Testosterone is positively related to the output of nematode eggs in male Alpine ibex (Capra ibex) faeces

Evolutionary Ecology Research

Volumn 9, Issue 8, 2007, Pages 1277-1292

  Decristophoris, Paola M A ^a,b   Von Hardenberg, Achaz ^c   McElligott, Alan G ^a,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^c Gran Paradiso National Park ^*  (Italy)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Body mass; Dominance; Faecal egg counts; Immunocompetence; Immunosuppression; Path model

Indexed keywords

CAPRA IBEX; UNGULATA;

EID: 38949138134     PISSN: 15220613     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Adamo, S.A. 2004. How should behavioural ecologists interpret measurements of immunity? Anim. Behav., 68: 1443-1449.
2. Albon, S.D., Stien, A., Irvine, R.J., Langvtan, R., Ropstad, E. and Halvorsen, O. 2002. The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. J. Anim. Ecol., 71: 937-945.
3. Alexander, J. and Stimson, W.H. 1988. Sex hormones and the course of parasitic infection. Parasitol. Today, 4: 189-193.
4. Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press.
5. Barnard, C.J., Behnke, J.M. and 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.
6. Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. and Smithurst, P.R. 1997. Modulation of behaviour and testosterone concentration in immunodepressed male laboratory mice (Mus musculus). Physiol. Behav., 61: 907-917.
7. Barnard, C.J., Behnke, J.M., Gage, A.R., Brown, H. and 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). Proc. R. Soc. Lond. B, 265: 693-101.
8. Bassano, B., von Hardenberg, A., Pelletier, F. and Gobbi, G. 2003. A method to weigh free-ranging ungulates without handling. Wildl. Soc. Bull., 31: 1205-1209.
9. Bro-Jørgensen, J. 2007. The intensity of sexual selection predicts weapon size in male bovids. Evolution, 61: 1316-1326.
10. Brunsdon, R.V. and Adam, J.L. 1975. Internal parasites and animal production. NZ Soc. Anim. Prod. Occ. Publ., 4: 53.
11. Buchanan, K.L., Evans, M.R. and Goldsmith, A.R. 2003. Testosterone, dominance signalling and immunosuppression in the house sparrow, Passer domesticus. Behav. Ecol. Sociobiol., 55: 50-59.
12. Coltman, D.W., Pilkington, J.G., Smith, J.A. and Pemberton, J.M. 1999. Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution, 53: 1259-1267.
13. Coltman, D.W., Festa-Bianchet, M., Jorgenson, J.T. and Strobeck, C. 2002. Age-dependent sexual selection in bighorn rams. Proc. R. Soc. Lond. B, 269: 165-172.
14. Côté, S.D. 2000. Determining social rank in ungulates: a comparison of aggressive interactions recorded at a bait site and under natural conditions. Ethology, 106: 945-955.
15. David, H.A. 1987. Ranking from unbalanced paired-comparison data. Biometrika, 74: 432-436.
16. de Vries, H. 1998. Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim. Behav., 55: 827-843.
17. Ditchkoff, S.S., Lochmiller, R.L., Masters, R.E., Hoofer, S.R. and Van der Bussche, R.A. 2001a. Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution, 55: 616-625.
18. Ditchkoff, S.S., Spicer, L.J., Masters, R.E. and Lochmiller, R.L. 2001b. Concentrations of insulin-like growth factor-I in adult male white-tailed deer (Odocoileus virginianus): associations with serum testosterone, morphometrics and age during and after the breeding season. Comp. Biochem. Physiol. A, 129: 887-895.
19. Duffy, D.L., Bentley, G.E., Drazen, D.L. and Ball, G.F. 2000. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav. Ecol., 11: 654-662.
20. Folstad, I. and Karter, A.J. 1992. Parasites, bright males, and the immunocompetence handicap. Am. Nat., 139: 603-622.
21. Folstad, I., Nilssen, A.C., Halvorsen, O. and Anderson J. 1989. Why do male reindeer have higher abundance of second and third instar larvae of Hypoderma tarandi than females? Oikos, 55: 87-92.
