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Local variation in helminth burdens of bank voles (Clethrionomys glareolus) from ecologically similar sites: temporal stability and relationships with hormone concentrations and social behaviour

Published online by Cambridge University Press:  12 April 2024

C.J. Barnard ,
K. Kulis ,
J.M. Behnke ,
A. Bajer ,
J. Gromadzka-Ostrowska ,
M. Stachon  and
E. Sinski
C.J. Barnard*
Affiliation:
Animal Behaviour and Ecology Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
K. Kulis
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
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
J. Gromadzka-Ostrowska
Affiliation:
Department of Dietetics and Functional Foods, Faculty of Human Nutrition and Consumer Services, Warszawa Agricultural University, Nowoursynowska 166, 02-787 Warszawa, Poland
M. Stachon
Affiliation:
Department of Dietetics and Functional Foods, Faculty of Human Nutrition and Consumer Services, Warszawa Agricultural University, Nowoursynowska 166, 02-787 Warszawa, Poland
E. Sinski
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
*
*Fax: (++44) 115 9513251 E-mail: [email protected]
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Abstract

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Populations of bank voles (Clethrionomys glareolus) in a fragmented forest habitat in north-east Poland showed local differences in helminth infection intensity, morphometric measures and organ weights that were consistent with differences at the same locations two years previously. Although overall intensities of infection were lower than previously, and there were some differences in the relative intensities of individual helminth species, site differences remained significant and were consistent across replicated subsites. In keeping with site differences in helminth infection and adrenal gland weight and asymmetry, voles at site 1 (high intensity infection) had higher circulating concentrations of corticosterone than those at site 2 (low intensity infection). Since males were sampled outside the breeding season, and thus non-scrotal, testosterone levels were low and did not differ between sites. As previously, voles at site 1 also showed greater hind foot asymmetry. Dyadic interactions between males from the same and different sites in the laboratory showed that males from site 1 were significantly less aggressive, especially when confronted with intruder males from site 2. There was no relationship between aggressiveness and intensity of infection overall or at site 1, but a significant negative relationship emerged at site 2. Aggression thus appeared to be downregulated at the higher intensity site independently of individual levels of infection. Terminal corticosterone concentrations were greater at site 1 and lower among residents that initiated more aggression. While corticosterone concentrations rose over the period of testing, they did not correlate with the amount of aggression initiated or received.

Type
Review Article
Information
Journal of Helminthology , Volume 77 , Issue 3 , September 2003 , pp. 185 - 195
Copyright
Copyright © Cambridge University Press 2003

