An experimental study on the causes of sex-biased mortality in the black-headed gull - The possible role of testosterone

Journal of Animal Ecology

Volumn 74, Issue 4, 2005, Pages 735-741

  Müller, Wendt ^a,b   Groothuis, Ton G G ^a   Eising, Corine M ^a   Dijkstra, Cor ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b NONE   (Netherlands)

Author keywords

Anti androgen; Brood size; Flutamide; Immunity; PHA

Indexed keywords

HATCHING; MORTALITY; PHENOTYPE; SEABIRD; SEX-RELATED DIFFERENCE; TESTOSTERONE;

AVES; LARUS RIDIBUNDUS;

EID: 23744487573     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2005.00964.x     Document Type: Article

References (46)

1. Alonso-Alvarez, C. & Tella, J.L. (2001) Effects of experimental food restriction and body-mass changes on avian T-cell mediated immune response. Canadian Journal of Zoology, 79, 101-105.
2. Balthazart, J. & Adkins-Regan, E.A. (2003) Sexual differentiation of brain and behaviour in birds. Hormones, Brain and Behavior, vol. IV (eds D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach & R. Rabin), pp. 223-301. Elsevier, the Netherlands.
3. Blount, J.D., Surai, P.F., Nager, R.G., Houston, D.C., Møller, A.P., Trewby, M.L. & Kennedy, M. (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proceedings of the Royal Society of London B, 269, 29-36.
4. Burke, W.H. (1996) Effects of in ovo injection of an antiandrogen on embryonic and posthatching growth of broiler chicks. Poultry Science, 75, 648-655.
5. Clutton-Brock, T.H., Albon, S.D. & Guinness, F.E. (1985) Parental investment and sex differences in juvenile mortality in birds and mammals. Nature, 313, 131-133.
6. Dijkstra, C., Daan, S. & Pen, I. (1998) Fledging sex ratios in relation to brood size in size-dimorphic altricial birds. Behavioral Ecology, 9, 287-296.
7. Eising, C.M., Eikenaar, C., Schwabl, H. & Groothuis, T.G.G. (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proceedings of the Royal Society London, Biological Sciences, 268, 839-846.
8. Eising, C.M., Visser, G.H., Müller, W. & Groothuis, T.G.G. (2003) Steroids for free? No metabolic costs of elevated maternal androgen levels in the black-headed gull. Journal of Experimental Biology, 206, 3211-3218.
9. Fargallo, A.J., Laaksonen, T., Pöyri, V. & Korpimäki, E. (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecology Letters, 5, 95-101.
10. Glutz von Blotzheim, U.N. & Bauer, K.M. (1982) Handbuch der Vögel Mitteleuropas, Band 8. Aula Verlag, Wiesbaden.
11. Griffiths, R. (1992) Sex-biased mortality in the lesser black-backed gull Larus fuscus during the nestling stage. Ibis, 134, 237-244.
12. Griffiths, R., Double, M.C., Orr, K. & Dawson, R.J.G. (1998) A DNA test to sex most birds. Molecular Ecology, 7, 1071-1075.
13. Grossman, C.J. (1985) Interactions between the gonadal steroids and the immune system. Science, 227, 257-261.
14. Henry, M.H. & Burke, W.H. (1998) Sexual dimorphism in broiler chick embryos and embryonic muscle development in late incubation. Poultry Science, 77, 728-736.
15. Jennings, A.R. & Soulsby, E.J.L. (1958) Disease in a colony of Black-headed Gulls Lams ridibundus. Ibis, 100, 305-312.
16. Klein, S.L. (2000) The effects of hormones on sex differences in infection: from genes to behavior. Neuroscience Biobehavioral Reviews, 24, 627-638.
17. Li, Q., Alston-Mills, G.B. & Ottinger, M.A. (1991) Avian LHRH-I during embryonic development: measurement by competitive ELISA with a monoclonal antibody. General and Comparative Endocrinology, 82, 444-450.
18. Lipar, J.L. & Ketterson, E.D. (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Aegelius phoeniceus. Proceedings of the Royal Society London, Biological Sciences, 267, 2005-2010.
19. Müller, W., Dijkstra, C. & Groothuis, T.G.G. (2003) Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ridibundus) depend on the hatching order. Behavioral Ecology and Sociobiology, 55, 80-86.
20. Müller, W., Eising, C., Dijkstra, C. & Groothuis, T.G.G. (2002) Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proceedings of the Royal Society London, Biological Sciences, 269, 2249-2256.
21. Nager, R.G., Monaghan, P., Griffiths, R., Houston, D.C. & Dawson, R. (1999) Experimental evidence that off spring sex ratio varies with maternal condition. Proceedings of the National Academy of Sciences USA, 96, 570-573.
