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The influence of climatic conditions on long-term changes in the helminth fauna of terrestrial molluscs and the implications for parasite transmission in southern England

Published online by Cambridge University Press:  01 December 2008

N.J. Morley  and
J.W. Lewis
N.J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
J.W. Lewis
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
*
*E-mail: [email protected]
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Abstract

The influence of climatic conditions on the prevalence and transmission of helminth parasites in a terrestrial mollusc population was studied in a grassland site in southern England between 1974 and 1983. Molluscs were sampled in each September of 5 years over this period (1974, 1976, 1979, 1981, 1983). Climatic conditions had a variable effect on parasite prevalence. Trematode sporocyst infections increased after wet summer and warm winter conditions and declined in hot, dry periods. Cestode infections increased after combined wet spring and summer weather and low winter temperatures, although trematode metacercariae and nematode infections were less likely to be influenced by climate. The effects on parasite transmission were undertaken by comparing parasite prevalences in the principal definitive hosts, the common shrew (Sorex araneus) and the wood mouse (Apodemus sylvaticus) in the same habitat over the period 1973–1983. Changes in parasite prevalences in the molluscan population were rarely replicated by changes in the small mammal population, except for trematode parasites in small mammals during a period of severe drought in 1976. These results suggest that only long-term persistent modifications in climate are likely to affect host–parasite dynamics.

Type
Research Papers
Information
Journal of Helminthology , Volume 82 , Issue 4 , December 2008 , pp. 325 - 335
Copyright
Copyright © Cambridge University Press 2008

