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Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions .... or pure randomness?

Published online by Cambridge University Press:  27 March 2008

J. M. BEHNKE*
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG2 7TR, UK
*
*Corresponding author. Tel: +44 (0)115 951 3208. Fax: +44(0)115 951 3251. E-mail: [email protected]

Summary

Experimental data establish that interactions exist between species of intestinal helminths during concurrent infections in rodents, the strongest effects being mediated through the host's immune responses. Detecting immune-mediated relationships in wild rodent populations has been fraught with problems and published data do not support a major role for interactions in structuring helminth communities. Helminths in wild rodents show predictable patterns of seasonal, host age-dependent and spatial variation in species richness and in abundance of core species. When these are controlled for, patterns of co-infection compatible with synergistic interactions can be demonstrated. At least one of these, the positive relationship between Heligmosomoides polygyrus and species richness of other helminths has been demonstrated in three totally independent data-sets. Collectively, they explain only a small percentage of the variance/deviance in abundance data and at this level are unlikely to play a major role in structuring helminth communities, although they may be important in the more heavily infected wood mice. Current worm burdens underestimate the possibility that earlier interactions through the immune system have taken place, and therefore interactions may have a greater role to play than is immediately evident from current worm burdens. Longitudinal studies are proposed to resolve this issue.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93100.CrossRefGoogle Scholar
Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (2000). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 716.CrossRefGoogle ScholarPubMed
Adams, D. B., Anderson, B. H. and Windon, R. G. (1989). Cross-immunity between Haemonchus contortus and Trichostrongylus colubriformis in sheep. International Journal for Parasitology 19, 717722.CrossRefGoogle ScholarPubMed
Alghali, S. T. O., Hagan, P. and Robinson, M. (1985). Hymenolepis citelli (Cestoda) and Nematospiroides dubius (Nematoda): interspecific interaction in mice. Experimental Parasitology 60, 369370.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411426.CrossRefGoogle ScholarPubMed
Anthony, R. M., Urban, J. F. Jr., Alem, F., Hamed, H. A., Rozo, C. T., Boucher, J.-L., Rooijen, N. V. and Gause, W. C. (2006). Memory Th2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nature, Medicine 12, 955960.CrossRefGoogle ScholarPubMed
Arneberg, P. (2001). An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352358.CrossRefGoogle Scholar
Artis, D. (2006). New weapons in the war on worms: identification of putative mechanisms of immune-mediated expulsion of gastrointestinal nematodes. International Journal for Parasitology 36, 723733.CrossRefGoogle ScholarPubMed
Artis, D., Wang, M. L., Keilbaugh, S. A., He, W., Brenes, M., Swain, G. P., Knight, P. A., Donaldson, D. D., Lazar, M. A., Miller, H. R. P., Schad, G. A., Scott, P. and Wu, G. D. (2004). RELMβ/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proceedings of the National Academy of Sciences, USA 101, 1359613600.CrossRefGoogle ScholarPubMed
Ashford, R. W. (1991). The human parasite fauna: towards an analysis and interpretation. Annals of Tropical Medicine and Parasitology 85, 189198.CrossRefGoogle ScholarPubMed
Ashford, R. W., Craig, P. S. and Oppenheimer, S. J. (1992). Polyparasitism on the Kenyan coast. 1. Prevalence and association between parasitic infections. Annals of Tropical Medicine and Parasitology 86, 671679.CrossRefGoogle Scholar
Bajer, A., Bednarska, M., Pawełczyk, A., Behnke, J. M., Gilbert, F. S. and Siński, E. (2002). Prevalence and abundance of Cryptosporidium parvum and Giardia spp. in wild rural rodents from the Mazury Lake District region of Poland. Parasitology 125, 2134.CrossRefGoogle ScholarPubMed
