Endocrine mechanisms controlling the migratory disposition in birds

A.L. Tsvey

Proceedings of the Zoological Institute RAS, 2023, 327(4): 683–718 · https://doi.org/10.31610/trudyzin/2023.327.4.683

Full text

Abstract

On Earth, billions of birds make seasonal migrations every year. Some species fly thousands of kilometers, overcoming seas, mountains and deserts on their way. For migration to be successful, birds must have perfect mechanisms for controlling its beginning, duration and termination. On the way, birds have to make many decisions: how much in energy reserves to accumulate; when to depart, how long and in which direction to fly; how to select optimal weather conditions for flight; and, finally, when and where to terminate migration. Prior to migration, birds develop a migratory disposition – a suite of changes in physiology and behavior (e.g. migratory fattening and expression of nocturnal migratory activity) which are typical for this important life-history stage. Such physiological changes and migratory behavior are the subject of hormonal regulation. The central structure that controls activity of various hormonal systems and development of migratory disposition is the hypothalamic-pituitary system. The hypothalamus controls the secretion of regulatory hormones by the pituitary gland and these hormones, in turn, regulate the activity of downstream endocrine glands. It has been established that spring migratory disposition is triggered by an increasing photoperiod, which stimulates the production of testosterone, prolactin and modulates the signaling of thyroid hormones. In contrast, it is practically unknown how autumn migratory disposition develops when the photoperiod decreases and does not stimulate release of the abovementioned hormones. While in migratory disposition, the endocrine control of behavior on the smaller temporal scales (for example, the level of fuel accumulation, or decision to depart from a migratory stopover) is associated with the combined action of melatonin, corticosterone, insulin, glucagon, adipokines, and other hormones and neurotransmitters. In this review, I will describe the role of these hormones in the control of migratory traits, highlight the existing inconsistencies, and present possible ways to progress in this area of research. A knowledge of endocrine regulation of migratory behavior will help to predict the limits of species adaptability, explain current population trends, and inform conservation actions, which is especially important in the light of modern climate change and anthropogenic transformation of landscapes.

Key words

passerines, hyperphagia, hypothalamopituitary system, ghrelin, fattening, corticosterone, Zugunruhe, stopovers, migration, neuropeptides, flight, sex hormones, prolactin, thyroid hormones, photoperiod

Submitted June 29, 2023 · Accepted November 17, 2023 · Published December 25, 2023

References

Ahima R.S. 2006. Adipose Tissue as an Endocrine Organ. Obesity, 14(S8): 242S–249S. https://doi.org/10.1038/oby.2006.317

Åkesson S., Bakam H., Martinez Hernandez E., Ilieva M. and Bianco G. 2021. Migratory orientation in inexperienced and experienced avian migrants. Ethology Ecology and Evolution, 33(3): 206–229. https://doi.org/10.1080/03949370.2021.1905076

Åkesson S. and Helm B. 2020. Endogenous Programs and Flexibility in Bird Migration. Frontiers in Ecology and Evolution, 8: 78. https://doi.org/10.3389/fevo.2020.00078

Alerstam T. 1993. Bird migration. Cambridge University Press, 420 p.

Alerstam T. 2011. Optimal bird migration revisited. Journal of Ornithology, 152(S1): 5–23. https://doi.org/10.1007/s10336-011-0694-1

Alerstam T. and Lindström Å. 1990. Optimal bird migration: the relative importance of time, energy, and safety. In: E. Gwinner (Ed.). Bird migration: physiology and ecophysiology. Springer, Berlin, Heidelberg, New-York: 331–351. https://doi.org/10.1007/978-3-642-74542-3_22

Astheimer L.B., Buttemer W.A. and Wingfield J.C. 1992. Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scandinavica, 23: 355–365. https://doi.org/10.2307/3676661

Bäckman J., Andersson A., Alerstam T., Pedersen L., Sjöberg S., Thorup K. and Tøttrup A.P. 2016. Activity and migratory flights of individual free-flying songbirds throughout the annual cycle: method and first case study. Journal of Avian Biology, 48(2): 309–319. https://doi.org/10.1111/jav.01068

Bäckman J., Andersson A., Pedersen L., Sjöberg S., Tøttrup A.P. and Alerstam T. 2017. Actogram analysis of free-flying migratory birds: new perspectives based on acceleration logging. Journal of Comparative Physiology A, 203: 543–564. https://doi.org/10.1007/s00359-017-1165-9

