Experimental and observational studies of seasonal interactions between overlapping life history stages in a migratory bird

Hormones and Behavior

Volumn 64, Issue 5, 2013, Pages 825-832

  Tonra, Christopher M ^a,b   Marra, Peter P ^b   Holberton, Rebecca L ^a  

^a UNIVERSITY OF MAINE   (United States)

^b SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

Author keywords

American redstart; Carry over effects; Departure timing; Migration; Setophaga ruticilla; Testosterone

Indexed keywords

ANDROGEN; TESTOSTERONE;

ANDROGEN BLOOD LEVEL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BIRD; BREEDING; BREEDING SUCCESS; CONTROLLED STUDY; ENERGY TRANSFER; EXPERIMENTAL STUDY; FIELD EXPERIMENT; LIFE HISTORY; MALE; MIGRATORY SPECIES; NONHUMAN; OBSERVATIONAL STUDY; PHENOLOGY; POPULATION MIGRATION; PRIORITY JOURNAL; REPRODUCTIVE SUCCESS; SEASONAL VARIATION; SETOPHAGA RUTICILLA; SEX HORMONE DETERMINATION;

AMERICAN REDSTART; CARRY-OVER EFFECTS; DEPARTURE TIMING; MIGRATION; SETOPHAGA RUTICILLA; TESTOSTERONE;

AGE FACTORS; ANDROGENS; ANIMAL EXPERIMENTATION; ANIMAL MIGRATION; ANIMALS; BEHAVIOR, ANIMAL; DRUG IMPLANTS; ECOSYSTEM; ENERGY METABOLISM; FEMALE; MALE; PASSERIFORMES; REPRODUCTION; SEASONS; SEXUAL MATURATION; TESTOSTERONE;

EID: 84887201977     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.10.004     Document Type: Article

References (67)