Bajer, A., Behnke, J. M., Bednarska, M., Kuliś, K. and Siński, E. (2004). Współwystępowanie Cryptosporidium parvum, Giardia spp. i helmintów w populacjach drobnych gryzoni. Wiadomosci Parazytologiczne 50, 307315 (In Polish).Google Scholar
Bajer, A., Behnke, J. M., Pawełczyk, A., Kulis, K., Sereda, M. J. and Siński, E. (2005). Medium-term temporal stability of the helminth component community structure in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 130, 213228.CrossRefGoogle ScholarPubMed
Bajer, A., Harris, P. D., Behnke, J. M., Bednarska, M., Barnard, C. J., Sherif, N., Clifford, S., Gilbert, F. S., Siński, E. and Zalat, S. (2006). Local variation of haemoparasites and arthropod vectors, and intestinal protozoa in spiny mice (Acomys dimidiatus) from four montane wadis in the St. Katherine Protectorate, Sinai, Egypt. Journal of Zoology 270, 924.CrossRefGoogle Scholar
Bajer, A., Pawełczyk, A., Behnke, J. M., Gilbert, F. S. and Siński, E. (2001). Factors affecting the haemoparasitic component community structure in bank voles (Clethrionomys glareolus) from the Mazury lake district region of Poland. Parasitology 122, 4354.CrossRefGoogle ScholarPubMed
Barnard, C. J., Behnke, J. M., Bajer, A., Bray, D., Race, T., Frake, K., Osmond, J., Dinmore, J. and Siński, E. (2002). Local variation in endoparasite intensities of bank voles (Clethrionomys glaroelus) from ecologically similar sites: morphometric and endocrine correlates. Journal of Helminthology 76, 103112.CrossRefGoogle ScholarPubMed
Begon, M., Townsend, C. R. and Harper, J. L. (2005). Ecology. Fourth Edition, Blackwell Publishing, Oxford.Google Scholar
Behnke, J. M. and Ali, N. M. H. (1984). Survival to patency of low level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Annals of Tropical Medicine and Parasitology 78, 509517.CrossRefGoogle ScholarPubMed
Behnke, J. M., Bajer, A., Siński, E. and Wakelin, D. (2000). Interactions involving rodent nematodes: experimental and field studies. Parasitology 122, S39S49.CrossRefGoogle Scholar
Behnke, J. M. and Barnard, C. J. (1990). Coevolution of parasites and hosts: host-parasite arms races and their consequences.. In Parasites: Immunity and Pathology. The Consequences of Parasitic Infection in Mammals (ed. Behnke, J. M.), Chapter 1, pp. 122. Taylor and Francis, London.CrossRefGoogle Scholar
Behnke, J. M., Barnard, C. J., Bajer, A., Bray, D., Dinmore, J., Frake, K., Osmond, J., Race, T. and Siński, E. (2001). Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123, 401414.CrossRefGoogle ScholarPubMed
Behnke, J. M., Barnard, C. J. and Wakelin, D. (1992). Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861907.CrossRefGoogle ScholarPubMed
Behnke, J. M., Bland, P. W. and Wakelin, D. (1977). Effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in mice. Parasitology 75, 7988.CrossRefGoogle ScholarPubMed
Behnke, J. M., Lewis, J. W., Mohd Zain, S. N. and Gilbert, F. S. (1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 3144.CrossRefGoogle ScholarPubMed
Behnke, J. M., Gilbert, F. S., Abu-Madi, M. A. and Lewis, J. W. (2005). Do the helminth parasites of wood mice interact Journal of Animal Ecology 74, 982993.CrossRefGoogle Scholar
Behnke, J. M., Harris, P. D., Bajer, A., Barnard, C. J., Sherif, N., Cliffe, L., Hurst, J., Lamb, M., Rhodes, A., James, M., Clifford, S., Gilbert, F. S. and Zalat, S. (2004). Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St. Katherine region of the Sinai Peninsula in Egypt. Parasitology 129, 379398.CrossRefGoogle ScholarPubMed
Behnke, J. M., Rose, R. and Little, J. (1994). Resistance of the hookworms Ancylostoma ceylanicum and Necator americanus to intestinal inflammatory responses induced by heterologous infection. International Journal for Parasitology 24, 91101.CrossRefGoogle ScholarPubMed
Behnke, J. M., Wakelin, D. and Wilson, M. M. (1978). Trichinella spiralis: delayed rejection in mice concurrently infected with Nematospiroides dubius. Experimental Parasitology 46, 121130.CrossRefGoogle ScholarPubMed
Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A. P., Potts, S. G., Kleukers, R., Thomas, C. D., Settele, J. and Kunin, W. E. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351353.CrossRefGoogle ScholarPubMed
Booth, M. and Bundy, D. A. P. (1992). Comparative prevalences of Ascaris lumbricoides, Trichuris trichiura, and hookworm infections and the prospects for control. Parasitology 105, 151157.CrossRefGoogle ScholarPubMed
Booth, M., Bundy, D. A., Albonico, M., Chwaya, H. M., Alawi, K. S. and Savioli, L. (1998). Associations among multiple geohelminth species infections in schoolchildren from Pemba Island. Parasitology 116, 8593.CrossRefGoogle ScholarPubMed
Bottomley, C., Isham, V. and Basanez, M.-G. (2005). Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 131, 417433.CrossRefGoogle ScholarPubMed
Brouat, C., Kane, M., Diouf, M., , K., Sall-Dramé, R. and Duplantier, J. M. (2007). Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134, 437450.CrossRefGoogle ScholarPubMed
Bruce, R. G. and Wakelin, D. (1977). Immunological interactions between Trichinella spiralis and Trichuris muris in the intestine of the mouse. Parasitology 74, 163173.CrossRefGoogle Scholar
Bruna, C. D. and 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, 490491.CrossRefGoogle ScholarPubMed
Buck, A. A., Anderson, R. I. and MacRae, A. A. (1978 a). Epidemiology of poly-parasitism. II. Types of combinations, relative frequency and associations of multiple infections. Tropenmedizin und Parasitologie 29, 137144.Google ScholarPubMed
Buck, A. A., Anderson, R. I. and MacRae, A. A. (1978 b). Epidemiology of poly-parasitism. IV. Combined effects on the state of health. Tropenmedizin und Parasitologie 29, 253268.Google ScholarPubMed
Bundy, D. A. P. (1988). Population ecology of intestinal helminth infections in human communities. Philosophical Transactions of the Royal Society of London B321, 405420.Google Scholar
Bush, A. O., Heard, R. W. and Overstreet, R. M. (1993). Intermediate hosts as source communities. Canadian Journal of Zoology 71, 13581363.CrossRefGoogle Scholar
Bush, A. O. and Holmes, J. C. (1986). Intestinal parasites of lesser scaup duck: an interactive community. Canadian Journal of Zoology 64, 142152.CrossRefGoogle Scholar
Castro, G. A., Olson, L. R. and Baker, R. D. (1967). Glucose malabsorption and intestinal histopathology in Trichinella spiralis infected guinea pigs. Journal of Parasitology 53, 595612.CrossRefGoogle ScholarPubMed
Christensen, N. O., Nansen, P., Fagbeni, B. O. and Monrad, J. (1987). Heterologous antagonistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.CrossRefGoogle ScholarPubMed
Christie, P. R., Wakelin, D. and Wilson, M. M. (1979). The effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in rats. Parasitology 78, 323330.CrossRefGoogle ScholarPubMed
Courtney, C. H. and Forrester, D. J. (1973). Interspecific interactions between Hymenolepis microstoma (Cestoda) and Heligmosomoides polygyrus (Nematoda) in mice. Journal of Parasitology 59, 480483.CrossRefGoogle ScholarPubMed
Dehlawi, M. S., Wakelin, D. and Behnke, J. M. (1987). Suppression of mucosal mastocytosis by infection with the intestinal nematode Nematospiroides dubius. Parasite Immunology 9, 187194.CrossRefGoogle ScholarPubMed
Dawkins, R. and Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society, London B205, 489511.Google Scholar
Diez-Baňos, N., Cabaret, J. and Diez-Baňos, P. (1992). Interspecific interactions in naturally acquired nematode communities from sheep abomasum in relation to age of host and season in four areas of Leon (Spain). International Journal for Parasitology 22, 327334.CrossRefGoogle ScholarPubMed
Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317347.CrossRefGoogle ScholarPubMed
Druilhe, P., Tall, A. and Sokhna, C. (2005). Worms can worsen malaria: towards a new means to roll back malaria Trends in Parasitology 21, 359362.CrossRefGoogle ScholarPubMed
Eira, C., Torres, J., Vingada, J. and Miquel, J. (2006). Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus in Dunas de Mira, Portugal. Acta Parasitologica 51, 300308.CrossRefGoogle Scholar
Else, K. J. and Finkelman, F. D. (1999). Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 11451158.CrossRefGoogle Scholar