Bairlein F. 2002. How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften, 89(1): 1–10. https://doi.org/10.1007/s00114-001-0279-6

Bairlein F., Dierschke V., Delingat J., Eikenaar C., Maggini I., Bulte M. and Schmaljohann H. 2013. Revealing the control of migratory fueling: An integrated approach combining laboratory and field studies in northern wheatears Oenanthe oenanthe. Current Zoology, 59(3): 381–392. https://doi.org/10.1093/czoolo/59.3.381

Bartell P.A. and Gwinner E. 2005. A separate circadian oscillator controls nocturnal migratory restlessness in the songbird Sylvia borin. Journal of Biological Rhythms, 20(6): 538–549. https://doi.org/10.1177/0748730405281826

Bauer C.M. and Watts H.E. 2021. Corticosterone's roles in avian migration: Assessment of three hypotheses. Hormones and Behavior, 135: 105033. https://doi.org/10.1016/j.yhbeh.2021.105033

Beck M.L., Davies S., Moore I.T., Schoenle L.A., Kerman K., Vernasco B.J. and Sewall K.B. 2016. Beeswax corticosterone implants produce long-term elevation of plasma corticosterone and influence condition. General and Comparative Endocrinology, 233: 109–114. https://doi.org/10.1016/j.ygcen.2016.05.021

Bernardi O., Estienne A., Reverchon M., Bigot Y., Froment P. and Dupont J. 2021. Adipokines in metabolic and reproductive functions in birds: An overview of current knowns and unknowns. Molecular and Cellular Endocrinology, 534: 111370. https://doi.org/10.1016/j.mce.2021.111370

Berthold P. 1975. Migration: control and metabolic physiology. In: D.S. Farner and J.R. King (Eds). Avian Biology. Academic Press, New York: 77–128. https://doi.org/10.1016/B978-0-12-249405-5.50010-0

Berthold P. 1996. Control of bird migration, Academic Press edn. Academic Press, London, UK, 355 p.

Berthold P. and Querner U. 1981. Genetic basis of migratory behavior in European warblers. Science, 212: 77–79. https://doi.org/10.1126/science.212.4490.77

Biebach H. 1985. Sahara stopover in migratory flycatchers: fat and food affect the time program. Experientia, 41(5): 695–697. https://doi.org/10.1007/BF02007727

Bojarinova J. and Babushkina O. 2015. Photoperiodic conditions affect the level of locomotory activity during autumn migration in the Long-tailed Tit (Aegithalos c. caudatus). The Auk, 132(2): 370–379. https://doi.org/10.1642/AUK-14-155.1

Bolshakov C.V., Chernetsov N., Mukhin A., Bulyuk V.N., Kosarev V., Ktitorov P., Leoke D. and Tsvey A. 2007. Time of nocturnal departures in European robins, Erithacus rubecula, in relation to celestial cues, season, stopover duration and fat stores. Animal Behaviour, 74: 855–865. https://doi.org/10.1016/j.anbehav.2006.10.024

Boswell T. 2005. Regulation of energy balance in birds by the neuroendocrine hypothalamus. The Journal of Poultry Science, 42(3): 161–181. https://doi.org/10.2141/jpsa.42.161

Boswell T., Hall M.R. and Goldsmith A.R. 1995a. Testosterone is secreted extragonadally by European quail maintained on short days. Physiological Zoology, 68: 967–984. https://doi.org/10.1086/physzool.68.6.30163789

Boswell T., Lehman T.L. and Ramenofsky M. 1997. Effects of plasma glucose manipulations on food intake in white-crowned sparrows. Comparative Biochemistry and Physiology Part A: Physiology, 118(3): 721–726. https://doi.org/10.1016/S0300-9629(96)00063-1

Boswell T., Sharp P.J., Hall M.R. and Goldsmith A.R. 1995b. Migratory fat deposition in European quail: a role for prolactin? Journal of Endocrinology, 146(1): 71–79. https://doi.org/10.1677/joe.0.1460071

De Bournonville C., McGrath A. and Remage-Healey L. 2020. Testosterone synthesis in the female songbird brain. Hormones and Behavior, 121: 104716. https://doi.org/10.1016/j.yhbeh.2020.104716

Braun E.J. and Sweazea K.L. 2008. Glucose regulation in birds. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 151(1): 1–9. https://doi.org/10.1016/j.cbpb.2008.05.007

