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Journal of Ornithology

, Volume 158, Issue 1, pp 203–212 | Cite as

Overlapping life-history stages in migrating songbirds: variation in circulating testosterone and testosterone production capacity

  • Kristen M. CovinoEmail author
  • Jodie M. Jawor
  • Jeffrey F. Kelly
  • Frank R. Moore
Original Article

Abstract

Understanding the extent of overlap between life-history stages is fundamental to understanding full-life cycle biology, especially for migratory species. Testosterone levels vary throughout the annual cycle in seasonally reproducing vertebrates. In migratory songbirds, testosterone increases associated with breeding preparation may overlap with the vernal migratory period; however, this overlap remains largely unexplored. We test the hypothesis that both circulating testosterone and the capacity to elevate testosterone increases throughout vernal migration in long-distance songbird migrants. Here we relate testosterone in songbirds sampled en route with the stable hydrogen isotope ratios in their feathers as a metric of breeding ground proximity. We determined the capacity to elevate testosterone using field gonadotropin-releasing hormone bioassays and related this to feather hydrogen ratios as well. Males that were closer to their breeding grounds had higher circulating testosterone, whereas there was no relationship between testosterone and breeding ground proximity in females. Similarly, while capacity to elevate testosterone was not related to breeding ground proximity in female migrants, this capacity was greater in males closer to their breeding grounds than those further away. These results reveal that male migrants prepare for breeding during their vernal migration, whereas the schedule for breeding preparation among females is less clear and may be more complex.

Keywords

Breeding preparation Vernal migration Testosterone Gonadotropin-releasing hormone bioassay 

Zusammenfassung

Überlappende Lebenszyklusstadien bei ziehenden Singvögeln: Variation im zirkulierenden Testosteron und in der Synthesekapazität für Testosteron Zu verstehen, in welchem Maße Lebenszyklusstadien überlappen, ist fundamental für ein Verständnis der Biologie des kompletten Lebenszyklus, und zwar besonders bei ziehenden Arten. Bei saisonal reproduzierenden Wirbeltieren variiert der Testosteronspiegel im Verlauf des Jahres. Bei ziehenden Singvögeln kann ein mit der Brutvorbereitung verbundener Anstieg des Testosteronspiegels mit dem Frühjahrszug überlappen, doch diese Überlappung ist bisher weitgehend unerforscht. Wir testeten die Hypothese, dass sowohl das im Blut zirkulierende Testosteron als auch die Kapazität, den Testosteronspiegel zu erhöhen, bei langstreckenziehenden Singvögeln auf dem Frühjahrszug ansteigen. Hierfür setzten wir die bei Singvögeln auf dem Zug gemessenen Testosteronspiegel in Beziehung zum stabilen Wasserstoffisotopenverhältnis in ihren Federn, welches als Maß für die Nähe zum Brutgebiet dient. Die Kapazität, den Testosteronspiegel zu erhöhen, haben wir ermittelt, indem wir im Freiland Gonadoliberin-Biotests durchgeführt haben. Diese Kapazität haben wir dann ebenfalls zu den Wasserstoffisotopenverhältnissen in den Federn in Beziehung gesetzt. Näher am Brutgebiet befindliche Männchen wiesen höheres zirkulierendes Testosteron auf, wohingegen bei Weibchen kein Zusammenhang zwischen Testosteron und der Nähe zum Brutgebiet bestand. Gleichermaßen hing die Kapazität, den Testosteronspiegel zu erhöhen, bei ziehenden Weibchen nicht mit der Nähe zum Brutgebiet zusammen, während sie bei näher am Brutgebiet befindlichen Männchen höher war als bei weiter vom Brutgebiet entfernten Männchen. Diese Ergebnisse zeigen, dass männliche Zugvögel sich bereits auf dem Frühjahrszug auf die Brut vorbereiten, während der Zeitplan der Brutvorbereitung bei Weibchen weniger klar und möglicherweise komplexer ist.

Notes

Acknowledgements

We thank the Migratory Bird Research Group and field technicians for their assistance with the field work. We also thank Sarah Engel and Sandra Pletschet for their work on the isotope sample preparation. Funding was provided by the Louisiana Ornithological Society, Eastern Bird Banding Association, Inland Bird Banding Association, and a National Science Foundation GK12 fellowship to K.M.C. (#0947944). Financial support was also provided via startup funds from the University of Southern Mississippi to J.M.J., from a basic research account at the University of Southern Mississippi under F.R.M., and through a National Science Foundation grant (EF-1340921) to J.F.K. All applicable institutional and/or national guidelines for the care and use of animals were followed.