References

Abramov, V.V., Karmatskikh, O.L., Kozlov, V.A. & Oskina, I.N. (1996) Functional asymmetry of adrenal glands in CBAxC57BL/6 F-1 mice. Doklady Akademii Nauk 347, 831–833.Google Scholar
Alexander, J. & Stimson, W.H. (1988) Sex hormones and the course of parasitic infection. Parasitology Today 4, 189–193.CrossRefGoogle Scholar
Alibhai, S.K. & Gipps, J.H. (1985) The population dynamics of bank voles.pp 120–134 in Flowerdew, J.R., Gurnell, J. & Gipps, J.H..(Eds) The ecology of woodland rodents: bank voles and wood mice.Oxford: Clarendon Press.Google 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, 373–398.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, 219–247.CrossRefGoogle Scholar
Anderson, R.M. & May, R.M. (1991) Infectious diseases of humans: dynamics and control. pp Oxford: 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, 43–54.CrossRefGoogle ScholarPubMed
Barnard, C.J. & Behnke, J.M. (2001) From psychoneuroimmunology to ecological immunology: life history strategies and immunity trade-offs.pp 35–47 in Ader, R., Felten, D. and 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 toBabesia microti . Parasitology 107, 183–192.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 toBabesia microti . Parasitology 108, 487–496.CrossRefGoogle ScholarPubMed
Barnard, C.J., Behnke, J.M. & Sewell, J. (1996) 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, 63–84.CrossRefGoogle Scholar
Barnard, C.J., Behnke, J.M. & Sewell, J. (1996) Environmental enrichment, immunocompetence and resistance toBabesia microti in male laboratory mice. Physiology and Behaviour 60, 1223–1231.CrossRefGoogle Scholar
Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. & Smithurst, P.R. (1997) Modulation of behaviour and testosterone concentration in immunodepressed male laboratory mice (Mus musculus). Physiology and Behaviour 61, 907–917.CrossRefGoogle ScholarPubMed
Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. & Smithurst, P.R. (1997) Immunity costs and behavioural modulation in male laboratory mice (Mus musculus) exposed to the odour of females. Physiology and Behaviour 62, 857–866.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, 2087–2093.CrossRefGoogle ScholarPubMed
Barnard, C.J., Behnke, J.M., Bajer, A., Bray, D., Race, T., Frake, K., Osmond, J., Dinmore, J. & Sinski, E. (2002) Local variation in endoparasite burdens of bank voles (Clethrionomys glareolus) from ecologically similar sites: morphometric and endocrine correlates. Journal of Helminthology 76, 103–112.CrossRefGoogle Scholar
Barnard, C.J., Sayed, E., Barnard, L.E., Behnke, J.M., Abdel Nabi, I., Sherif, N., Shutt, A. & Zalat, S. (2003) Local variation in helminth burdens of Egyptian spiny mice (Acomys cahirinus dimidiatus) from ecologically similar sites: relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 197–207.CrossRefGoogle ScholarPubMed
Behnke, J.M., Barnard, C.J., Mason, N., Harris, P.D., Sherif, N.E., Zalat, S. & Gilbert, F.S. (2000) Intestinal helminths of spiny mice (Acomys cahirinus dimidiatus) from St Katherine's Protectorate in the Sinai, Egypt. Journal of Helminthology 74, 31–43.CrossRefGoogle ScholarPubMed
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, 401–414.CrossRefGoogle ScholarPubMed
Borkowska, A. (1999) Genetic and morphological variation among populations of the bank voleClethrionomys glareolus from north-eastern Poland: the seasonal aspect. Zeitschrift für Saugetierkunde 64, 285–297.Google Scholar
Brinkmann, V. & Kristofic, C. (1995) Regulation by corticosteroids of Th1 and Th2 cytokine production in human CD4+ effector T cells generated from CD45RO- and CD45RO+ subsets. Journal of Immunology 152, 3322–3328.CrossRefGoogle Scholar
Crofton, H.D. (1971) A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle 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 epididimys. Journal of Molecular Endocrinology 24, 253–260.CrossRefGoogle Scholar
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, 301–309.3.0.CO;2-1>CrossRefGoogle Scholar
Edwards, J.C. (1988) The effects ofTrichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice. Animal Behaviour 36, 529–540.CrossRefGoogle Scholar
Edwards, J.C. & Barnard, C.J. (1987) The effects ofTrichinella infection on intersexual interactions between mice. Animal Behaviour 35, 533–540.CrossRefGoogle Scholar
Ehman, K.D. & Scott, M.E. (2001) Urinary odour preferences of MHC congenic female mice,Mus domesticus: implications for kin recognition and detection of parasitized males. Animal Behaviour 62, 781–789.CrossRefGoogle Scholar
Fernandes, G.A. (2000) Immunological stress in rats induces bodily alterations in saline-treated conspecifics. Physiology and Behaviour 69, 221–230.CrossRefGoogle ScholarPubMed
Folstad, I. & Karter, A.J. (1992) Parasites, bright males and the immunocompetence handicap. American Naturalist 139, 603–622.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, 153–160.CrossRefGoogle Scholar
Gerendai, I. & Halasz, B. (1997) Neuroendocrine asymmetry. Frontiers of Neuroendocrinology 18, 354–381.CrossRefGoogle ScholarPubMed
Gerlach, G. & Musolf, K. (2000) Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology 14, 1066–1074.CrossRefGoogle Scholar
Gliwicz, J. & Rajska-Jurgiel, E. (1983) Social organization.Acta Theriologica 28(Suppl.), 134–140.CrossRefGoogle Scholar
Gregory, R.D. & Woolhouse, M.E.J. (1993) Quantification of parasite aggregation: a simulation study. Acta Tropica 54, 131–139.CrossRefGoogle ScholarPubMed
Grossman, C.J. (1985) Interactions between the gonadal steroids and the immune system. Science 227, 257–261.CrossRefGoogle ScholarPubMed