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References

Abdou, A.H. (1958) Studies on the development of Davainea proglottina in the intermediate host. Journal of Parasitology 44, 484–488.CrossRefGoogle ScholarPubMed
Badger, L.I. & Oyerinde, J.P.O. (1996) Schistosoma mansoni: effect of aestivation on the intra-molluscan stages and the survival rate of infected Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 90, 617–620.CrossRefGoogle ScholarPubMed
Bailey, S.E.R. (1975) The seasonal and daily patterns of locomotor activity in the snail Helix aspersa Muller, and their relation to environmental variables. Proceedings of the Malacological Society of London 41, 415–428.Google Scholar
Browne, T.J. & Robinson, D.A. (1984) Exceptional rainfall around Lewes and the South Downs, Autumn 1982. Weather 39, 132–136.CrossRefGoogle Scholar
Burt, S.D. (1980) Snowfall in Britain during winter 1978/79. Weather 35, 288–301.CrossRefGoogle Scholar
Butcher, A.R. & Grove, D.I. (2003) Field prevalence and laboratory susceptibility of southern Australian land snails to Brachylaima cribbi sporocyst infection. Parasite 10, 119–125.CrossRefGoogle ScholarPubMed
Butcher, A.R. & Grove, D.I. (2005a) Second intermediate host land snails and definitive host animals of Brachylaima cribbi in southern Australia. Parasite 12, 31–37.CrossRefGoogle ScholarPubMed
Butcher, A.R. & Grove, D.I. (2005b) Seasonal variation in rates of sporocyst and metacercarial infection by Brachylaima cribbi in helicid and hygromiid land snails on the Yorke Peninsula, South Australia. Australian Journal of Zoology 53, 375–382.CrossRefGoogle Scholar
Cain, A.J. (1983) Ecology and ecogenetics of terrestrial molluscan populations. pp. 597–648in Russell-Hunter, W.D. (Ed.) The Mollusca, vol. 6 (Ecology). London, Academic Press.Google Scholar
Cameron, R.A.D. (1982) Life histories, density and biomass in a woodland snail community. Journal of Molluscan Studies 48, 159–166.Google Scholar
Cameron, R.A.D. & Redfern, M. (1976) British land snails. Synopses of the British fauna (new series), No. 6. Linnean Society of London. London, Academic Press.Google Scholar
Cattadori, I.M., Haukisalmi, V., Henttonen, H. & Hudson, P.J. (2006) Transmission ecology and the structure of parasite communities in small mammals. pp. 349–369in Morand, S., Krasnov, B.R. & Poulin, R. (Eds) Micromammals and macroparasites. Berlin, Springer.CrossRefGoogle Scholar
Chatfield, J.E. (1976) Studies on food and feeding in some European land molluscs. Journal of Conchology 29, 5–20.Google Scholar
Churchfield, S., Hollier, J. & Brown, V.K. (1991) The effects of small mammal predators on grassland invertebrates, investigated by field exclosure experiment. Oikos 60, 283–290.CrossRefGoogle Scholar
Churchfield, S., Hollier, J. & Brown, V.K. (1995) Population dynamics and survivorship patterns in the common shrew Sorex araneus in southern England. Acta Theriologica 40, 53–68.CrossRefGoogle Scholar
Collins, M.B. (1981) Sediment yield studies of headwater catchments in Sussex, SE England. Earth Surface Processes and Landforms 6, 517–539.CrossRefGoogle Scholar
Corbet, G.B. & Harris, S. (1991) The handbook of British mammals. Oxford, Blackwell Scientific Press.Google Scholar
Cragg, J.B., Foster, R. & Vincent, M. (1957) Larval trematodes (Brachylaemidae) from the slugs Milax sowerbii (Ferussac), Agriolimax reticulatus (Muller) and Arion lusitanicus Mabille. Parasitology 47, 396–404.CrossRefGoogle ScholarPubMed
Davies, P. & Snow, D.W. (1965) Territory and food of the song thrush. British Birds 58, 161–175.Google Scholar
Doornkamp, J.C. & Gregory, K.J. (eds) (1980) Atlas of drought in Britain 1975–76. London, Institute of British Geographers.Google Scholar
Foster, R. (1958a) Infestation of the slugs Milax sowerbii Ferussac and Agriolimax reticulatus Muller by trematode metacercariae (Brachylaemidae). Parasitology 48, 303–311.CrossRefGoogle Scholar
Foster, R. (1958b) The effects of trematode metacercariae (Brachylaemidae) on the slugs Milax sowerbii Ferussac and Agriolimax reticulatus Muller. Parasitology 48, 261–268.CrossRefGoogle ScholarPubMed
Gemmell, M.A. (1978) The effects of weather on tapeworm eggs and its epidemiological implications. World Meteorological Organization Technical Note (Weather & Parasitic Animal Diseases) 159, 83–94.Google Scholar
Graham, E.G., Harris, T.J. & Ollerenshaw, C.B. (1984) Some observations on the epidemiology of Nematodirus battus in Anglesey. Agricultural and Forest Meteorology 32, 121–132.CrossRefGoogle Scholar
Hapca, S., Crawford, J., Rae, R., Wilson, M. & Young, I. (2007) Movement of the parasitic nematode Phasmarhabditis hermaphrodita in the presence of mucus from the host slug Deroceras reticulatum. Biological Control 41, 223–229.CrossRefGoogle Scholar
Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S. & Samuel, M.D. (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.CrossRefGoogle ScholarPubMed
Haukisalmi, V. & Henttonen, H. (1990) The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia 83, 309–315.CrossRefGoogle ScholarPubMed
Jenkins, E.J., Veitch, A.M., Kutz, S.J., Hoberg, E.P. & Polley, L. (2006) Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep (Ovis d. dalli). Parasitology 132, 387–401.CrossRefGoogle ScholarPubMed
Jourdane, J. (1972) Étude expérimentale du cycle biologique de deux espèces de Choanotaenia intestinaux des Soricidae. Zeitschrift der Parasitenkunde 38, 333–343.CrossRefGoogle Scholar