References

  1. Adkins-Regan E (2005) Hormones and animal social behavior. Princeton University Press, PrincetonGoogle Scholar
  2. Angelier F, Tonra CM, Holberton RL, Marra PP (2010) How to capture wild passerine species to study baseline corticosterone levels. J Ornithol 151:415–422. doi: 10.1007/s10336-009-0471-6 CrossRefGoogle Scholar
  3. Ball GF, Ketterson ED (2008) Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos Trans R Soc Lond B Biol Sci 363:231–246. doi: 10.1098/rstb.2007.2137 CrossRefPubMedGoogle Scholar
  4. Bates D (2010) lmr4: mixed effects modeling with R. Springer, New YorkGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R Package Version 1:1–7Google Scholar
  6. Bauchinger U, Wohlmann A, Biebach H (2005) Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin). Zoology 108:97–106. doi: 10.1016/j.zool.2005.03.003 CrossRefPubMedGoogle Scholar
  7. Bauchinger U, Hof T, Biebach H (2007) Testicular development during long-distance spring migration. Horm Behav 51:295–305. doi: 10.1016/j.yhbeh.2006.10.010 CrossRefPubMedGoogle Scholar
  8. BirdLife-International and NatureServe (2014) Bird species distribution maps of the world. BirdLife International, Cambridge, UK and NatureServe, Arlington, USAGoogle Scholar
  9. Bluhm C, Schwabl H, Schwabl I et al (1991) Variation in hypothalamic gonadotrophin-releasing hormone content, plasma and pituitary LH, and in vitro testosterone release in a long-distance migratory bird, the garden warbler (Sylvia borin), under constant photoperiods. J Endocrinol 128:339–345CrossRefPubMedGoogle Scholar
  10. Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348. doi: 10.1007/s00442-004-1813-y CrossRefPubMedGoogle Scholar
  11. Busch DS, Robinson TR, Hahn TP, Wingfield JC (2008) Sex hormones in the Song Wren: variation with time of year, molt, gonadotropin releasing hormone, and social challenge. Condor 110:125–133. doi: 10.1525/cond.2008.110.1.125 CrossRefGoogle Scholar
  12. Covino KM, Morris SR, Moore FR (2015) Patterns of testosterone in three Nearctic-Neotropical migratory songbirds during spring passage. Gen Comp Endocrinol 224:186–193. doi: 10.1016/j.ygcen.2015.08.012 CrossRefPubMedGoogle Scholar
  13. Deviche P, Breuner C, Orchinik M (2001) Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. Gen Comp Endocrinol 122:67–77. doi: 10.1006/gcen.2001.7613 CrossRefPubMedGoogle Scholar
  14. DeVries MS, Holbrook AL, Winters CP, Jawor JM (2011) Non-breeding gonadal testosterone production of male and female Northern Cardinals (Cardinalis cardinalis) following GnRH challenge. Gen Comp Endocrinol 174:370–378. doi: 10.1016/j.ygcen.2011.09.016 CrossRefPubMedGoogle Scholar
  15. Farner DS, Lewis RA (1971) Photoperiodism and reproductive cycles in birds. In: Giese AC (ed) Photophysiology: current topics in photochemistry and photobiology, vol 6. Academic Press, New York, pp 325–370CrossRefGoogle Scholar
  16. Hobson KA, Wassenaar LI (1997) Linking breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 109:142–148. doi: 10.1007/s004420050068 CrossRefGoogle Scholar
  17. Hobson KA, Wassenaar LI, Bayne E (2004) Using isotopic variance to detect long-distance dispersal and philopatry in birds: an example with Ovenbirds and American Redstarts. Condor 106:732–743. doi: 10.1650/7631 CrossRefGoogle Scholar
  18. Hobson KA, Wilgenburg SL Van, Faaborg J, et al. (2014) Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity. 85, 237–257. doi: 10.1111/jofo.12065
  19. Jacobs JD, Wingfield JC (2000) Endocrine control of life-cycle stages: a constraint on response to the environment? Condor 102:35–51. doi: 10.1650/0010-5422(2000)102[0035:ECOLCS]2.0.CO;2
  20. Jawor JM, McGlothlin JW, Casto JM et al (2006) Seasonal and individual variation in response to GnRH challenge in male dark-eyed juncos (Junco hyemalis). Gen Comp Endocrinol 149:182–189. doi: 10.1016/j.ygcen.2006.05.013 CrossRefPubMedGoogle Scholar
