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Local variation in endoparasite intensities of bank voles (Clethrionomys glareolus) from ecologically similar sites: morphometric and endocrine correlates

Published online by Cambridge University Press:  12 April 2024

C.J. Barnard*
Affiliation:
Animal Behaviour and Ecology Research Group
J.M. Behnke
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
A. Bajer
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
D. Bray
Affiliation:
Animal Behaviour Group, Department of Veterinary Clinical Science and Animal Husbandry, University of Liverpool, Leahurst, Neston, CH64 7TE, UK
T. Race
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
K. Frake
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
J. Osmond
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
J. Dinmore
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
E. Sinski
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
*
*Fax: +44 (0) 115 9513251 E-mail: [email protected]
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Abstract

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Much interest has centred recently on the role of adaptive trade-offs between the immune system and other components of life history in determining resistance and parasite intensities among hosts. Steroid hormones, particularly glucocorticoids and sex steroids, provide a plausible mechanism for mediating such trade-offs. A basic assumption behind the hypothesis, however, is that steroid activity will generally correlate with reduced resistance and thus greater parasite intensities. Here, we present some findings from a field study of bank voles (Clethrionomys glareolus) in which we have looked at associations between parasite intensities, anatomical and morphometric measures relating to endocrine function and life history variation in three local populations inhabiting similar but mutually isolated woodland habitats. In general, sites with greater parasite intensities were those in which male C. glareolus had significantly larger adrenal glands, testes and seminal vesicles for their age and body size. Females also showed a site difference in adrenal gland weight. Some aspects of site-related parasite intensity were associated with asymmetry in adrenal gland weight and hind foot length, which may have reflected developmental effects on glucocorticoid activity.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2002