Elton, C. (1927). Animal Ecology. Sidgwick & Jackson, London, republished in 2001 by The University of Chicago Press, Chicago.Google Scholar
Esch, G. W., Shostak, A. W., Marcogliese, D. J. and Goater, T. M. (1990). Patterns and processes in helminth parasite communities: an overview. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 119. Chapman and Hall, London.Google Scholar
Ezeamama, A. E., Friedman, J. F., Olveda, R. M., Acosta, L. P., Kurtis, J. D., Mor, V. and McGarvey, S. T. (2005). Functional significance of low-intensity polyparasite helminth infections in anaemia. Journal of Infectious Diseases 192, 21602170.CrossRefGoogle Scholar
Gause, W. C., Urban, J. F. Jr. and Stadecker, M. J. (2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269277.CrossRefGoogle ScholarPubMed
Graham, A. L. (2002). When T-helper cells don't help: immunopathology during concomitant infections. The Quarterly Review of Biology 77, 409434.CrossRefGoogle Scholar
Graham, A. L. (2008). Ecological rules governing helminth-microparasite coinfection. Proceedings of the National Academy, USA 105, 566570.CrossRefGoogle ScholarPubMed
Graham, A. L., Cattadori, I. M., Lloyd-Smith, J. O., Ferrari, M. J. and Bjornstad, O. N. (2007). Transmission consequences of coinfection: cytokines writ large? Trends in Parasitology 23, 284291.CrossRefGoogle ScholarPubMed
Guernier, V., Hochberg, M. E. and Guegan, J.-F. (2004). Ecology drives the worldwide distribution of human diseases. PLoS Biology 2, 740746.CrossRefGoogle ScholarPubMed
Hanski, I. (1982). Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38, 210221.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (1990). The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia 83, 309315.CrossRefGoogle ScholarPubMed
Haukisalmi, V. and Henttonen, H. (1993). Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221229.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (1998). Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia 116, 565574.CrossRefGoogle ScholarPubMed
Haukisalmi, V. and Henttonen, H. (2000). Variability of helminth assemblages and populations in the bank vole Clethrionomys glareolus. Polish Journal of Ecology 48 (Suppl.), 219231.Google Scholar
Hazel, S. M., Bennett, M., Chantrey, J., Bown, K., Cavanagh, R., Jones, T. R., Baxby, D. and Begon, M. (2000). A longitudinal study of an endemic disease in its wildlife reservoir: cowpox and wild rodents. Epidemiology and Infection 124, 551562.CrossRefGoogle ScholarPubMed
Holland, C. V., Asaolu, S. O., Crompton, D. W. T., Stoddart, R. C., MacDonald, R. and Torimiro, S. E. A. (1989). The epidemiology of Ascaris lumbricoides and other soil-transmitted helminths in primary school children from Ile-Ife, Nigeria. Parasitology 99, 275285.CrossRefGoogle ScholarPubMed
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, 209216.CrossRefGoogle Scholar
Holmes, J. C. (1962 a). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala) 2. Effects on growth. Journal of Parasitology 48, 8796.CrossRefGoogle Scholar
Holmes, J. C. (1962 b). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala) 2. Effects in hamsters. Journal of Parasitology 48, 97100.CrossRefGoogle Scholar
Holmes, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site segregation and their importance to the development of the helminth communities. Canadian Journal of Zoology 51, 333347.CrossRefGoogle Scholar
Hopkins, C. A. (1980). Immunity and Hymenolepis diminuta. In Biology of theTapeworm Hymenolpis diminuta (ed. Arai, H. A.), pp. 551614. Academic Press, New York.CrossRefGoogle Scholar
Howard, R. J., Christie, D., Wakelin, D., Wilson, M. M. and Behnke, J. M. (1978). The effect of concurrent infection with Trichinella spiralis on Hymenolepis microstoma in mice. Parasitology 77, 273279.CrossRefGoogle ScholarPubMed
Howard, S. C., Donnelly, C. A. and Chan, M.-S. (2001). Methods for estimation of associations between multiple species parasite infections. Parasitology 122, 233251.CrossRefGoogle ScholarPubMed
