Seasonal and population variation in male testosterone levels in breeding orange-crowned warblers (Vermivora celata)

General and Comparative Endocrinology

Volumn 168, Issue 3, 2010, Pages 333-339

  Horton, Brent M ^a   Yoon, Jongmin ^b   Ghalambor, Cameron K ^b   Moore, Ignacio T ^c   Scott Sillett, T ^a  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Breeding density; Life history; Mating effort; Parental investment; Testosterone; Trade offs

Indexed keywords

TESTOSTERONE;

ARTICLE; BIRD; BREEDING; CONTROLLED STUDY; GEOGRAPHIC DISTRIBUTION; LIFE HISTORY; MALE; MALE GENITAL SYSTEM; MATING; NESTLING; NONHUMAN; POPULATION DENSITY; PRIORITY JOURNAL; SEASONAL VARIATION; SOCIAL ENVIRONMENT; SPECIES DIFFERENCE; TESTOSTERONE BLOOD LEVEL; VERMIVORA CELATA;

EID: 77955569584     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2010.04.019     Document Type: Article

References (74)

1. Alatalo R.V., Hoglund J., Lundberg A., Rintamaki P.T., Silverin B. Proceedings of the Royal Society B: Biological Sciences 1996, 263:1697-1702.
2. Ball G.F., Wingfield J.C. Changes in plasma levels of sex steroids in relation to multiple broodedness and nest site density in male starlings. Physiological Zoology 1987, 60:191-199.
3. Beletsky L.D., Orians G.H., Wingfield J.C. Steroid hormones in relation to territoriality, breeding density, and parental behavior in male yellow-headed blackbirds. Auk 1990, 107:60-68.
4. Beletsky L.D., Orians G.H., Wingfield J.C. Year-to-year patterns of circulating levels of testosterone and corticosterone in relation to breeding density, experience, and reproductive success of the polygynous red-winged blackbird. Hormones and Behavior 1992, 26:420-432.
5. Beletsky L.D., Gori D.F., Freeman S., Wingfield J.C. Testosterone and polygyny in birds. Current Ornithology 1995, 12:654-662.
6. Buchanan K.L., Evans M.R., Goldsmith A.R., Bryant D.M., Rowe L.V. Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signaling?. Proceedings of the Royal Society B: Biological Sciences 2001, 268:1337-1344.
7. Buttemer W.A., Warne S., Bech C., Astheimer L.B. Testosterone effects on avian basal metabolic rate and aerobic performance. Facts and artifacts. Comparative Biochemistry and Physiology A 2008, 150:204-210.
8. Cawthorn J.M., Morris D.L., Ketterson E.D., Nolan V. Influence of experimentally elevated testosterone on nest defense in dark-eyed juncos. Animal Behaviour 1998, 56:617-621.
9. Chandler C.R., Ketterson E.D., Nolan V., Ziegenfus C. Effects of testosterone on spatial activity in free-ranging male dark-eyed juncos, Junco hyemalis. Animal Behaviour 1994, 47:1445-1455.
10. Dawson A. The effects of daylength and testosterone on the initiation and progress of moult in starlings, Sturnus vulgaris. Ibis 1994, 136:335-340.
11. Dufty A.M. Testosterone and survival. Hormones and Behavior 1989, 23:185-193.
12. Endstrom D.A., Ketterson E.D., Nolan V. Testosterone and mate choice in the dark-eyed junco. Animal Behaviour 1997, 54:1135-1146.
13. Finch C.E., Rose M.R. Hormones and the physiological architecture of testosterone's effects on fitness. American Naturalist 1995, 167:667-683.
14. Folstad I., Karter A.J. Parasites, bright males, and the immunocompetence handicap. American Naturalist 1992, 139:603-622.
15. Fusani L. Testosterone control of male courtship in birds. Hormones and Behavior 2008, 54:227-233.
16. Ghalambor C.K., Martin T.E. Fecundity-survival trade-offs and parental risk-taking in birds. Science 2001, 292:494-497.
17. Goymann W., Geue D., Schwabl I., Links H., Schmidl D., Schwabl H., Gwinner E. Testosterone and corticosterone during the breeding cycle of equatorial and European stonechats (Saxicola torquata axillaris and S. t. rubicola). Hormones and Behavior 2006, 50:779-785.
18. Greives T.J., McGlothlin J.W., Jawor J.M., Demas G.E., Ketterson E.D. Testosterone and innate immune function inversely covary in a wild population of breeding dark-eyed juncos (Junco hyemalis). Functional Ecology 2006, 20:812-818.
19. Hau M. Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays 2007, 29:133-144.
20. Hegner R.E., Wingfield J.C. Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 1987, 104:462-469.
21. Holberton R.L., Dufty A.M. Hormones and variation in life history strategies of migratory and non-migratory birds. Birds of Two Worlds: The Ecology and Evolution of Migratory Birds 2005, 290-302. Johns Hopkins Press. P. Marra, R. Goldberg (Eds.).
22. Hunt K., Wingfield J.C., Astheimer L.B., Buttemer W.A. Temporal patterns of territorial behavior and circulating testosterone in the Lapland longspur and other arctic passerines. American Zoologist 1995, 35:274-284.