1. Ardia D.R., Broughton D.R., Gleicher M.J. Short-term exposure to testosterone propionate leads to rapid bill color and dominance changes in zebra finches. Horm. Behav. 2010, 58:526-532.
2. Bauchinger U., Van't Hof T., Biebach H. Testicular development during long-distance migration. Horm. Behav. 2007, 51:295-305.
3. Bauchinger U., Van't Hof T., Biebach H. Migratory stopover conditions affect the developmental state of male gonads in garden warblers (Sylvia borin). Horm. Behav. 2008, 54:312-318.
4. Bauchinger U., Van't Hof T., Biebach H. Food availability during migratory stopover affects testis growth and reproductive behavior in a migratory passerine. Horm. Behav. 2009, 55:425-433.
5. Blâs J., Perez-Rodriguez L., Bortolotti G.R., Vinuela J., Marchant T.A. Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc. Natl. Acad. Sci. U. S. A. 2007, 103:18633-18637.
6. Both C., Visser M.E. Adjustment to climate change is constrained by arrival date in a long-distance migratory bird. Nature 2001, 411:296-298.
7. Deviche P.E. Androgen regulation of avian premigratory hyperphagia and fattening: from eco-physiology to neuroendocrinology. Am. Zool. 1995, 35:234-245.
8. Drent R.H., Daan S. The prudent parent: energetic adjustments in avian breeding. Ardea 1980, 68:225-252.
9. Fennell M.J., Scanes C.G. Effects of androgen (testosterone, 5-alpha-dihydrotestosterone, 19-nortestosterone) administration on growth in turkeys. Poult. Sci. 1992, 71:539-547.
10. Fusani L. Testosterone control of male courtship in birds. Horm. Behav. 2008, 54:227-233.
11. Gardner T.J., Naef F., Nottebohm F. Freedom and rules: the acquisition and reprogramming of a bird's learned song. Science 2005, 308:1046-1049.
12. Gunnarsson T.G., Gill J.A., Newton J., Potts P.M., Sutherland W.J. Seasonal matching of habitat quality and fitness in a migratory bird. Proc. Roy. Soc. London B 2005, 272:2319-2323.
13. Gunnarsson T.G., Gill J.A., Atkinson P.W., Gélinaud G., Potts P.M., Croger R.E., Gudmundsson G.A., Appleton G.F., Sutherland W.J. Population-scale drivers of individual arrival times in migratory birds. J. Anim. Ecol. 2006, 75:1119-1127.
14. Gwinner E., Rödl T., Schwabl H. Pair territoriality of wintering stonechats: behaviour, function, and hormones. Behav. Ecol. Sociobiol. 1994, 34:321-327.
15. Hasselquist D., Marsh J.A., Sherman P.W., Wingfield J.C. Is avian humoral immunocompetence suppressed by testosterone?. Behav. Ecol. Sociobiol. 1999, 45:167-175.
16. Hobson K.A., Wassenaar L.I. Linking breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 1997, 109:142-148.
17. Holberton R.L., Dufty A.M. Hormones and variation in life history strategies of migratory and nonmigratory birds. Birds of Two Worlds: The Ecology and Evolution of Temperate-Tropical Migration Systems 2005, 291-302. Johns Hopkins University Press, Baltimore. R. Greenberg, P.P. Marra (Eds.).
18. Holberton R.L., Wilson C.M., Hunter M.J., Cash W.B., Sims C.G. The role of corticosterone in supporting migratory lipogenesis in the Dark-eyed Junco, Junco hyemalis: a model for central and peripheral regulation. Physiol. Biochem. Zool. 2007, 80:125-137.
19. 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). Behav. Ecol. Sociobiol. 1999, 45:360-369.
20. Ketterson E.D., Nolan V., Wolf L., Zeigenfus C. Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am. Nat. 1992, 140:980-999.
21. Landys M.M., Ramenofsky M., Wingfield J.C. Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocrinol. 2006, 148:132-149.
22. Langin K.M., Norris D.R., Kyser T.K., Marra P.P., Ratcliffe L.M. Capital versus income breeding in a migratory passerine bird: evidence from stable-carbon isotopes. Can. J. Zool. 2006, 84:947-953.
23. Lynn S.E., Prince L.E., Schook D.M., Moore I.T. Supplementary testosterone inhibits parental care in a tropically breeding sparrow, Zonotrichia capensis. Physiol. Biochem. Zool. 2009, 82:699-708.
24. Marra P.P. The role of behavioral dominance in structuring patterns of habitat occupancy in a migrant bird during the non-breeding period. Behav. Ecol. 2000, 11:299-308.
25. Marra P.P., Holmes R.T. Consequences of dominance-mediated habitat segregation in American redstarts during the nonbreeding season. Auk 2001, 118:92-104.
26. Marra P.P., Hobson K.A., Holmes R.T. Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 1998, 282:1884-1886.
27. Marra P.P., Francis C.M., Mulvihill R.S., Moore F.R. The influence of climate on the timing of migration events. Oecologia 2005, 142:307-315.
28. 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 sparrows, Zonotrichia capensis. Anim. Behav. 2004, 67:411-420.
29. Morbey Y.E., Ydenberg C. Protandrous arrival to breeding areas: a review. Ecol. Lett. 2001, 4:663-673.
30. Morton M.L. Hematocrits in montane sparrows in relation to reproductive schedule. Condor 1994, 96:119-126.
31. Morton M.L. The Mountain White-crowned Sparrow: migration and reproduction at high altitude. Stud. Avian Biol. 2002, 24:1-236.
32. Morton M.L., Peterson L.E., Burns D.M., Allen N. Seasonal and age-related changes in plasma testosterone levels in Mountain White-crowned Sparrows. Condor 1990, 92:166-173.
33. Neelin J.D., Munnich M., Su H., Meyerson J.E., Holloway C.E. Tropical drying trends in global warming models and observations. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6110-6115.
34. O'Neal D.M., Reichard D.G., Pavilis K., Ketterson E.D. Experimentally elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed Junco (Junco hyemalis). Horm. Behav. 2008, 54:571-578.
