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Helminth species richness in wild wood mice, Apodemus sylvaticus, is enhanced by the presence of the intestinal nematode Heligmosomoides polygyrus

Published online by Cambridge University Press:  02 June 2009

J. M. BEHNKE ,
C. EIRA ,
M. ROGAN ,
F. S. GILBERT ,
J. TORRES ,
J. MIQUEL  and
J. W. LEWIS
J. M. BEHNKE*
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
C. EIRA
Affiliation:
CESAM and Department of Biology, University of Aveiro, Campus de Santiago 3810-193 Aveiro, Portugal
M. ROGAN
Affiliation:
Department of Biological Sciences, University of Salford, Salford M5 4WT, UK
F. S. GILBERT
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
J. TORRES
Affiliation:
Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av Joan XXIII, sn, 08028 Barcelona, Spain
J. MIQUEL
Affiliation:
Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av Joan XXIII, sn, 08028 Barcelona, Spain
J. W. LEWIS
Affiliation:
School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, UK
*
*Corresponding author: School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK. Tel: 0115 951 3208. Fax 0115 951 3251. E-mail: [email protected]
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Summary

We analysed 3 independently collected datasets of fully censused helminth burdens in wood mice, Apodemus sylvaticus, testing the a priori hypothesis of Behnke et al. (2005) that the presence of the intestinal nematode Heligmosomoides polygyrus predisposes wood mice to carrying other species of helminths. In Portugal, mice carrying H. polygyrus showed a higher prevalence of other helminths but the magnitude of the effect was seasonal. In Egham, mice with H. polygyrus showed a higher prevalence of other helminth species, not confounded by other factors. In Malham Tarn, mice carrying H. polygyrus were more likely to be infected with other species, but only among older mice. Allowing for other factors, heavy residual H. polygyrus infections carried more species of other helminths in both the Portugal and Egham data; species richness in Malham was too low to conduct a similar analysis, but as H. polygyrus worm burdens increased, so the prevalence of other helminths also increased. Our results support those of Behnke et al. (2005), providing firm evidence that at the level of species richness a highly predictable element of co-infections in wood mice has now been defined: infection with H. polygyrus has detectable consequences for the susceptibility of wood mice to other intestinal helminth species.

Keywords

Apodemus sylvaticusassociations of helminthsco-occurrence of helminthsHeligmosomoides polygyrushelminthshelminth species richnessinteractions between helminths
Type
Research Article
Information
Parasitology , Volume 136 , Issue 7 , June 2009 , pp. 793 - 804
Copyright
Copyright © Cambridge University Press 2009