References

Abramov, V.V., Karmatskikh, O.L., Kozlov, V.A. & Oskina, I.N. (1996) Functional asymmetry of adrenal glands in CBA×C57BL/6 F-1 mice. Doklady Akademii Nauk 347, 831833.Google Scholar
Alexander, J. & Stimson, W.H. (1988) Sex hormones and the course of parasitic infection. Parasitology Today 4, 189193.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, 373398.CrossRefGoogle ScholarPubMed
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219247.CrossRefGoogle Scholar
Anderson, R.M. & May, R.M. (1991) Infectious diseases of humans: dynamics and control. Oxford University Press CrossRefGoogle Scholar
Bajer, A., Pawelczyk, A., Behnke, J.M., Gilbert, F.S. & Sinski, E. (2001) Factors affecting the component community structure of haemoparasites in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 122, 4354.CrossRefGoogle ScholarPubMed
Barnard, C.J. & Behnke, J.M. (2001) From psychoneuroimmunology to ecological immunology: life history strategies and immunity trade-offs. pp. 3547 in Ader, R., Felten, D. & Cohen, N. (Eds) Psychoneuroimmunology, 3rd edn. San Diego, Academic Press.Google Scholar
Barnard, C.J., Behnke, J.M. & Sewell, J. (1993) Social behaviour, stress and susceptibility to infection in house mice (Mus musculus): effects of duration of grouping and aggressive behaviour prior to infection on susceptibility to Babesia microti . Parasitology 107, 183192.CrossRefGoogle ScholarPubMed
Barnard, C.J., Behnke, J.M. & Sewell, J. (1994) Social behaviour and susceptibility to infection in house mice (Mus musculus): effects of group size, aggressive behaviour and status-related hormonal responses prior to infection on resistance to Babesia microti . Parasitology 108, 487496.CrossRefGoogle ScholarPubMed
Barnard, C.J., Behnke, J.M. & Sewell, J. (1996a) Social status and resistance to disease in house mice (Mus musculus): status-related modulation of hormonal responses in relation to immunity costs in different social and physical environments. Ethology 102, 6384.CrossRefGoogle Scholar
Barnard, C.J., Behnke, J.M. & Sewell, J. (1996b) Environmental enrichment, immunocompetence and resistance to Babesia microti in male laboratory mice. Physiology and Behaviour 60, 12231231.CrossRefGoogle Scholar
Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. & Smithurst, P.R. (1997a) Modulation of behaviour and testosterone concentration in immunodepressed male laboratory mice (Mus musculus). Physiology and Behaviour 61, 907917.CrossRefGoogle ScholarPubMed
Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. & Smithurst, P.R. (1997b) Immunity costs and behavioural modulation in male laboratory mice (Mus musculus) exposed to the odour of females. Physiology and Behaviour 62, 857866.CrossRefGoogle Scholar
Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. & Smithurst, P.R. (1998) Maternal effects on the development of social rank and immunity trade-offs in male laboratory mice (Mus musculus). Proceedings of the Royal Society of London Series B 265, 20872093.CrossRefGoogle ScholarPubMed
Beckage, N.E. (Ed.) (1997) Parasites and pathogens: effects on host hormones and behavior. New York, Chapman and Hall.CrossRefGoogle Scholar
Behnke, J.M., Barnard, C.J., Bajer, A., Bray, D., Dinmore, J., Frake, K., Osmond, J., Race, T. & Sinski, 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
Borkowska, A. (1999) Genetic and morphological variation among populations of the bank vole Clethrionomys glareolus from north-eastern Poland: the seasonal aspect. Zeitschrift für Saugetierkunde 64, 285297.Google Scholar
Crofton, H.D. (1971) A quantitative approach to parasitism. Parasitology 62, 179193.CrossRefGoogle Scholar
Davies, I.B. (1997) The effects of hormone treatment on social status-related differences in infection with Babesia microti in adult male CFLP mice. Unpublished PhD thesis, University of Nottingham.Google Scholar
Desai, K.V. & Kondaiah, P. (2000) Androgen ablation results in differential regulation of transforming growth factor beta isoforms in rat male accessory sex organs and epididymis. Journal of Molecular Endocrinology 24, 253260.CrossRefGoogle ScholarPubMed
Drickamer, L.C., Saal, F.S. vom, Marriner, L.M. & Mossman, C.A. (1995) Anogenital distance and dominance status in male house mice (Mus domesticus). Aggressive Behaviour 21, 301309.3.0.CO;2-1>CrossRefGoogle Scholar
Escutenaire, S., Chalon, P., Verhagen, R., Heyman, P., Thomas, I., Karelle-Bui, L., Avsic-Zupanc, T., Lundkvist, A., Plyusnin, A. & Pastoret, P.P. (2000) Spatial and temporal dynamics of Puumala hantavirus in red bank vole (Clethrionomys glareolus) populations in Belgium. Virus Research 67, 91107.CrossRefGoogle ScholarPubMed
Folstad, I. & Karter, A.J. (1992) Parasites, bright males and the immunocompetence handicap. American Naturalist 139, 603622.CrossRefGoogle Scholar
Fukazawa, Y. & Iguchi, T. (1999) Effects of hormones and growth factors on the development of the male mouse reproductive tract in vitro. Zoological Science 16, 153160.CrossRefGoogle Scholar
Gerendai, I. & Halasz, B. (1997) Neuroendocrine asymmetry. Frontiers in Neuroendocrinology 18, 354381.CrossRefGoogle ScholarPubMed
Gerlach, G. & Musolf, K. (2000) Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology 14, 10661074.CrossRefGoogle Scholar
Gregory, R.D. & Woolhouse, M.E.J. (1993) Quantification of parasite aggregation: a simulation study. Acta Tropica 54, 131139.CrossRefGoogle ScholarPubMed
Grossman, C.J. (1985) Interactions between the gonadal steroids and the immune system. Science 227, 257261.CrossRefGoogle ScholarPubMed
Harder, A., Danneschewski, A. & Wunderlich, F. (1994) Genes of the mouse H-2 complex control the efficacy of testosterone to suppress immunity against the intestinal nematode Heterakis spumosa . Parasitology Research 80, 446448.CrossRefGoogle ScholarPubMed