Buehler D.M., Tieleman B.I. and Piersma T. 2010. How Do Migratory Species Stay Healthy Over the Annual Cycle? A Conceptual Model for Immune Function and For Resistance to Disease. Integrative and Comparative Biology, 50(3): 346–357. https://doi.org/10.1093/icb/icq055

Bulyuk V.N., Sokolov L.V., Markovets M.Y. and Lubkovskaia R.S. 2018. Study of migratory strategies of common cuckoos (Cuculus canorus) using satellite transmitters. In: V.M. Gavrilov, I. Beme, N. Chernetsov, K. Avilova, V. Gavrilov, T.B. Golubeva, M. Goretskaia and T.A. Ilyina (Eds). Ornithology: history, traditions, problems and prospects. Materials of the conference and workshop dedicated to the 120th anniversiary of professor G.P. Dementyev. KMK Scientific Press Ltd., Moscow: 61–67. [In Russian].

Bulyuk V.N. and Tsvey A. 2013. Regulation of stopover duration in the European Robin Erithacus rubecula. Journal of Ornithology, 154: 1115–1126. https://doi.org/10.1007/s10336-013-0981-0

Buntin J.D., Hnasko R.M. and Zuzick P.H. 1999. Role of the Ventromedial Hypothalamus in Prolactin-Induced Hyperphagia in Ring Doves. Physiology and Behavior, 66(2): 255–261. https://doi.org/10.1016/S0031-9384(98)00288-1

Casagrande S., DeMoranville K.J., Trost L., Pierce B., Bryła A., Dzialo M., Sadowska E.T., Bauchinger U. and McWilliams S.R. 2020. Dietary antioxidants attenuate the endocrine stress response during long-duration flight of a migratory bird. Proceedings of the Royal Society B: Biological Sciences, 287(1929): 20200744. https://doi.org/10.1098/rspb.2020.0744

Cassone V.M. 2014. Avian circadian organization: A chorus of clocks. Frontiers in Neuroendocrinology, 35(1): 76–88. https://doi.org/10.1016/j.yfrne.2013.10.002

Cerasale D.J., Zajac D.M. and Guglielmo C.G. 2011. Behavioral and physiological effects of photoperiod-induced migratory state and leptin on a migratory bird, Zonotrichia albicollis: I. Anorectic effects of leptin administration. General and Comparative Endocrinology, 174(3): 276–286. https://doi.org/10.1016/j.ygcen.2011.08.025

Chernetsov N. 2012. Passerine migration: stopovers and flight. Springer, Berlin, Heidelberg, 184 p. https://doi.org/10.1007/978-3-642-29020-6

Chernetsov N.S. 2016. Orientation and navigation of migrating birds. Biology Bulletin, 43(8): 788–803. https://doi.org/10.1134/S1062359016080069

Chernetsov N. 2023. Bird migration research today: some achievements and new challenges. Proceedings of the Zoological Institute RAS, 327(4): 607–622. [In Russian]. https://doi.org/10.31610/trudyzin/2023.327.4.607

Churchman E. and MacDougall-Shackleton S.A. 2022. Leptin administration does not influence migratory behaviour in white-throated sparrows (Zonotrichia albicollis). PeerJ, 10: e13584. https://doi.org/10.7717/peerj.13584

Combs T.P. and Marliss E.B. 2014. Adiponectin signaling in the liver. Reviews in Endocrine and Metabolic Disorders, 15(2): 137–147. https://doi.org/10.1007/s11154-013-9280-6

Coppack T. and Bairlein F. 2011. Circadian control of nocturnal songbird migration. Journal of Ornithology, 152: 67–73. https://doi.org/10.1007/s10336-011-0708-z

Cornelius J.M., Boswell T., Jenni-Eiermann S., Breuner C.W. and Ramenofsky M. 2013. Contributions of endocrinology to the migration life history of birds. General and Comparative Endocrinology, 190: 47–60. https://doi.org/10.1016/j.ygcen.2013.03.027

Covino K.M. and Holberton R.L. 2011. The Influence of Energetic Condition on Flight Initiation and Orientation of Migratory Songbirds in the Gulf of Maine Region. The Auk, 128(2): 313–320. https://doi.org/10.1525/auk.2011.09225

Crossin G.T., Love O.P., Cooke S.J. and Williams T.D. 2016. Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context and reproductive state. Functional Ecology, 30(1): 116–125. https://doi.org/10.1111/1365-2435.12482

Dawson A., King V.M., Bentley G.E. and Ball G.F. 2001. Photoperiodic Control of Seasonality in Birds. Journal of Biological Rhythms, 16(4): 365–380. https://doi.org/10.1177/074873001129002079

