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Local variation in helminth burdens of Egyptian spiny mice (Acomys cahirinus dimidiatus) from ecologically similar sites: relationships with hormone concentrations and social behaviour

Published online by Cambridge University Press:  12 April 2024

C.J. Barnard ,
E. Sayed ,
L.E. Barnard ,
J.M. Behnke ,
I. Abdel Nabi ,
N. Sherif ,
A. Shutt  and
S. Zalat
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
E. Sayed
Affiliation:
Department of Zoology, Faculty of Science, Suez Canal University, Ismailia, Egypt
L.E. Barnard*
Affiliation:
Animal Behaviour and Ecology Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
J.M. Behnke
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
I. Abdel Nabi
Affiliation:
Department of Zoology, Faculty of Science, Suez Canal University, Ismailia, Egypt
N. Sherif
Affiliation:
Department of Zoology, Faculty of Science, Suez Canal University, Ismailia, Egypt
A. Shutt
Affiliation:
Infection and Immunity Research Group, School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
S. Zalat
Affiliation:
Department of Zoology, Faculty of Science, Suez Canal University, Ismailia, Egypt
*
*Fax: (++44) 115 9513251 E-mail: [email protected]
†Current address: Epidemiology Group, Faculty of Veterinary Science, University of Liverpool, Leahurst, Neston, Cheshire, CH64 7TE, UK
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Abstract

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Populations of Egyptian spiny mice (Acomys cahirinus dimidiatus) in a fragmented montane wadi system in the Sinai showed significant differences in the abundance of gut helminths. Differences in parasite load between populations were positively associated with measures of androgen activity but showed no significant relationship with glucocorticoid activity. Social discrimination tests with adult males from different wadis showed that those from sites with greater helminth abundance were less likely to investigate odours from other males and were less aggressive when subsequently interacting with the odour donors. Subjects showed markedly more investigation towards the odours of males from distant wadis compared with those from their own or immediately neighbouring wadi, but were less aggressive when confronted with odour donors from distant wadis. Despite this, there was a positive relationship between the amount of investigation towards distant male odour and subsequent aggression towards the male. While aggressiveness was positively associated with measures of androgen and glucocorticoid activity, no significant relationship emerged with individual helminth infection. Thus aggressiveness appeared to relate to overall local population levels of infection rather than individual challenge.

Type
Review Article
Information
Journal of Helminthology , Volume 77 , Issue 3 , September 2003 , pp. 197 - 207
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
Barnard, C.J., & Behnke, J.M. (Eds) (1990)Parasitism and host behaviour. London, Taylor & Francis.CrossRefGoogle Scholar
Barnard, C.J. & Behnke, J.M. (2001) From psychoneuroimmunology to ecological immunology: life history strategies and immunity trade-offs. pp 35–45. inAder, 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, 183–192.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) The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proceedings of the Royal Society of London Series B 265, 693–701.CrossRefGoogle ScholarPubMed
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., Kulis, K., Behnke, J.M., Bajer, A., Gromadzka-Ostrakowska, J., Stachon, E. & Sinski, E. (2003) Local variation in helminth burdens of bank voles (Clethrionomys glareolus) from ecologically similar sites: temporal stability and relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 185–195.CrossRefGoogle ScholarPubMed
Behnke, J.M., Barnard, C.J. & 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., 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
Borkowska, A. (1999) Genetic and morphological variation among populations of the bank voleClethrionomys glareolus from north-eastern Poland: the seasonal aspect. Zeitschrift Saugetierkunde 64, 285–297.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 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
Gasparotto, O.C., Ignacio, Z.M., Lin, K. & Goncalves, S. (2002) The effect of different psychological profiles and timings of stress exposure on humoral immune response. Physiology and Behaviour 76, 321–326.CrossRefGoogle ScholarPubMed
Gerendai, I. & Halasz, B. (1997) Neuroendocrine asymmetry. Frontiers in Neuroendocrinology 18, 354–381.CrossRefGoogle ScholarPubMed
Grossman, C.J. (1985) Interactions between the gonadal steroids and the immune system. Science 227, 257–261.CrossRefGoogle ScholarPubMed
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
Hobbs, J.J. (1995) Mount Sinai.Austin, Texas: Texas University Press.Google Scholar
Hurst, J.L., Fang, J. & Barnard, C.J. (1994) The role of substrate odours in maintaining social tolerance between male house mice,Mus musculus domesticus: relatedness, incidental kinship effects and the establishment of social status. Animal Behaviour 48, 157–167.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
Hurst, J.L., Barnard, C.J., Hare, R., Wheeldon, E.B. & West, C.D. (1996) Housing and welfare in laboratory rats: tome-budgeting and pathophysiology in single-sex groups. Animal Behaviour 52, 335–360.CrossRefGoogle Scholar
Irvin, A.D., Young, E.R., Osborn, G.D. & Francis, L.M.A. (1981) A comparison ofBabesia infections in intact, surgically splenectomized, and congenitally asplenic (Dh/+) mice. International Journal for Parasitology 11, 251–255.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
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
Lamers, W.H., Mooren, P.G., Griep, H., Endert, E., Degenhart, H.J. & Charles, R. (1986) Hormones in perinatal rat and spiny mouse: relation to altricial and precocial timing of birth.American Journal of Physiology 14, E78–E85.Google Scholar
Mackintosh, J.H. (1981) Behaviour of the house mouse. Symposium of the Zoological Society of London 47, 337–365.Google Scholar
Møller, A.P. & Swaddle, J.P. (1997) Asymmetry, developmental stability and evolution. pp Oxford:Oxford University Press.CrossRefGoogle Scholar
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
Penn, D. & Potts, W.K. (1998) Chemical signals and parasite-mediated sexual signals. Trends in Ecology and Evolution 13, 391–396.CrossRefGoogle Scholar
Phillips, R.S. (1969) The role of the spleen in relation to natural and acquired immunity to infections ofBabesia rodhaini in the rat. Parasitology 59, 637–648.CrossRefGoogle ScholarPubMed
Poiani, A., Goldsmith, A.R. & Evans, M.R. (2000) Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model. Behavioral Ecology and Sociobiology 47, 230–240.CrossRefGoogle Scholar
Roberts, C.W., Satoskar, A. & Alexander, J. (1996) Sex steroids, pregancy-associated hormones and immunity to parasitic infections. Parasitology Today 12, 382–388.CrossRefGoogle Scholar
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
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
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, 893–913.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, 374–380.Google ScholarPubMed
Wakelin, D. & Selby, G.R. (1974) The induction of immunological tolerance to the parasitic nematodeTrichuris muris in corticosterone-treated mice. Immunology 26, 1–10.Google Scholar
Wedekind, C. & Folstad, I. (1994) Adaptive and non-adaptive immunosuppression by sex hormones. American Naturalist 143, 936–938.CrossRefGoogle Scholar
Wilckens, T. & Rijk, R.de(1997) Glucocorticoids and immune function: unknown dimensions and new frontiers. Immunology Today 18, 418–424.CrossRefGoogle ScholarPubMed
Zalat, S. & Gilbert, F.S. (1998) A walk in the Sinai: St Katherine to Al Galt al Azraq (the Blue Pool). Cairo: El Haramen Press.Google Scholar