22. Giacometti, M., Willing, R. and Defila, C. 2002. Ambient temperature in spring affects horn growth in male Alpine ibexes. J. Mammal., 83: 245-251.
23. Greenman, C.G., Martin, L.B. and Hau, M. 2005. Reproductive state, but not testosterone, reduces immune function in male house sparrows (Passer domesticus). Physiol. Biochem. Zool., 78: 60-68.
24. Grossman, C.J. 1984. Regulation of the immune system by sex steroids. Endocr. Rev., 5: 435-455.
25. Grossman, C.J. 1985. Interactions between the gonadal steroids and the immune system. Science, 227: 257-261.
26. Hamilton, W.D. and Zuk, M. 1982. Heritable true fitness and bright birds: a role of parasites? Science, 218: 384-387.
27. Hasselquist, D., Marsh, J.A., Sherman, P.W. and Wingfield, J.C. 1999. Is avian humoral immunocompetence suppressed by testosterone? Behav. Ecol. Sociobiol., 45: 167-175.
28. Henderson, R.E. and Firebaugh, J.E. 1997. Horn growth of a castrated Bighorn sheep, Ovis canadensis. Can. Field Nat., 111: 475-477.
29. Hillgarth, N. and Wingfield, J.C. 1997. Testosterone and immunosuppression in vertebrates: implications for parasite-mediated sexual selection. In Parasites and Pathogens, Effects on Host Hormones and Behavior (N.E. Beckage, ed.), pp. 143-155. New York: Chapman & Hall.
30. Hughes, V.L. and Randolph, S.E. 2001. Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. J. Parasitol., 87: 49-54.
31. Khan, M.Z., Altmann, J., Isani, S.S. and Yu, J. 2002. A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen. Comp. Endocrinol., 128: 57-64.
32. Kimball, J.W. 1990. Introduction to Immunology. New York: Macmillan.
33. Kraus, C., Heistermann, M. and Kappeler, P.M. 1999. Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi). Physiol. Behav., 66: 855-861.
34. Lanfranchi, P., Manfredi, M.T., Zaffaroni, E., Fraquelli, C., Ratti, P. and Giacometti, M. 1995. Eine dreijährige Untersuchung der Labmagen-Helminthenfauna beim Alpensteinbock (Capra ibex) der Colonie Albris, Graubünden, Schweiz. Z. Jagdwiss., 41: 24-35.
35. Li, C.W., Jiang, Z.G., Zeng, Y. and Yan, C. 2004. Relationship between serum testosterone, dominance and mating success in Père David's deer stags. Ethology, 110: 681-691.
36. Lincoln, G.A. 1998. Reproductive seasonality and maturation throughout the complete life-cycle in the mouflon ram (Ovis musimon). Anim. Reprod. Sci., 53: 87-105.
37. Lincoln, G.A., Guinness, F. and Short, R.V. 1972. Way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Horm. Behav., 3: 375-396.
38. Lindström, K.M., Krakower, D., Lundström, J.O. and Silverin, B. 2001. The effects of testosterone on a viral infection in greenfinches (Carduelis chloris): and experimental test of the immunocompetence- handicap hypothesis. Proc. R. Soc. Lond. B, 268: 207-211.
39. Litvinova, E.A., Kudaeva, O.T., Mershieva, L.V. and Moshkin, M.P. 2005. High level of circulating testosterone abolishes decline in scent attractiveness in antigen-treated male mice. Anim. Behav., 69: 511-517.
40. McElligott, A.G., Mattiangeli, V., Mattiello, S., Verga, M., Reynolds, C.A. and Hayden, T.J. 1998. Fighting tactics of fallow bucks (Dama dama, Cervidae): reducing the risks of serious conflict. Ethology, 104: 789-803.
41. McElligott, A.G., Gammell, M.P., Harty, H.C., Paini, D.R., Murphy, D.T., Walsh, J.T et al. 2001. Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success? Behav. Ecol. Sociobiol., 49: 266-272.