22. Nager, R.G., Monaghan, P., Houston, D.C. & Genovart, M. (2000) Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behavioral Ecology and Sociobiology, 48, 452-457.
23. Nielsen, H.C. & Torday, J.S. (1985) Sex differences in avian embryo pulmonary surfactant production: evidence for sex chromosome involvement. Endocrinology, 117, 31-37.
24. Olsen, N.J. & Kovacs, W.J. (1996) Gonadal steroids and immunity. Endocrinology Reviews, 17, 369-384.
25. Ottinger, M.A. & Abelnabi, M.A. (1997) Neuroendocrine system and avian sexual differentiation. American Zoologist, 37, 514-523.
26. Ottinger, M.A., Pitts, S. & Abelnabi, M.A. (2001) Steroid hormones during embryonic development in Japanese quail: plasma, gonadal, and adrenal levels. Poultry Science, 80, 795-799.
27. Rasbash, J., Browne, W., Healy, M., Cameron, B. & Charlton, C. (2000) Multilevel Models Project. University of London, London.
28. Røskraft, E. & Slagsvold, T. (1985) Differential mortality of male and female offspring in experimentally manipulated broods of the rook. Journal of Animal Ecology, 54, 261-266.
29. Sayag, N., Snapir, N., Robinzon, B., Arnon, E., El Halawani, M.E. & Grimm, V.E. (1989) Embryonic sex steroids affect mating behavior and plasma LH in adult chicken. Physiology and Behavior, 45, 1107-1112.
30. Sayce, J.R. & Hunt, G.L. (1987) Sex ratios of prefledging western gulls. Auk, 104, 33-37.
31. Schumacher, M., Sulon, J. & Balthazart, J. (1988) Changes in serum concentrations of steroids during embryonic and post-hatching development of male and female Japanese quail (Coturnix coturnix japonica). Journal of Endocrinology, 118, 127-134.
32. Schwabl, H. (1993) Yolk is a source of maternal testosterone for developing birds. Proceedings of The National Academy of Sciences USA, 90, 11446-11450.
33. Schwabl, H. (1996) Maternal testosterone in the egg enhances postnatal growth. Comparative Biochemical Physiology, 114, 271-276.
34. Schwabl, H. & Kriner, E. (1991) Territorial aggression and song of male robins (Erithacus rubecula) in autumn and spring: effects of antiandrogen treatment. Hormones and Behavior, 25, 180-194.
35. Smits, J.E., Bortolotti, G.R. & Tella, J.L. (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Functional Ecology, 13, 567-572.
36. Soma, K.K., Sullivan, K. & Wingfield, J. (1999) Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during non-breeding season. General and Comparative Endocrinology, 115, 442-453.
37. Strasser, R. & Schwabl, H. (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behavioral Ecology and Sociobiology, 56, 491-497.
38. Tanabe, Y., Nakamura, T., Fujoika, K. & Doi, O. (1979) Production and secretion of sex steroids by the testes the ovary, and the adrenal glands of embryonic and young chickens (Gallus domesticus). General and Comparative Endocrinology, 39, 26-33.
39. Tanabe, Y., Saito, N. & Nakamura, T. (1986) Ontogenetic steroidgenesis by testes, ovary and adrenals of embryonic and postembryonic chickens (Gallus domesticus). General and Comparative Endocrinology, 63, 456-463.
40. Tanabe, Y., Takashi, Y. & Nakamura, T. (1983) Steroid hormone synthesis and secretion by testes, ovary, and adrenals of embryonic and postembryonic ducks. General and Comparative Endocrinology, 49, 144-153.
41. Torres, R. & Drummond, H. (1997) Female-biased mortality in daughters of a bird with size dimorphism. Journal of Animal Ecology, 66, 859-865.
42. Tschirren, B., Fitze, P.S. & Richner, H. (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology, 72, 839-845.
43. Verboven, N., Monaghan, P., Evans, D.M., Schwabl, H., Evans, N., Whitelaw, C. & Nager, R.G. (2003) Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proceedings of the Royal Society London, Biological Sciences, 270, 2223-2232.
44. Williams, T.D. (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biological Reviews, 68, 35-59.
45. Wilson, J.A. & Glick, B. (1970) Ontogeny of mating behavior in the chicken. American Journal of Physiology, 218, 951-955.
46. Woods, J.E., Simpson, R.M. & Moore, P.L. (1975) Plasma testosterone levels in the chick embryo. General and Comparative Endocrinology, 27, 543-547.