Hartvigsen, R. & Kennedy, C.R. (1993) Patterns in the composition and richness of helminth communities in brown trout, Salmo trutta, in a group of reservoirs. Journal of Fish Biology 43, 603615.CrossRefGoogle Scholar
Haukisalmi, V. & Henttonen, H. (1999) Determinants of helminth aggregation in natural host populations: individual differences or spatial heterogeneity? Ecography 22, 629636.Google Scholar
Hazel, S.M., Bennett, M., Chantrey, J., Bown, K., Cavanagh, R., Jones, T.R., Baxby, D. & 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
Henriksen, S. & Pohlenz, J. (1981) Staining of cyptosporidia by modified Ziehl-Neelsen technique. Acta Veterinaria Scandinavica 22, 594596.CrossRefGoogle ScholarPubMed
Hillgarth, N. & Wingfield, J.C. (1997) Testosterone and immunosuppression in vertebrates: implications for parasite-mediated sexual selection. pp. 143155 in Beckage, N.E. (Ed.) Parasites and pathogens; effects on host hormones and behavior. London, Chapman and Hall.Google Scholar
Jarred, R.A., Cancilla, B., Prins, G.S., Thayer, K.A., Cunha, G.R. & Ridbridger, G.P. (2000) Evidence that estrogens directly alter androgen-regulated prostate development. Endocrinology 141, 34713477.CrossRefGoogle ScholarPubMed
Kennedy, C.R., Hartvigsen, R. & Halvorsen, O. (1991) The importance of fish stocking in the dissemination of parasites throughout a group of reservoirs. Journal of Fish Biology 38, 541552.CrossRefGoogle Scholar
Klein, S.L. (2000) Hormones and mating system affect sex and species differences in immune function among vertebrates. Behavioural Processes 51, 149166.CrossRefGoogle ScholarPubMed
Kozakiewicz, M. (1976) The weight of the eye lens as a proposed age indicator of the bank vole. Acta Theriologia 21, 314316.CrossRefGoogle Scholar
Maier, S.F. & Watkins, L.R. (1999) Bidirectional communications between the brain and the immune system: implications for behaviour. Animal Behaviour 57, 741751.CrossRefGoogle Scholar
Maier, S.F., Watkins, L.R. & Fleshner, M. (1994) Psychoneuroimmunology: the interface between behavior, brain and immunology. American Psychologist 49, 10041017.CrossRefGoogle Scholar
Møller, A.P. & Swaddle, J. (1997) Asymmetry, developmental stability and evolution. Oxford, Oxford University Press.CrossRefGoogle Scholar
Morris, P. (1972) A review of mammalian age determination methods. Mammal Review 2, 69104.CrossRefGoogle Scholar
Nunn, C.L., Gittelman, J.L. & Antonovics, J. (2000) Promiscuity and the primate immune system. Science 290, 11681170.CrossRefGoogle ScholarPubMed
Palanza, P., Parmigiani, S. & Saal, F.S. vom (1995) Urine marking and maternal aggression of wild female mice in relation to anogenital distance at birth. Physiology and Behaviour 58, 827835.CrossRefGoogle ScholarPubMed
Palmer, A.R. & Strobeck, C. (1986) Fluctuating asymmetry: measurement, analysis, pattern. Annual Review of Ecology and Systematics 17, 391421.CrossRefGoogle Scholar
Pawelczyk, A. & Sinski, E. (2000) Prevalence of IgG antibodies response to Borrelia burgdorferi in populations of wild rodents from the Mazury Lake District region of Poland. Annals of Agricultural and Environmental Medicine 7, 7983.Google ScholarPubMed
Poiani, A., Goldsmith, A.R. & Evans, M.R. (2000) Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis. Behavioural Ecology and Sociobiology 47, 230242.CrossRefGoogle Scholar
Quinnell, R.J. & Keymer, A.E. (1990) Acquired immunity and epidemiology. pp. 317343 in Behnke, J.M. (Ed.) Parasites: immunity and pathology. London, Taylor and Francis.Google Scholar
Ros, A.F.G., Groothuis, T.G.G. & Apanius, V. (1997) The relation among gonadal steroids, immunocompetence, body mass and behavior in young black headed gulls (Larus ridibundus). American Naturalist 150, 201219.CrossRefGoogle ScholarPubMed
Saino, N., Canova, L., Fasola, M. & Martinelli, R. (2000) Reproduction and population density affect humoral immunity in bank voles under field experimental conditions. Oecologia 124, 358366.CrossRefGoogle ScholarPubMed
Shaw, D.J. & Dobson, A.P. (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology (Suppl.) 111, S111S133.CrossRefGoogle ScholarPubMed
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317321.CrossRefGoogle ScholarPubMed
Sire, C., Langland, J., Barral, V. & Théron, A. (2001) Parasite (Schistosoma mansoni) and host (Biomphalaria glabrata) genetic diversity: population structure in a fragmented landscape. Parasitology 122, 545554.CrossRefGoogle Scholar
Stearns, S.C. & Koella, J. (1986) The evolution of phenotypic plasticity in life-history traits: predictions for norms of reaction for age- and size-at-maturity. Evolution 40, 893913.Google ScholarPubMed
Szigethy, E., Conwell, Y., Forbes, N.T., Cox, C. & Caine, E.D. (1994) Adrenal weight and morphology in victims of completed suicide. Biological Psychology 36, 374380.Google ScholarPubMed
Tahka, K.M., Zhuang, Y.H., Tahka, S. & Tuohimaa, P. (1997) Photoperiod-induced changes in androgen receptor expression in testes and accessory sex glands of the bank vole, Clethrionomys glareolus . Biology of Reproduction 56, 898908.CrossRefGoogle ScholarPubMed
Valen, L. van, (1962) A study of fluctuating asymmetry. Evolution 16, 125142.CrossRefGoogle Scholar
Wakelin, D. & Blackwell, J.M. (1993) Genetic variation in immunity to parasitic infections. pp. 322 in Warren, K.S. (Ed.) Immunology and molecular biology of parasitic infections. Boston, Blackwell Scientific Publications.Google Scholar
Wedekind, C. & Folstad, I. (1994) Adaptive or nonadaptive immunosuppression by sex hormones? American Naturalist 143, 936938.CrossRefGoogle Scholar
Wilckens, T. & Rijk, R. de (1997) Glucocorticoids and immune function: unknown dimensions and new frontiers. Immunology Today 18, 418424.CrossRefGoogle ScholarPubMed