Deakin J.E., Guglielmo C.G. and Morbey Y.E. 2019. Sex differences in migratory restlessness behavior in a Nearctic–Neotropical songbird. The Auk, 136(3): ukz017. https://doi.org/10.1093/auk/ukz017

DeLuca W.V., Woodworth B.K., Mackenzie S.A., Newman A.E.M., Cooke H.A., Phillips L.M., Freeman N.E., Sutton A.O., Tauzer L., McIntyre C., Stenhouse I.J., Weidensaul S., Taylor P.D. and Norris D.R. 2019. A boreal songbird's 20,000 km migration across North America and the Atlantic Ocean. Ecology: e02651. https://doi.org/10.1002/ecy.2651

Demina I., Tsvey A., Babushkina O. and Bojarinova J. 2019. Time‐keeping programme can explain seasonal dynamics of leukocyte profile in a migrant bird. Journal of Avian Biology, 50(7): jav.02117. https://doi.org/10.1111/jav.02117

DeMoranville K.J., Carter W.A., Pierce B.J. and McWilliams S.R. 2020. Flight training in a migratory bird drives metabolic gene expression in the flight muscle but not liver, and dietary fat quality influences select genes. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 319(6): R637–R652. https://doi.org/10.1152/ajpregu.00163.2020

DeMoranville K.J., Corder K.R., Hamilton A., Russell D.E., Huss J.M. and Schaeffer P.J. 2019. PPAR expression, muscle size, and metabolic rates across the Gray catbird's annual cycle are greatest in preparation for fall migration. Journal of Experimental Biology, 222(14): jeb.198028. https://doi.org/10.1242/jeb.198028

Deviche P. 1995. Androgen regulation of avian premigratory hyperphagia and fattening: from eco-physiology to neuroendocrinology. American Zoologist, 35(3): 234–245. https://doi.org/10.1093/icb/35.3.234

Dolnik V.R. 1975. Migratory disposition in birds. Nauka, Moscow, 398 p. [In Russian].

Dolnik V.R. and Blyumental T.I. 1967. Autumnal premigratory and migratory periods in the chaffinch (Fringilla coelebs coelebs) and some other temperate zone passerine birds. Condor, 69: 435–468. https://doi.org/10.2307/1366146

Dubois V., Laurent M., Boonen S., Vanderschueren D. and Claessens F. 2012. Androgens and skeletal muscle: cellular and molecular action mechanisms underlying the anabolic actions. Cellular and Molecular Life Sciences, 69: 1651–1667. https://doi.org/10.1007/s00018-011-0883-3

Dupont J., Rideau N. and Simon J. 2015. Endocrine pancreas. In: C.G. Scanes (Ed.). Sturkie's Avian Physiology. Elsevier, Amsterdam, Boston: 613–631. https://doi.org/10.1016/B978-0-12-407160-5.00027-0

Dyachenko V.P. 1974. Stimulation of fattening by prolactin in house sparrow Passer domesticus. Journal of Evolutionary Biochemistry and Physiology, 10(4): 408–410. [In Russian].

Dyachenko V.P. 1976. The role of seasonal dynamics in prolactin secretion and sensitivity to this hormone in regulation of migratory fattening in some bird species. In Physiological adjustments of migratory disposition in birds: 77–88. [In Russian].

Dyachenko V.P. 1982. Circadian rhythms of prolactin secretion and control of migratory fattening in chaffinch Fringilla coelebs. Uspechi sovremennoy biologii, 18(4): 341–348. [In Russian].

Dyachenko V.P. and Dolnik V.R. 1984. The role of prolactin in regulation of seasonal states in birds. Uspechi sovremennoy biologii, 97(2): 295–308. [In Russian].

Eikenaar C. 2017. Endocrine regulation of fueling by hyperphagia in migratory birds. Journal of Comparative Physiology A, 203(6–7): 439–445. https://doi.org/10.1007/s00359-017-1152-1

Eikenaar C., Bairlein F., Stöwe M. and Jenni-Eiermann S. 2014a. Corticosterone, food intake and refueling in a long-distance migrant. Hormones and Behavior, 65(5): 480–487. https://doi.org/10.1016/j.yhbeh.2014.03.015

Eikenaar C., Ballstaedt E., Hessler S., Klinner T., Müller F. and Schmaljohann H. 2018a. Cues, corticosterone and departure decisions in a partial migrant. General and Comparative Endocrinology, 261: 59–66. https://doi.org/10.1016/j.ygcen.2018.01.023