42. McElligott, A.G., Naulty, F., Clarke, W.V. and Hayden, T.J. 2003. The somatic cost of reproduction: what determines reproductive effort in prime-aged fallow bucks? Evol. Ecol. Res., 5: 1239-1250.
43. McKenna, P.B. 1987. The estimation of gastrointestinal worm burdens in young sheep flocks: a new approach to the interpretation of faecal egg counts. NZ Vet. J., 35: 94-97.
44. Mougeot, F., Irvine, J.R., Seivwright, L., Redpath, S.M. and Piertney, S. 2004. Testosterone, immunocompetence, and honest sexual signalling in male red grouse. Behav. Ecol., 15: 930-937.
45. Nievergelt, B. 1974. A comparison of rutting behaviour and grouping in the Ethiopian and alpine ibex. In The Behaviour of Ungulates and its Relation to Management (V. Geist and F. Walther, eds.), pp. 324-340. Morges: IUCN.
46. Pelletier, F., Bauman, J. and Festa-Bianchet, M. 2003. Faecal testosterone in bighorn sheep (Ovis canadensis): behavioural and endocrine correlates. Can. J. Zool., 81: 1678-1684.
47. Pelletier, F., Page, K.A., Ostiguy, T. and Festa-Bianchet, M. 2005. Faecal counts of lungworm larvae and reproductive effort in bighorn sheep, Ovis canadensis. Oikos, 110: 473-480.
48. Perez, J.M., Granados, J.E., Pérez, M.C., Màrquez, F.J., Ferroglio, E. and Rossi, L. 2003. A survey of the gastrointestinal nematodes of Spanish ibex (Capra pyrenaica) in a high mountain habitat. Parasitology, 89: 315-318.
49. Peters, A. 2000. Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc. R. Soc. Lond. B, 267: 883-889.
50. Peters, A., Delhey, K., Denk, A.G. and Kempenaers, B. 2004. Trade-offs between immune investment and sexual signaling in male mallards. Am. Nat., 164: 51-59.
51. Pinheiro, J.C. and Bates, D.M. 2001. Mixed Effects Models in S and S-Plus. New York: Springer-Verlag.
52. Poiani, A., Goldsmith, A.R. and Evans, M.R. 2000. Ectoparasites of house sparrows (Passer domesticus): an experimental test of immunocompetence handicap hypothesis and a new model. Behav. Ecol. Sociobiol., 47: 230-242.
53. Pomroy, W.E. 1997. Internal helminth parasites of ruminants. In Sustainable Control of Internal Parasites in Ruminants - An Animal Industries Workshop (G.K. Barrell, ed.), pp. 81-91. Lincoln: Animal and Veterinary Science Group, Lincoln University.
54. Preston, B.T., Stevenson, I.R., Pemberton, J.M., Coltman, D.W. and Wilson, K. 2003. Overt and covert competition in a promiscuous mammal: the relative importance of weaponry and testes size to male reproductive success. Proc. R Soc. Lond. B, 270: 633-640.
55. Ratti, P. and Habermehl, K.H. 1977. Untersuchen zur Altersschätzung und Alterbestimmung beim Alpensteinbock (Capra ibex ibex) im Kanton Graubunden. Z. Jagdwiss., 4: 188-213.
56. Roberts, M.L., Buchanan, K.L. and Evans, M.R. 2004. Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim. Behav., 68: 227-239.
57. Rolf, H.J. and Fischer, K. 1990. Serum testosterone (T) and 5-α-dihydrotestosterone (DHT) in male fallow deer (Dama dama L.): seasonality and age dependence. Comp. Biochem. Physiol. A, 95: 445-452.
58. Saino, N., Møller, A.P. and Bolzern, A.M. 1995. Testosterone effects on the immune system and parasite infestations in the barn sparrow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behav. Ecol., 6: 397-404.