23. Hunt K.E., Hahn T.P., Wingfield J.C. Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus). Behavioral Ecology and Sociobiology 1999, 45:360-369.
24. Ketterson E.D., Nolan V., Wolf L., Ziegenfus C., Dufty A.M., Ball G.F., Johnson T.S. Testosterone and avian life histories: the effect of experimentally elevated testosterone on corticosterone and body mass in male Dark-eyed Juncos (Junco hyemalis). Hormones and Behavior 1991, 25:489-503.
25. Ketterson E.D., Nolan V. Hormones and avian life histories: an integrative approach. American Naturalist 1992, 140:S33-S62.
26. Ketterson E.D., Nolan V., Wolf L., Ziegenfus C. Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). American Naturalist 1992, 140:980-999.
27. Ketterson E.D., Nolan V. Adaptation, exaptation, and constraint: a hormonal perspective. American Naturalist 1999, 154:S4-S25.
28. Langin, K.M., Sillett, T.S., Yoon, J., Sofaer, H.R., Morrison, S.A., Ghalambor, C.K., 2009. Reproductive consequences of an extreme drought for orange-crowned warblers on Santa Catalina and Santa Cruz Islands. Proceedings of the 7th California Islands Symposium.
29. Levy D.J., Stiles F.G. Evolutionary precursors of long-distance migration: Resource availability and movement patterns in neotropical landbirds. American Naturalist 1992, 140:447-476.
30. Lynn A.M., Houtman W.W., Weathers E.D., Ketterson V., Nolan Jr. Testosterone increases activity but not daily energy expenditure in captive male dark-eyed juncos. Animal Behaviour 2000, 60:581-587.
31. Lynn S.E., Hayward L.S., Benowitz-Fredericks Z.M., Wingfield J.C. Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur, Calcarius ornatus. Animal Behaviour 2002, 63:795-803.
32. Lynn S.E., Walker B.G., Wingfield J.C. A phylogenetically controlled test for hypotheses for behavioral insensitivity to testosterone in birds. Hormones and Behavior 2005, 47:170-177.
33. Lynn S.E. Behavioral insensitivity to testosterone: why and how does testosterone alter paternal behavior and aggressive behavior in some avian species but not others?. General and Comparative Endocrinology 2008, 157:233-240.
34. Martin L.B., Weil Z.M., Nelson R.J. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Tractions of the Royal Society B 2008, 363:321-339.
35. Meddle S.L., Romero L.M., Astheimer L.B., Buttemer W.A., Moore I.T., Wingfield J.C. Steroid hormone interrelationships with territorial aggression in an arctic-breeding songbird, Gambel's white-crowned sparrow, Zonotrichia leucophrys gambelii. Hormones and Behavior 2002, 42:212-221.
36. McGlothlin J.W., Jawor J.M., Ketterson E.D. Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist 2007, 170:864-875.
37. Moore M.C. Hormonal responses of free-living male white-crowned sparrows to experimental manipulation of female sexual behavior. Hormones and Behavior 1982, 16:323-329.
38. Moore M.C. Effect of female sexual displays on the endocrine physiology and behavior of male white crowned sparrows, Zonotrichia leucophrys gambelii. Journal of Zoology, London 1983, 199:137-148.
39. Moore M.C. Changes in territorial defense produced by changes in circulation levels of testosterone: a possible hormonal basis for mate-guarding behavior in white-crowned sparrows. Behaviour 1984, 88:215-226.
40. Moore I.T., Lerner J.P., Lerner D.T., Moore R.T. Relationships between annual cycles of testosterone, corticosterone, and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus. Physiological and Biochemical Zoology 2000, 73:307-312.
41. Moore I.T., Perfito N., Wada H., Sperry T.S., Wingfield J.C. Latitudinal variation in plasma testosterone levels in birds of the genus Zonotrichia. General and Comparative Endocrinology 2002, 129:13-19.
42. Moore I.T., Wada H., Perfito N., Busch D.S., Hahn T.P., Wingfield J.C. Territoriality and testosterone in an equatorial population of rufous-collared sparrow, Zonotrichia capensis. Animal Behaviour 2004, 67:411-420.
43. Moss R., Parr R., Lambin X. Effects of testosterone on breeding density, breeding success and survival of red grouse. Proceedings of the Royal Society B 1994, 258:175-180.
44. Nolan V., Ketterson E.D., Ziegenfus C., Cullen D.P., Chandler C.R. Testosterone and avian life histories: effects of experimentally elevated testosterone on prebasic molt and survival in male dark-eyed juncos. Condor 1992, 94:364-370.
45. Owen-Ashley N.T., Hasselqueist D., Wingfield J.C. Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. American Naturalist 2004, 164:490-505.
46. Parisot M., Tanvez A., Lacroix A., Vallet E., Béguin N., Leboucher G. Social competition and plasma testosterone profile in domesticated canaries: an experimental test of the challenge hypothesis. Hormones and Behavior 2005, 48:225-232.