35. Parmesan C., Yohe G. A globally coherent fingerprint of climate change impacts on natural systems. Nature 2003, 421:37-42.
36. Pyle P. Identification Guide to North American Birds: Part 1 1997, Slate Creek Press, Bolinas, CA.
37. R Core Development Team R: A Language and Environment for Statistical Computing 1999, R Foundation for Statistical Computing, Vienna.
38. Ramenofsky M., Wingfield J.C. Behavioural and physiological conflicts in migrants: the transition between migration and breeding. J. Ornithol. 2006, 147:135-145.
39. Reudink M.W., Marra P.P., Kyser T.K., Boag P.T., Langin K.M., Ratcliffe L. Non-breeding season events influence sexual selection in a long-distance migratory bird. Proc. Roy. Soc. London B 2009, 276:1619-1626.
40. Ricklefs R.E., Wikelski M. The physiology/life-history nexus. Trends Ecol. Evol. 2002, 17:462-468.
41. Runge M., Marra P.P. Modeling seasonal interactions in the annual cycle of migratory birds. Birds of Two Worlds: The Ecology and Evolution of Temperate-Tropical Migration Systems 2005, 375-389. Johns Hopkins University Press, Baltimore. R. Greenberg, P.P. Marra (Eds.).
42. Schulte-Hostedde A.I., Millar J.S., Hickling G.J. Restitution of mass-size residuals: validating body condition indices. Ecology 2005, 86:155-163.
43. Schwabl H., Farner D.S. Dependency on testosterone of photoperiodically-induced vernal fat deposition in female white-crowned sparrows. Condor 1989, 91:108-112.
44. Schwabl H., Farner D.S. Endocrine and environmental control of vernal migration in male white-crowned sparrows, Zonotrichia leucophrys gambelii. Physiol. Zool. 1989, 62:1-10.
45. Senner N.R. One species but two patterns: populations of the Hudsonian Godwit (Limosa haemastica) differ in spring migration timing. Auk 2012, 129:670-682.
46. Sherry T.W., Holmes R.T. American redstart (Setophaga ruticilla). Birds of North America 1997, vol. 277. The Academy of Natural Sciences of Philadelphia and the American Ornithologists' Union, Philadelphia. A. Poole, F. Gill (Eds.).
47. Smith R.J., Moore F.R. Arrival timing and seasonal reproductive performance in a long-distance migratory bird. Behav. Ecol. Sociobiol. 2005, 57:231-239.
48. Soma K.K., Hartman V.N., Wingfield J.C., Brenowitz E.A. Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird. J. Comp. Neurol. 1999, 409:224-236.
49. SPSS SPSS for Windows, Version 17.0 2008, SPSS Inst., Chicago.
50. Stenseth N.C., Mysterud A. Climate, changing phenology, and other life history and traits: nonlinearity and match-mismatch to the environment. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13379-13381.
51. Stephens P.A., Boyd I.L., McNamara J.M., Houston A.I. Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 2009, 90:2057-2067.
52. Studds C.E., Marra P.P. Nonbreeding habitat occupancy and population processes: an upgrade removal experiment with a migratory bird. Ecology 2005, 86:2380-2385.
53. Studds C.E., Marra P.P. Linking fluctuations in rainfall to nonbreeding season performance in a long-distance migratory bird, Setophaga ruticilla. Clim. Res. 2007, 35:115-132.
54. Studds C.E., Marra P.P. Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proc. Roy. Soc. London B. 2011, 278:3437-3443.
55. Studds C.E., Kyser T.K., Marra P.P. Natal dispersal driven by environmental conditions interacting across the annual cycle of a migratory songbird. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2929-2933.
56. Tonra C.M., Marra P.P., Holberton R.L. Migration phenology and winter habitat quality are related to circulating androgen in a long-distance migratory bird. J. Avian Biol. 2011, 42:397-404.
57. Tonra C.M., Marra P.P., Holberton R.L. Early elevation of testosterone advances migratory preparation in a songbird. J. Exp. Biol. 2011, 214:2761-2767.
58. van Meir V., Verhoye M., Absil P., Eens M., Balthazart J., van der Linden A. Differential effects of testosterone on neuronal populations and their connections in a sensorimotor brain nucleus controlling song production in songbirds: a manganese enhanced-magnetic resonance imaging study. Neuroimage 2004, 21:914-923.
59. Viau V. Functional cross-talk between the hypothalamic-pituitary-gonadal and adrenal axes. J. Neuroendocrinol. 2002, 14:506-513.
60. Walther G.R., Post E., Convey P., Menzel A., et al. Ecological responses to recent climate change. Nature 2002, 416:389-395.
61. Wikelski M., Lynn S.E., Breuner C., Wingfield J.C., Kenagy G.J. Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J. Comp. Physiol. A 1999, 5:463-470.
62. Wingfield J.C. Organization of vertebrate annual cycles: implications for control mechanisms. Phil. Trans. R. Soc. B 2008, 363:425-441.
63. Wingfield J.C., Farner D.S. The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Biol. Reprod. 1978, 19:1046-1056.
64. Wingfield J.C., Farner D.S. Endocrinology of reproduction in wild species. Avian Biology 1993, 163-327. Academic Press, New York. D.S. Farner, J.R. King, K.C. Parkes (Eds.).
65. Wingfield J.C., Hahn T.P., Levin R., Honey P. Environmental predictability and control of gonadal cycles in birds. J. Exp. Zool. 1992, 261:214-231.
66. Wingfield J.C., Vleck C.M., Moore M.C. Seasonal changes in the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool. 1992, 264:419-428.
67. Zurr A.F., Ieno E.N., Walker N.J., Saveliev A.A., Smith G.M. Mixed Effects Models and Extensions in Ecology with R 2009, Springer Press, New York.