59. Saunders, F.C., McElligott, A.G., Safi, K. and Hayden, T.J. 2005. Mating tactics of male feral goats (Capra hircus): risks and benefits. Acta Ethol., 8: 103-110.
60. Seivwright, L.J., Redpath, S.M., Mougeot, F., Leckie, F. and Hudson, P.J. 2005. Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse. Proc. R. Soc. Lond. B, 272: 2299-2304.
61. Shipley, B. 1999. Testing causal explanations in organismal biology: causation, correlation and structural equation modelling. Oikos, 86: 374-382.
62. Shipley, B. 2000. Cause and Correlation in Biology: A User's Guide to Path Analysis, Structural Equations and Causal Inference. Cambridge: Cambridge University Press.
63. Shipley, B. 2004. Analysing the allometry of multiple interacting traits. Persp. Plant Ecol. Evol. Syst., 6: 235-241.
64. Smith, J.A., Wilson, K., Pilkington, J.G. and Pemberton, J.M. 1999. Heritable variation in resistance to gastro-intestinal nematodes in an unmanaged mammal population. Proc. R. Soc. Lond. B, 266: 1283-1290.
65. Stear, M.J. and Murray, M. 1994. Genetic resistance to parasitic disease: particularly of resistance in ruminants to gastrointestinal nematodes. Vet. Parasitol., 54: 161-176.
66. Stear, M.J., Bishop, S.C., Doligalska, M., Duncan, J.L., Holmes, P.H., Irvine, J. et al. 1995. Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunol., 17: 643-652.
67. Stear, M.J., Bairden, K., Duncan, J.L., Holmes, P.H., McKellar, Q.A., Park, M. et al. 1997. How hosts control worms. Nature, 389: 27.
68. Sthoeger, Z.M., Chiorazzi, N. and Lahita, R.G. 1988. Regulation of the immune response by sex hormones: in vitro effects of estradiol and testosterone on pokeweed mitogen-induced human B cell differentiation. J. Immunol., 141: 91-98.
69. Stoehr, A.M. and Kokko, H. 2006. Sexual dimorphism in immunocompetence: what does life-history theory predict? Behav. Ecol., 17: 751-756.
70. Thienpont, D., Rochette, F. and Vanparijs, O.F.J. 1979. Diagnostic de verminose par examen coprologique. Beerse: Janssen Research Foundation.
71. Toïgo, C., Gaillard, J.M., Festa-Bianchet, M., Largo, E., Michallet, J. and Maillard, D. 2007. Sex- and age-specific survival of the highly dimorphic alpine ibex: evidence for a conservative life-history tactic. J. Anim. Ecol., 76: 679-686.
72. Vicente, J., Höfle, U., García Fernandez-De-Mera, I. and Gortazar, C. 2007. The importance of parasite life history and host density in predicting the impact of infections in red deer. Oecologia, 152: 655-664.
73. von Hardenberg, A. 2005. Sénescence, selection sexuelle et dynamique de population du bouquetin des alpes (Capra ibex). PhD dissertation, Université de Sherbrooke, Sherbrooke, Canada.
74. von Hardenberg, A., Bassano, B., del Pilar Zumel Arraz, M. and Bogliani, G. 2004. Horn growth but not asymmetry heralds the onset of senescence in male alpine ibex. J. Zool., 263: 425-432.
75. Weckerly, F.W. 1998. Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J. Mammal., 79: 33-52.
76. Zaffaroni, E., Manfredi, M.T., Citterio, C., Sala, M., Piccolo, G. and Lanfranchi, P. 2000. Host specificity of abomasal nematodes in free ranging alpine ruminants. Vet. Parasitol., 90: 221-230.
77. Zahavi, A. 1975. Mate selection - a selection for a handicap. J. Theor. Biol., 53: 205-214.
78. Zuk, M. 1996. Disease, endocrine-immune interactions, and sexual selection. Ecology, 77: 1037-1042.
79. Zuk, M., Johnsen, T.S. and Maclarty, T. 1995. Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc. R. Soc. Lond. B, 260: 205-210.