Sur quelques points de la théorie des probabilités. Annales de Institute Henri Poincaré 1, 117–61.Google Scholar
Preston, F. W. (1948). The commonness, and rarity, of species. Ecology 29, 254–83.CrossRefGoogle Scholar
Rees, G. (1950). Observations on the vertical migrations of the third-stage larva of Haemonchus contortus (rud) on experimental plots of Lolium perenne s24, in relation to meteorlogical and micrometerological factors. Parasitology 40, 127–43.CrossRefGoogle Scholar
Rees, G. (1970). Some helminth parasites of fishes of Bermuda and an account of the attachment organ of Alcicornis carangis MacCallum, 1917 (Digenea: Bucephalidae). Parasitology 60, 195–221.CrossRefGoogle Scholar
Schmid, W. D. & Robinson, E. J. (1972). The pattern of a host-parasite distribution. Journal of Parasitology 58, 907–10.CrossRefGoogle ScholarPubMed
Scott, M. E. (1987). Temporal changes in aggregation: a laboratory study. Parasitology 94, 583–95.CrossRefGoogle ScholarPubMed
Sekhar, C. S. & Threlfall, W. (1970). Helminth parasites of the Cunner, Tautogolabrus adspersus (Walbaum) in Newfoundland. Journal of Helminthology 44, 169–88.CrossRefGoogle Scholar
Skellam, J. G. (1951). Random dispersal in theoretical populations. Biometrika 38, 196–218.CrossRefGoogle ScholarPubMed
Skorping, A. (1981). Seasonal dynamics in abundance, development and pattern of infection of Bundodera luciopercae (Muller) in perch, Perca fluviatilis L. from an oligotrophic lake in Norway. Journal of Fish Biology 18, 401–10.CrossRefGoogle Scholar
Skorping, A. (1985). Parasite-induced reduction in host survival and fecundity: the effect of the nematode Elaphostrongylus rangiferi on the snail intermediate host. Parasitology 91, 555–62.CrossRefGoogle Scholar
Smith, G. & Grenfell, B. T. (1994). Modelling of parasite populations – gastrointestinal nematode models. Veterinary Parasitology 54, 127–43.CrossRefGoogle ScholarPubMed
Smith, G., Grenfell, B. T. & Anderson, R. M. (1986). The development and mortality of the non-infective free-living stages of Ostertagia ostertagi in the field and in laboratory culture. Parasitology 92, 471–82.CrossRefGoogle ScholarPubMed
Sonquist, J. N. & Morgan, J. N. (1964). The Detection of Interaction Effects. Michigan: University of Michigan.Google Scholar
Southwood, T. R. E. (1966). Ecological Methods, 2nd edn.London: Chapman & Hall.Google Scholar
Stromberg, P. C., Toussant, M. J. & Dubey, J. P. (1978). Population biology of Paragonimus kellicoti metacercariae in central Ohio. Parasitology 77, 13–18.CrossRefGoogle Scholar
Taylor, L. R. (1961). Aggregation, variance and the mean. Nature 189, 732–5.CrossRefGoogle Scholar
Taylor, L. R. & Taylor, R. A. J. (1977). Aggregation, migration and population dynamics. Nature 265, 415–21.CrossRefGoogle Scholar
Taylor, L. R. & Woiwod, I. P. (1980). Temporal stability as a density-dependent species characteristic. Journal of Animal Ecology 49, 209–24.CrossRefGoogle Scholar
Taylor, L. R., Woiwod, I. P. & Perry, J. N. (1978). The density-dependence of spatial behaviour and the rarity of randomness. Journal of Animal Ecology 47, 383–406.CrossRefGoogle Scholar
Thomas, J. D. (1964). A comparison between the helminth burdens of male and female brown trout, Salmo trutta L., from a natural population in the River Teifi, West Wales. Parasitology 54, 263–72.CrossRefGoogle Scholar
Thomas, M. (1949). A generalisation of poisson's binomial limit for use in ecology. Biometrika 36, 18–25.CrossRefGoogle ScholarPubMed