  21. Jawor JM, Mcglothlin JW, Casto JM et al (2007) Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects. Funct Ecol 21:767–775. doi: 10.1111/j.1365-2435.2007.01280.x CrossRefGoogle Scholar
  22. Kelly JF (2006) Stable isotope evidence links breeding geography and migration timing in wood warblers (Parulidae). Auk 123:431–437. doi: 10.1642/0004-8038 CrossRefGoogle Scholar
  23. Kelly JF, Atudorei V, Sharp ZD, Finch DM (2002) Insights into Wilson’s Warbler migration from analyses of hydrogen stable-isotope ratios. Oecologia 130:216–221. doi: 10.1007/s004420100789 CrossRefGoogle Scholar
  24. Kelly JF, Ruegg KC, Smith TB (2005) Combining isotopic and genetic markers to identify breeding orising of migrant birds. Ecol Appl 15:1487–1494CrossRefGoogle Scholar
  25. King JR, Follett BK, Farner DS, Morton ML (1966) Annual gonadal cycles and pituitary gonadotropins in Zonotrichia leucophrys gambelii. Condor 68:476–487CrossRefGoogle Scholar
  26. Kricher JC (2014) Black-and-white Warbler (Mniotilta varia). In: Birds North Am. Online. http://bna.birds.cornell.edu.bnaproxy.birds.cornell.edu/bna/species/158. Accessed 20 Jan 2015
  27. Marra PP (2000) The role of behavioral dominance in structuring patterns of habitat occupancy in a migrant bird during the nonbreeding season. Behav Ecol 11:299–308CrossRefGoogle Scholar
  28. Marra PP, Cohen EB, Loss SR et al (2015) A call for full annual cycle research in animal ecology. Biol Lett. doi: 10.1098/rsbl.2015.0552 Google Scholar
  29. Morton ML (2002) The mountain white-crowned sparrow: migration and reproduction at high altitude. In: Rotenberry JT (ed) Studies in avian biology. Cooper Ornithological Society, Lawrence, KansasGoogle Scholar
  30. Morton L, Peterson LE, Burns DM (1990) Seasonal and age-related changes in plasma testosterone levels in mountain white-crowned sparrows. Condor 92:166–173CrossRefGoogle Scholar
  31. Norris DO (1997) Vertebrate endocrinology, 3rd edn. Academic Press, LondonGoogle Scholar
  32. Owen JC, Moore FR (2006) Seasonal differences in immunological condition of three species of thrushes. Condor 108:389–398CrossRefGoogle Scholar
  33. Owen JC, Garvin MC, Moore FR (2014) Elevated testosterone advances onset of migratory restlessness in a nearctic-neotropical landbird. Behav Ecol Sociobiol 68:561–569. doi: 10.1007/s00265-013-1671-x CrossRefGoogle Scholar
  34. Paritte JM, Kelly JF (2009) Effect of cleaning regime on stable-isotope ratios of feathers in Japanese quail (Coturnix japonica). Auk 126:165–174. doi: 10.1525/auk.2009.07187 CrossRefGoogle Scholar
  35. Paxton KL, Moore FR (2015) Carry-over effects of winter habitat quality on en route timing and condition of a migratory passerine during spring migration. J Avian Biol 45:001–012Google Scholar
  36. Pyle P (1997) Identification guide to North American birds: part 1. Braun-Brumfield Inc., Ann ArborGoogle Scholar
  37. Ramenofsky M (2011) Hormones in migration and reproductive cycles of birds. In: Norris D, Lopez K (eds) Hormones and reproduction in vertebrates, vol 8. Academic Press, California, USA, pp 205–236Google Scholar
  38. Ramenofsky M, Wingfield JC (2006) Behavioral and physiological conflicts in migrants: the transition between migration and breeding. J Ornithol 147:135–145. doi: 10.1007/s10336-005-0050-4 CrossRefGoogle Scholar
  39. Ramenofsky M, Savard R, Greenwood MRC (1999) Seasonal and diel transitions in physiology and behavior in the migratory dark-eyed junco. Comp Biochem Physiol Part A Mol Integr Physiol 122:385–397. doi: 10.1016/S1095-6433(99)00013-6 CrossRefGoogle Scholar
  40. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol A Mol Integr Physiol 140:73–79. doi: 10.1016/j.cbpb.2004.11.004 CrossRefPubMedGoogle Scholar
  41. Rundel CW, Wunder MB, Alvarado AH et al (2013) Novel statistical methods for integrating genetic and stable isotope data to infer individual-level migratory connectivity. Mol Ecol 22:4163–4176. doi: 10.1111/mec.12393 CrossRefPubMedGoogle Scholar