Kisielewska, K. (1961) Circulation of tapeworms of Sorex araneus araneus L. in biocenosis in Bialowieza National Park. Acta Parasitologica Polonoca 9, 331–369.Google Scholar
Kisielewska, K. (1964) Changes in the structure of cestodofauna of Sorex araneus araneus L. from the Bialowieza National Park due to climatic conditions in 1960. Acta Parasitologica Polonica 12, 33–46.Google Scholar
Krull, W.H. (1935) Some observations on the life history of Brachylaemus virginiana (Dickerson) Krull (Trematoda: Brachylaimidae). Transactions of the American Microscopical Society 54, 118–134.CrossRefGoogle Scholar
Lewis, J.W. (1968) Studies on the helminth parasites of voles and shrews from Wales. Journal of Zoology 154, 313–331.CrossRefGoogle Scholar
Lewis, J.W. (1969) Studies on the life history of Brachylaimus oesophagei Shaldybin, 1953 (Digenea: Brachylaimidae). Journal of Helminthology 63, 79–98.CrossRefGoogle Scholar
Manga-Gonzalez, M.Y., Gonzalez-Lanza, C., Cabanas, E. & Campo, R. (2001) Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum. Parasitology 123, S91–S114.CrossRefGoogle Scholar
Morand, S., Wilson, M.J. & Glen, D.M. (2004) Nematodes (Nematoda) parasitic in Terrestrial Gastropods. pp. 525–557in Baker, G.M. (Ed.) Natural enemies of terrestrial molluscs. Wallingford, CAB International.CrossRefGoogle Scholar
Morley, N.J. & Lewis, J.W. (2004) Free living endohelminths: the influence of multiple factors. Trends in Parasitology 20, 114–115.CrossRefGoogle ScholarPubMed
Ollerenshaw, C.B. (1966) The approach to forecasting the incidence of Fascioliasis over England and Wales 1958–1962. Agricultural Meteorology 3, 35–53.CrossRefGoogle Scholar
Ollerenshaw, C.B. (1970) Some aspects of the epidemiology of Fascioliasis in Britain. Proceedings of the Malacological Society 39, 238–243.Google Scholar
Ollerenshaw, C.B. (1983) Present and past trends of the weather over England and Wales in relation to Fascioliasis. Proceedings of Meetings of the Sheep Veterinary Society 7, 63–65.Google Scholar
Ollerenshaw, C.B. & Smith, L.P. (1969) Meteorological factors and forecasts of helminthic disease. Advances in Parasitology 7, 283–323.CrossRefGoogle ScholarPubMed
Pietrock, M. & Marcogliese, D.J. (2003) Free-living endohelminths: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.CrossRefGoogle ScholarPubMed
Pojmanska, T. (1961) Investigations on the occurrence and biology of trematodes of Sorex araneus araneus L. in Bialowieza National Park. Acta Parasitologica Polonica 9, 305–330.Google Scholar
Ratcliffe, R.A.S. (1983) July 1983 – the hottest for 324 years? Weather 38, 291–292.CrossRefGoogle Scholar
Reiczigel, J. & Rozsa, L. (2001) Quantitative parasitology 2.0 Budapest. Distributed by the authors.Google Scholar
Rogan, M.T., Craig, P.S., Hide, G., Heath, S., Pickles, A. & Storey, D.M. (2007) The occurrence of the trematode Plagiorchis muris in the wood mouse Apodemus sylvaticus in North Yorkshire, UK. Journal of Helminthology 81, 57–62.CrossRefGoogle ScholarPubMed
Rose, J.H. (1957) Observations on the bionomics of the free-living first stage larvae of the sheep lungworm, Muellerius capillaris. Journal of Helminthology 31, 17–28.CrossRefGoogle Scholar
Schuster, R. (1993) Infection patterns in the first intermediate host of Dicrocoelium dendriticum. Veterinary Parasitology 47, 235–243.CrossRefGoogle ScholarPubMed
Smith, G. & Wilson, R.A. (1980) Seasonal variations in the microclimate of Lymnaea truncatula habitats. Journal of Animal Ecology 17, 329–342.Google Scholar
Solomon, A., Paperna, I. & Markovics, A. (1996) The influence of aestivation in land snails on the larval development of Muellerius cf. capillaris (Metastrongyloidea: Protostrongylidae). International Journal for Parasitology 26, 363–367.CrossRefGoogle ScholarPubMed
Sternberg, M. (2000) Terrestrial gastropods and experimental climate change: a field study in a calcareous grassland. Ecological Research 15, 73–81.CrossRefGoogle Scholar
Svadzhyan, P.K. (1953) [Dynamics of infestation of terrestrial molluscs of Armenian S.S.R. by parthenogenetic stages of Dicrocoelium lanceatum and factors influencing the emergence of multiple cysts]. pp. 642–648in Petrov, A.M. (Ed.) Contributions to Helminthology Published to Commemorate the 75th birthday of K.I. Skrjabin (in Russian). English translation: Israel programme for Scientific Translations, Jerusalem, 1966.Google Scholar
Wiktorowa, J. (1972) [A contribution to a better knowledge of Helminthofauna in Terrestrial Molluscs]. Wiadomosci Parazytologiczne 18, 101–111(in Polish).Google Scholar
Williams, D.W. (1942) Studies on the biology of the larva of the nematode lungworm, Muellerius capillaris, in molluscs. Journal of Animal Ecology 11, 1–8.CrossRefGoogle Scholar
Wilson, R.A., Smith, G. & Thomas, M.R. (1982) Facioliasis. pp. 262–361in Anderson, R.M. (Ed.) The population dynamics of infectious diseases: theory and applications. London, Chapman & Hall.CrossRefGoogle Scholar
Wood, P.A. (1977) Controls of variation in suspended sediment concentration in the River Rother, West Sussex, England. Sedimentology 24, 437–445.CrossRefGoogle Scholar
Wood, P.A. (1978) Fine-sediment mineralogy of source rocks and suspended sediment, Rother catchment, West Sussex. Earth Surface Processes and Landforms 3, 255–263.CrossRefGoogle Scholar
Wood, N.L.H. (1979) The warm dry autumn of 1978 in southern Britain. Weather 34, 188–190.CrossRefGoogle Scholar
Wright, P.B. (1975) Four mild winters – in Europe. Weather 30, 125–126.CrossRefGoogle Scholar