Gustafsson, T., Andersson, B. & Meurling, P. (1980) Effect of rank on the growth of the preputial glands in male bank voles,Clethrionomys glareolus . Physiology and Behaviour 24, 689–692.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, 603–615.CrossRefGoogle Scholar
Haukisalmi, V. & Henttonen, H. (1999) Determinants of helminth aggregation in natural host populations: individual differences or spatial heterogeneity?. Ecography 22, 629–636.CrossRefGoogle 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, 551–562.CrossRefGoogle ScholarPubMed
Hillgarth, N. & Wingfield, J.C. (1997) Testosterone and immunosuppression in vertebrates: implications for parasite-mediated sexual selection. pp 143–155 in Beckage, N.E.. (Ed.)Parasites and pathogens; effects on host hormones and behavior. London: Chapman and Hall.Google Scholar
Hoffmeyer, I. (1982) Responses of female bank voles (Clethrionomys glareolus) to dominant vs. subordinate conspecific males and to urine odors from dominant vs. subordinate males. Behavioral Neural Biology 36, 178–188.CrossRefGoogle ScholarPubMed
Hughes, V.L. & Randolph, S.E. (2001) Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. Journal of Parasitology 87, 49–54.CrossRefGoogle ScholarPubMed
Hurst, J.L. (1993) The priming effects of urine substrate marks on interactions between house mice,Mus musculus domesticus, Schwarz and Schwarz. Animal Behaviour 45, 55–81.CrossRefGoogle Scholar
Hurst, J.L., Hall, S., Roberts, R. & Christian, C. (1996) Social organization in the aboriginal house mouse,Mus spretus Lataste: behavioural mechanisms underlying the spatial dispersion of competitors. Animal Behaviour 51, 327–344.CrossRefGoogle 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, 3471–3477.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D.D. (1995) Discrimination by female mice between the odours of parasitized and non-parasitized males. Proceedings of the Royal Society of London Series B 261, 31–35.Google ScholarPubMed
Kavaliers, M., Colwell, D.D. & Choleris, E. (1998) Analgesic responses of male mice exposed to the odors of parasitized females: effects of male sexual experience and infection status. Behavioral Neuroscience 112, 1001–1011.CrossRefGoogle Scholar
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, 541–552.CrossRefGoogle Scholar
Klein, S.L. (2000) Hormones and mating system affect sex and species differences in immune function among vertebrates. Behavioural Processes 51, 149–166.CrossRefGoogle ScholarPubMed
Klein, S.L., Hairston, J.E., DeVries, A.C. & Nelson, R.J. (1997) Social environment and steroid hormones affect species and sex differences in immune function in voles. Hormones and Behavior 32, 30–39.CrossRefGoogle ScholarPubMed
Kozakiewicz, M. (1976) The weight of the eye lens as a proposed age indicator of the bank vole. Acta Theriologia 21, 314–316.CrossRefGoogle Scholar
Maier, S.F., Watkins, L.R. & Fleshner, M. (1994) Psychoneuroimmunology: the interface between behavior, brain and immunology. American Psychologist 49, 1004–1017.CrossRefGoogle Scholar
Moller, 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, 69–104.CrossRefGoogle Scholar
Nunn, C.L., Gittelman, J.L. & Antonovics, J. (2000) Promiscuity and the primate immune system. Science 290, 1168–1170.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, 827–835.CrossRefGoogle ScholarPubMed
Palmer, A.R. & Strobeck, C. (1986) Fluctuating asymmetry: measurement, analysis, pattern. Annual Review of Ecology and Systematics 17, 391–421.CrossRefGoogle Scholar
Pawelczyk, A. & Sinski, E. (2000) Prevalence of IgG antibodies response toBorrelia burgdorferi in populations of wild rodents from the Mazury Lake District region of Poland. Annals of Agricultural and Environmental Medicine 7, 79–83.Google ScholarPubMed
Penn, D. & Potts, W.K. (1998) Untrained mice discriminate MHC-determined odors. Physiology and Behaviour 64, 235–243.CrossRefGoogle ScholarPubMed
Quinnell, R.J. & Keymer, A.E. (1990) Acquired immunity and epidemiology. pp 317–343 Behnke, J.M..Parasites: immunity and pathology. London: Taylor and Francis.Google Scholar
Rozenfeld, F.M. & Rasmont, R. (1991) Odour cue recognition by dominant male bank voles,Clethrionomys glareolus . Animal Behaviour 41, 839–850.CrossRefGoogle Scholar
Rutovskaya, V. (1968) Acoustic activity and social behaviour of the bank vole.pp 177–188 inSokolov, V.E., Rozhnov, V.V. & Serbenyuk, M.A..(Eds)Behaviour, communication and behaviour in mammals. V.E. IEE RAS Moskva.Google Scholar
Shaw, D.J. & Dobson, A.P. (1995)Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111(Suppl.), S111–S133.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, 317–321.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, 545–554.CrossRefGoogle Scholar
Smith, F.V., Barnard, C.J. & Behnke, J.M. (1996) Social odours, hormone modulation and resistance to disease in male laboratory mice. Animal Behaviour 52, 141–153.CrossRefGoogle Scholar
Stachon, M., Furstenburg, E., Gromadzka-Ostrowska, J. & Romanowicz, K. (2001) The influence of different dietary fat sources on tissue corticosterone concentration in rats. Journal of Animal and Feed Sciences 10, 341–354.CrossRefGoogle Scholar
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, 374–380.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, 898–908.CrossRefGoogle ScholarPubMed
Wakelin, D. & Blackwell, J.M. (1993) Genetic variation in immunity to parasitic infections. pp 3–32 inWarren, K.S.(Ed.)Immunology and molecular biology of parasitic infections. Boston: Blackwell Scientific Publications.Google Scholar
Wilckens, T. & Rijk, R. de (1997) Glucocorticoids and immune function: unknown dimensions and new frontiers. Immunology Today 18, 418–424.CrossRefGoogle ScholarPubMed