Howard, S. C., Donnelly, C. A., Kabatereine, N. B., Ratard, R. C. and Brooker, S. (2002). Spatial and intensity-dependent variations in associations between multiple species helminth infections. Acta Tropica 83, 141149.CrossRefGoogle ScholarPubMed
Hudson, P. J., Cattadori, I. M., Boag, B. and Dobson, A. P. (2006). Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology 80, 175182.CrossRefGoogle ScholarPubMed
Janovy, J. Jr. (2002). Concurrent infections and the community ecology of helminth parasites. Journal of Parasitology 88, 440445.CrossRefGoogle ScholarPubMed
Jenkins, D. C. (1975). The influence of Nematospiroides dubius on subsequent Nippostrongylus brasiliensis infections in mice. Parasitology 71, 349355.CrossRefGoogle ScholarPubMed
Jenkins, S. N. and Behnke, J. M. (1977). Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 7178.CrossRefGoogle ScholarPubMed
Keusch, G. T. and Migasena, P. (1982). Biological implications of polyparasitism. Reviews of Infectious Diseases 4, 880882.CrossRefGoogle ScholarPubMed
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587.CrossRefGoogle ScholarPubMed
Kennedy, M. W. (1980). Immunologically mediated, non-specific interactions between the intestinal phases of Trichinella spiralis and Nippostrongylus brasiliensis in the mouse. Parasitology 80, 6172.CrossRefGoogle ScholarPubMed
Kisielewska, K. (1970 a). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). III. Structure of the helminth groupings in C. glareolus populations of various forest biocoenoses in Poland. Acta Parasitologica Polonica 18, 163176.Google Scholar
Kisielewska, K. (1970 b). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). V. Some questions concerning helminth groupings in the host individuals. Acta Parasitologica Polonica 17, 197208.Google Scholar
Kisielewska, K. (1970 c). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). 1. Structure and seasonal dynamics of helminth groupings in a host population in the Bialowieża National Park. Acta Parasitologica Polonica 18, 121147.Google Scholar
Kvalsvig, J. D. (1988). The effects of parasitic infection on cognitive performance. Parasitology Today 4, 206208.CrossRefGoogle ScholarPubMed
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840844.CrossRefGoogle ScholarPubMed
Lotz, J. M. and Font, W. F. (1994). Excess positive associations in communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398413.CrossRefGoogle Scholar
Loukas, A. and Prociv, P. (2001). Immune responses in hookworm infections. Clincial and Microbiological Reviews 14, 689703.CrossRefGoogle ScholarPubMed
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunological Reviews 201, 89116.CrossRefGoogle ScholarPubMed
Mercer, J. G., Mitchell, P. I., Moar, K. M., Bissett, A., Geissler, S., Bruce, K. and Chappell, L. H. (2000). Anorexia in rats infected with the nematode, Nippostrongylus brasiliensis: experimental manipulations. Parasitology 120, 641647.CrossRefGoogle ScholarPubMed
Mimori, T., Nawa, Y., Korenaga, M. and Tada, I. (1983). Nippostrongylus brasiliensis and Strongyloides ratti: concurrent infection in normal and immunized rats. Australian Journal of Experimental Biology and Medical Science 61, 435437.CrossRefGoogle ScholarPubMed
Montgomery, S. S. J. and Montgomery, W. I. (1988). Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice Apodemus sylvaticus. Journal of Helminthology 62, 7890.CrossRefGoogle ScholarPubMed
Montgomery, S. S. J. and Montgomery, W. I. (1990). Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225242.CrossRefGoogle ScholarPubMed
Moqbel, R. and Wakelin, D. (1979). Trichinella spiralis and Strongyloides ratti: immune interaction in adult rats. Experimental Parasitology 47, 6572.CrossRefGoogle ScholarPubMed
Murphy, K. M., Travers, P. and Walport, M. (2008). Janeway's Immunobiology (7th Edition). Garland Science Publications, London.Google Scholar
Nacher, M. (2002). Worms and malaria: noisy nuisances and silent benefits. Parasite Immunology 24, 391393.CrossRefGoogle ScholarPubMed
Nair, M. G., Guild, K. J. and Artis, D. (2006). Novel effector molecules in the type 2 inflammation: lessons drawn from helminth infection and allergy. Journal of Immunology 177, 13931399.CrossRefGoogle ScholarPubMed