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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, 93–100.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, 7–16.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 1–71.Google Scholar
Behnke, J. M. (2008). Structure in parasite component communities in wild rodents. Predictability, stability, associations and interactions …. or pure randomness? Parasitology 135, 751–766.CrossRefGoogle ScholarPubMed
Behnke, J. M., Bajer, A., Sinski, E. and Wakelin, D. (2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122, S39–S49.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, 861–907.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, 31–44.Google Scholar
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, 982–993.Google Scholar
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, 151–157.Google Scholar
Bottomley, C., Isham, V. and Basáñez, M.-G. (2005). Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 131, 417–433.CrossRefGoogle ScholarPubMed
Buck, A. A., Anderson, R. I. and MacRae, A. A. (1978 a). Epidemiology of poly-parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities in Chad, Peru, Afghanistan and Zaire. Tropenmedizin und Parasitologie 29, 61–70.Google ScholarPubMed
Buck, A. A., Anderson, R. I. and MacRae, A. A. (1978 b). Epidemiology of poly-parasitism. II. Types of combinations, relative frequency and associations of multiple infections. Tropenmedizin und Parasitologie 29, 137–144.Google Scholar
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, 87–410.Google Scholar
Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317–347.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, 359–362.Google Scholar
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, 300–308.Google Scholar
Elton, C., Ford, E. B., Baker, J. R. and Gardiner, A. D. (1931). The health and parasites of a wild mouse population. Proceedings of the Zoological Society of London 1931, 657–721.CrossRefGoogle Scholar
Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88–94.Google Scholar
Gortázar, C., Ferroglio, E., Höfle, U., Frölich, K. and Vicente, J. (2007). Diseases shared between wildlife and livestock: a European perspective. European Journal of Wildlife Research 53, 241–256.Google Scholar
Graham, A. L. (2002). When T-helper cells don't help: immunopathology during concomitant infections. The Quarterly Review of Biology 77, 409–434.CrossRefGoogle Scholar
Graham, A. L. (2008). Ecological rules governing helminth-microparasite coinfection. Proceedings of the National Academy of Sciences, USA 105, 566–570.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, 284–291.Google Scholar
Gregory, R. D., Keymer, A. E. and Clarke, J. R. (1990). Genetics, sex and exposure: the ecology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 59, 363–378.CrossRefGoogle Scholar
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, 221–229.Google Scholar
Haukisalmi, V. and Henttonen, H. (1998). Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia 116, 565–574.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, 275–285.CrossRefGoogle ScholarPubMed
Hominick, W. M. and Aston, A. J. (1981). Association between Pelodera strongyloides (Nematoda: Rhabditidae) and wood mice, Apodemus sylvaticus. Parasitology 83, 67–75.Google Scholar
Howard, S. C., Donnelly, C. A. and Chan, M.-S. (2001). Methods for estimation of associations between multiple species parasite infections. Parasitology 122, 233–251.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, 141–149.CrossRefGoogle ScholarPubMed
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Janovy, J. Jr. (2002). Concurrent infections and the community ecology of helminth parasites. Journal of Parasitology 88, 440–445.CrossRefGoogle ScholarPubMed
Janovy, J. Jr., Clopton, R. E., Clopton, D. A., Snyder, S. D., Efting, A. and Krebs, L. (1995). Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecological Modelling 77, 189–196.Google Scholar
Jolles, A. E., Ezenwa, V. O., Etienne, R. S., Turner, W. C. and Olff, H. (2008). Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89, 2239–2250.Google Scholar
Keusch, G. T. and Migasena, P. (1982). Biological implications of polyparasitism. Reviews of Infectious Diseases 4, 880–882.Google Scholar
Kisielewska, K. (1970). 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, 197–208.Google Scholar
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, London 428, 840–844.CrossRefGoogle ScholarPubMed
Lotz, J. M. and Font, W. F. (1994). Excess positive associations of communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398–413.Google Scholar
Monroy, F. G. and Enriquez, F. J. (1992). Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 49–54.CrossRefGoogle Scholar
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, 225–242.CrossRefGoogle ScholarPubMed
Pedersen, A. B. and Fenton, A. (2006). Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.Google Scholar
Pedersen, A. B. and Greives, T. J. (2008). The interaction of parasites and resources causes crashes in wild mouse population. Journal of Animal Ecology 77, 70–377.CrossRefGoogle ScholarPubMed
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3–S11.Google Scholar
Rogan, M. T., Craig, P. S., Hide, G., Heath, S., Pickles, A. and Storey, D. M. (2007). The occurrence of the trematode Plagiorchis muris in the wood mouse Apodemus sylvaticus in North Yorshire, UK. Journal of Helminthology 81, 57–62.CrossRefGoogle Scholar
Rohlf, F. J. and Sokal, R. R. (1995). Statistical Tables. W. H. Freeman and Company, San Francisco, CA, USA.Google Scholar
Suttle, K. B., Thomsen, M. A. and Power, M. E. (2007). Species interactions reverse grassland response to changing climate. Science 315, 640–642.CrossRefGoogle ScholarPubMed
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, 975–986.Google Scholar
Venables, W. N. and Ripley, B. D. (1997). Modern Applied Statistics with S-Plus. Springer, New York, USA.CrossRefGoogle Scholar
Vignon, M., Sasal, P. and Galzin, R. (2009). Host introduction and parasites: a case study on the parasite community of the peacock grouper Cephalopholis argus (Serranidae) in the Hawaiian Islands. Parasitology Research 104, 775–782.CrossRefGoogle ScholarPubMed