Threlfall, W. (1968). Helminths recovered from Wilson's Snipe, Capella gallinago delicata. Journal of Helminthology 42, 173–8.CrossRefGoogle Scholar
Tilman, D. (1994). Competition and biodiversity in spatially structured habitats. Ecology 75, 2–16.CrossRefGoogle Scholar
Udonsi, J. K. (1990). Human community ecology of urinary schistosomiasis in relation to snail vector bionomics in the Igwun River Basin of Nigeria. Tropical Medicine and Parasitology 41, 131–5.Google ScholarPubMed
Van Den Broek, E. L. F. (1979). Copepod ectoparasites of Merlangius merlangus and Platichthys flesus. Journal of Fish Biology 14, 371–80.CrossRefGoogle Scholar
Vanparijs, O. F. J. & Thienport, D. C. (1973). Canine and feline helminth and protozoan infections in Belgium. Journal of Parasitology 59, 327–30.CrossRefGoogle ScholarPubMed
Vincent, A. L. (1972). Parasites of the starling, Sturnus vulgaris, in San Diego County, California. Journal of Parasitology 58, 1020–2.CrossRefGoogle ScholarPubMed
Wakelin, D. (1964). A survey of the intestinal helminths parasitic in British domestic fowl. Journal of Helminthology 38, 191–200.CrossRefGoogle ScholarPubMed
Waller, P. J. & Thomas, R. J. (1978). Nematode parasitism in sheep in north-east England: The epidemiology of Ostertagia species. International Journal for Parasitology 8, 275–83.CrossRefGoogle ScholarPubMed
Warren, E. G. (1970). Observation on the life-cycle of Toxocara mackerrasae. Parasitology 60, 239–53.CrossRefGoogle ScholarPubMed
Williams, C. B. (1964). Patterns in the Balance of Nature, and Related Problems in Quantitative Biology. London: Academic Press.Google Scholar
Williams, I. C. (1963). The infestation of the redfish Sebastes marinus (L.) and S. mentella Travin (Scleroparei: Scorpaenidae) by the copepods Peniculus clavatus (Müller), Sphyrion lumpi (Kroyer) and Chondracanthopsis nodusus (Müller) in the eastern North Atlantic. Parasitology 53, 501–25.CrossRefGoogle Scholar
Williams, I. C. (1965). The stomach worm Tetrameres fissipina (Diesing, 1861) (Nematoda: Spiruridea) infecting the wood-pigeons, Columba palumbrus L., and Stock dove, C. oenas L., in Cambridgeshire. Journal of Helminthology 39, 303–8.CrossRefGoogle Scholar
Williams, R. T. (1972). The distribution and abundance of the ectoparasites of the wild rabbit, Oryctolagus cuniculus (L.), in New South Wales, Australia. Parasitology 64, 321–30.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J. & Chandiwana, S. K. (1989). Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology 98, 21–34.CrossRefGoogle ScholarPubMed
Wootten, R. (1973 a). Occurrence of the metacercariae of Cotylurus erraticus (Rudolphi, 1809) Szidat, 1928 (Digenea: Strigeidae) in Brown Trout Salmo trutta L., and Rainbow Trout S. gairdneri Richardson, 1836, from Hanningfield Reservoir, Essex. Journal of Helminthology 47, 389–8.CrossRefGoogle ScholarPubMed
Wootten, R. (1973 b). Occurrence of Bunodera luciopercae (Digenea: Allocreadiidae) in Fish from Hanningfield Reservoir, Essex. Journal of Helminthology 47, 399–408.CrossRefGoogle ScholarPubMed
Wootten, R. (1974). Observations on strigeid metacercariae in the eyes of fish from Hanningfield Reservoir, Essex, England. Journal of Helminthology 48, 73–83.CrossRefGoogle ScholarPubMed
Yanez, D. M. & Canaris, A. G. (1988). Metazoan parasite community composition and structure of migrating Wilson's Phalarope, Steganopus tricolor Viellot, 1819 (Aves), From El Paso County, Texas. Journal of Parasitology 74, 754–62.CrossRefGoogle Scholar