Nawa, Y., Mimori, T., Korenaga, M. and Tada, I. (1982). Stage-specific cross-resistance between Nippostrongylus brasiliensis and Strongyloides ratti (Nematoda) in rats. Journal of Parasitology 68, 804808.CrossRefGoogle ScholarPubMed
Nilssen, A. C., Haugerud, R. E. and Folstad, I. (1998). No interspecific covariation in intensities of macroparasites of reindeer, Rangifer tarandus (L.). Parasitology 117, 273281.CrossRefGoogle ScholarPubMed
Nilsson, L. A. (1998). Deep flowers for long tongues. Trends in Ecology and Evolution 13, 259260.CrossRefGoogle ScholarPubMed
Pedersen, A. B. and Fenton, A. (2006). Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133139.CrossRefGoogle ScholarPubMed
Pemberton, A. D., Knight, P. A., Gamble, J., Colledge, W. H., Lee, J.-K., Pierce, M. and Miller, H. R. P. (2004). Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, Intelectin-2, and its natural deletion in C57BL/10 mice. Journal of Immunology 173, 18941901.CrossRefGoogle ScholarPubMed
Petney, T. N. and Andrews, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377393.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites. From Individuals to Communities. Chapman and Hall, London.Google Scholar
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3S11.CrossRefGoogle ScholarPubMed
Poulin, R. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Reviews in Ecology and Systematics 28, 341358.CrossRefGoogle Scholar
Poulin, R. (2004). Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423434.CrossRefGoogle Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, New Jersey.Google ScholarPubMed
Read, C. P. (1951). The crowding effect in tapeworm infections. Journal of Parasitology 37, 174178.CrossRefGoogle ScholarPubMed
Roberts, L. S. (2000). The crowding effect revisited. Journal of Parasitology 86, 209211.Google ScholarPubMed
Rohde, K. (1991). Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60, 91104.CrossRefGoogle Scholar
Rzepecka, J., Lucius, R., Doligalska, M., Beck, S., Rausch, S. and Hartmann, S. (2006). Screening for immunomodulatory proteins of the intestinal parasitic nematode Heligmosomoides polygyrus. Parasite Immunology 28, 463472.CrossRefGoogle ScholarPubMed
Schad, G. A. (1963). Niche diversification in a parasitic species flock. Nature, London 198, 404406.CrossRefGoogle Scholar
Silver, B. B., Dick, T. A. and Welch, H. E. (1980). Concurrent infections of Hymenolepis diminuta and Trichinella spiralis in the rat intestine. Journal of Parasitology 66, 786791.CrossRefGoogle ScholarPubMed
Stadler, B. and Dixon, A. F. G. (2005). Ecology and evolution of aphid-ant interactions. Annual Reviews of Ecology and Systematics 36, 345372.CrossRefGoogle Scholar
Telfer, S., Begon, M., Bennett, M., Bown, K. J., Burthe, S., Lambin, X., Telford, G. and Birtles, R. (2007 a). Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology 134, 413425.CrossRefGoogle ScholarPubMed
Telfer, S., Clough, H. E., Birtles, R. J., Bennet, M., Carslake, D., Helyar, S. and Begon, M. (2007 b). Ecological differences and coexistence in a guild of microparasites: Bartonella in wild rodents. Ecology 88, 18411849.CrossRefGoogle Scholar
Tchuem Tchuenté, L.-A., Behnke, J. M., Gilbert, F. S., Southgate, V. R. and Vercruysse, J. (2003). Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine and International Health 8, 975986.CrossRefGoogle ScholarPubMed
Tokeshi, M. (1999). Species Coexistence: Ecological and Evolutionary Perspectives. Blackwell Science, Oxford.Google Scholar
Warren, M. and Wigglesworth, T. (2007). Large Blue. DEFRA factsheet from www.butterfly-conservation.org/conservation/defrafactsheets/butterflies.Google Scholar
Wilson, M. S., Taylor, M. D., Balic, A., Finney, C. A., Lamb, J. R. and Maizels, R. M. (2005). Suppression of allergic airway inflammation by helminth-induced regulatory T cells. Journal of Experimental Medicine 202, 11991212.CrossRefGoogle ScholarPubMed
Wootton, T. J. (1994). The nature and consequences of indirect effects in ecological communities. Annual Reviews of Ecology and Systematics 25, 443466.CrossRefGoogle Scholar