47. Peluc S.I., Sillett T.S., Rotenberry J.T., Ghalambor C.K. Adaptive phenotypic plasticity in an island songbird exposed to a novel predation risk. Behavioral Ecology 2008, 19:830-835.
48. Peters A., Cockburn A., Cunningham R. Testosterone treatment suppresses paternal care in superb fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship. Behavioral Ecology and Sociobiology 2002, 51:538-547.
49. Poiani A., Goldsmith A.R., Evans M.R. Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetance handicap hypothesis and a new model. Behavioral Ecology and Sociobiology 2000, 47:230-242.
50. Raouf S.A., Parker P.G., Ketterson E.D., Nolan V., Ziegenfus C. Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis). Proceedings of the Royal Society B 1997, 264:1599-1603.
51. Redpath S.M., Mougeot F., Leckie F.M., Evans S.A. The effects of autumn testosterone on survival and productivity in red grouse, Lagopus lagopus scoticus. Animal Behaviour 2006, 71:1297-1305.
52. Reed W.L., Clark M.E., Parker P.G., Raouf S.A., Arguedas N., Monk D.S., Snajdr E., Nolan V., Ketterson E.D. Physiological effects on demography: a long-term experimental study of testosterone's effects on fitness. American Naturalist 2006, 167:667-683.
53. Ricklefs R.E., Wikelski M. The physiology/life-history nexus. Trends in Ecology and Evolution 2002, 17:462-468.
54. Roberts M.L., Buchanan K.L., Evans M.R. Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behaviour 2004, 68:227-239.
55. Roff D.A. Life history evolution 2002, Sinauer Associates, Sunderland, MA.
56. Romero L.M., Soma K.K., O'Reilly K.M., Suydam R., Wingfield J.C. Hormones and territorial behavior during breeding in snow buntings Plectrophenax nivalis: an arctic-breeding songbird. Hormones and Behavior 1998, 33:40-47.
57. Runfeldt S., Wingfield J.C. Experimentally prolonged sexual activity in female sparrows delays termination of reproductive activity in their untreated mates. Animal Behaviour 1985, 33:403-410.
58. Saino N., Møller A.P. Testosterone-induced depression of male parental behavior in the barn swallow: female compensation and effects on seasonal fitness. Behavioral Ecology and Sociobiology 1995, 33:151-157.
59. Sheldon B.C., Verhulst S. Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution. 1996, 11:317-321.
60. Silverin B. Effects of a long-acting testosterone treatment on free-living pied flycatchers, Ficedula hypoleuca. Animal Behaviour 1980, 28:906-912.
61. Sinervo B., Svensson E. Mechanistic and selective causes of life history trade-offs and plasticity. Oikos 1998, 83:432-442.
62. Sogge M.K., Gilbert W.M., Riper C.v. Orange-crowned Warbler (Vermivora celata). The Birds of North America, No. 101 1994, Academy of Natural Sciences, Philadelphia, and American Ornithologists' Union, Washington, DC. A. Poole, F. Gill (Eds.).
63. Stearns S. The evolution of life histories 1992, Oxford University Press, Oxford.
64. Van Duyse E., Pinxten R., Eens M. Does testosterone affect the trade-off between investment in sexual/territorial behaviour and parental care in male great tits?. Behaviour 2000, 137:1503-1515.
65. Van Duyse E., Pinxten R., Eens M. Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major. Hormones and Behavior 2002, 41:178-186.
66. Van Roo B.L., Ketterson E.D., Sharp P.J. Testosterone and prolactin in two songbirds that differ in paternal care: the blue-headed vireo and the red-eyed vireo. Hormones and Behavior 2003, 44:435-441.
67. White G.C., Burnham K.P. Program MARK: survival estimation from populations of marked animals. Bird Study 1999, (Suppl. 46):120-138.
68. Wingfield J.C. Androgens and mating systems: testosterone-induced polygyny in normally monogamous birds. Auk 1984, 101:665-671.
69. Wingfield J.C., Hegner R.E., Dufty A.M., Ball G.E. The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist 1990, 136:829-846.
70. Wingfield J.C., Hegner R.E., Lewis D. Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. Journal of Zoology, London 1991, 225:43-48.
71. Wingfield J.C., Hahn T.P. Testosterone and territorial behaviour in sedentary and migratory sparrows. Animal Behaviour 1994, 47:77-89.
72. Wingfield J.C., Jacobs J.D., Tramontin A.D., Perfito N., Meddle S., Maney D.L., Soma K. Toward and ecological basis of hormone-behavior interactions in reproduction of birds. Reproduction in Context 2000, 85-128. MIT Press, Cambridge. K. Wallen, J. Schneider (Eds.).
73. Wingfield J.C., Lynn S.E., Soma K.K. Avoiding the 'costs' of testosterone: ecological bases of hormone-behavior interactions. Brain, Behavior and Evolution 2001, 57:239-251.
74. Zera A.J., Harshman L.G. The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics 2001, 32:95-126.