  42. Schoech SJ, Mumme RL, Wingfield JC (1996) Delayed breeding in the cooperatively breeding Florida scrub- jay (Aphelocoma coerulescens): inhibition or the absence of stimulation? Behav Ecol Sociobiol 39:77–90. doi: 10.1007/s002650050269 CrossRefGoogle Scholar
  43. Schwabl H, Farner DS (1989a) Dependency on testosterone of photoperiodically-induced vernal fat deposition in female white-crowned sparrows. Condor 91:108–112CrossRefGoogle Scholar
  44. Schwabl H, Farner DS (1989b) Endocrine and environmental control of vernal migration in male white-crowned sparrows, Zonotrichia leucophrys gambelii. Physiol Zool 62:1–10CrossRefGoogle Scholar
  45. Staub NL, De Beer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108:1–24. doi: 10.1006/gcen.1997.6962 CrossRefPubMedGoogle Scholar
  46. Studds CE, Kyser TK, Marra PP (2008) Natal dispersal driven by environmental conditions interacting across the annual cycle of a migratory songbird. Proc Natl Acad Sci U S A 105:2929–2933. doi: 10.1073/pnas.0710732105 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Swett MB, Breuner CW (2008) Interaction of testosterone, corticosterone and corticosterone binding globulin in the white-throated sparrow (Zonotrichia albicollis). Comp Biochem Physiol A Mol Integr Physiol 151:226–231. doi: 10.1016/j.cbpa.2008.06.031 CrossRefPubMedGoogle Scholar
  48. Tonra CM, Marra PP, Holberton RL (2011a) Early elevation of testosterone advances migratory preparation in a songbird. J Exp Biol 214:2761–2767. doi: 10.1242/jeb.054734 CrossRefPubMedGoogle Scholar
  49. Tonra CM, Marra PP, Holberton RL (2011b) Migration phenology and winter habitat quality are related to circulating androgen in a long-distance migratory bird. J Avian Biol 42:397–404. doi: 10.1111/j.1600-048X.2011.05333.x CrossRefGoogle Scholar
  50. Tonra CM, Marra PP, Holberton RL (2013) Experimental and observational studies of seasonal interactions between overlapping life history stages in a migratory bird. Horm Behav 64:825–832. doi: 10.1016/j.yhbeh.2013.10.004 CrossRefPubMedGoogle Scholar
  51. Wassenaar LI, Hobson KA (2003) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Health Stud 39:211–217. doi: 10.1080/1025601031000096781 CrossRefGoogle Scholar
  52. Wikelski M, Lynn S, Breuner JC et al (1999) Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J Comp Physiol A Sensory Neural Behav Physiol 185:463–470. doi: 10.1007/s003590050407 CrossRefGoogle Scholar
  53. Wingfield JC, Farner DS (1978a) The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Biol Reprod 19:1046–1056CrossRefPubMedGoogle Scholar
  54. Wingfield JC, Farner DS (1978b) The endocrinology of a natural breeding population of the White-crowned Sparrow (Zonotrichia leucophrys pugetensis). Physiol Zool 51:188–205CrossRefGoogle Scholar
  55. Wingfield JC, Crim JW, Mattocks PWJ, Farner DS (1979) Responses of photosensitive and photorefractory male white-crowned sparrows (Zonotrichia leucophrys gambelii) to synthetic mammalian luteinizing hormone releasing hormone (Syn-LHRH). Biol Reprod 21:801–806CrossRefPubMedGoogle Scholar
  56. Wingfield JC, Hahn TP, Wada M, Schoech SJ (1997) Effects of day length and temperature on gonadal development, body mass, and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis. Gen Comp Endocrinol 107:44–62. doi: 10.1006/gcen.1997.6894 CrossRefPubMedGoogle Scholar
  57. Wingfield JC, Lynn SE, Soma KK (2001) Avoiding the “costs” of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Evol 57:239–251. doi: 10.1159/000047243 CrossRefPubMedGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2016

Authors and Affiliations

  • Kristen M. Covino
    • 1
    • 2
    Email author
  • Jodie M. Jawor
    • 3
  • Jeffrey F. Kelly
    • 4
  • Frank R. Moore
    • 1
  1. 1.Department of Biological SciencesUniversity of Southern MississippiHattiesburgUSA
  2. 2.Biology DepartmentCanisius CollegeBuffaloUSA
  3. 3.Department of BiologyNew Mexico State UniversityLas CrucesUSA
  4. 4.Oklahoma Biological Survey and Department of BiologyUniversity of OklahomaNormanUSA

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