Eikenaar C., Fritzsch A. and Bairlein F. 2013. Corticosterone and migratory fueling in northern wheatears facing different barrier crossings. General and Comparative Endocrinology, 186: 181–186. https://doi.org/10.1016/j.ygcen.2013.02.042

Eikenaar C., Hessler S., Ballstaedt E., Schmaljohann H. and Kaiya H. 2018b. Ghrelin, corticosterone and the resumption of migration from stopover, an automated telemetry study. Physiology and Behavior, 194: 450–455. https://doi.org/10.1016/j.physbeh.2018.06.036

Eikenaar C., Klinner T., Szostek K.L. and Bairlein F. 2014b. Migratory restlessness in captive individuals predicts actual departure in the wild. Biology Letters, 10(4): 20140154–20140154. https://doi.org/10.1098/rsbl.2014.0154

Eikenaar C., Müller F., Klinner T. and Bairlein F. 2015. Baseline corticosterone levels are higher in migrating than sedentary common blackbirds in autumn, but not in spring. General and Comparative Endocrinology, 224: 121–125. https://doi.org/10.1016/j.ygcen.2015.07.003

Eikenaar C., Müller F., Leutgeb C., Hessler S., Lebus K., Taylor P.D. and Schmaljohann H. 2017. Corticosterone and timing of migratory departure in a songbird. Proceedings of the Royal Society B, 284(1846): 20162300. https://doi.org/10.1098/rspb.2016.2300

Eikenaar C., Schäfer J., Hessler S., Packmor F. and Schmaljohann H. 2020. Diel variation in corticosterone and departure decision making in migrating birds. Hormones and Behavior, 122: 104746. https://doi.org/10.1016/j.yhbeh.2020.104746

Falcón J., Besseau L., Sauzet S. and Boeuf G. 2007. Melatonin effects on the hypothalamo–pituitary axis in fish. Trends in Endocrinology and Metabolism, 18(2): 81–88. https://doi.org/10.1016/j.tem.2007.01.002

Falsone K., Jenni-Eiermann S. and Jenni L. 2009. Corticosterone in migrating songbirds during endurance flight. Hormones and Behavior, 56(5): 548–556. https://doi.org/10.1016/j.yhbeh.2009.09.009

Friedman-Einat M. and Seroussi E. 2019. Avian Leptin: Bird’s-Eye View of the Evolution of Vertebrate Energy-Balance Control. Trends in Endocrinology and Metabolism, 30(11): 819–832. https://doi.org/10.1016/j.tem.2019.07.007

Fudickar A.M., Peterson M.P., Greives T.J., Atwell J.W., Bridge E.S. and Ketterson E.D. 2016. Differential gene expression in seasonal sympatry: mechanisms involved in diverging life histories. Biology Letters, 12(3): 20160069. https://doi.org/10.1098/rsbl.2016.0069

Fusani L., Cardinale M., Carere C. and Goymann W. 2009. Stopover decision during migration: physiological conditions predict nocturnal restlessness in wild passerines. Biology Letters, 5(3): 302–305. https://doi.org/10.1098/rsbl.2008.0755

Fusani L., Cardinale M., Schwabl I. and Goymann W. 2011. Food availability but not melatonin affects nocturnal restlessness in a wild migrating passerine. Hormones and Behavior, 59(1): 187–192. https://doi.org/10.1016/j.yhbeh.2010.11.013

Fusani L., Coccon F., Mora A.R. and Goymann W. 2013. Melatonin reduces migratory restlessness in Sylvia warblers during autumnal migration. Frontiers in Zoology, 10(1): 79. https://doi.org/10.1186/1742-9994-10-79

Fusani L. and Gahr M. 2015. Differential expression of melatonin receptor subtypes MelIa, MelIb and MelIc in relation to melatonin binding in the male songbird brain. Brain, Behavior and Evolution, 85(1): 4–14. https://doi.org/10.1159/000367984

Fusani L. and Gwinner E. 2004. Simulation of migratory flight and stopover affects night levels of melatonin in a nocturnal migrant. Proceedings of the Royal Society B, 271(1535): 205–211. https://doi.org/10.1098/rspb.2003.2561

Gaidica M. and Dantzer B. 2022. An implantable neurophysiology platform: Broadening research capabilities in free-living and non-traditional animals. Frontiers in Neural Circuits, 16: 940989. https://doi.org/10.3389/fncir.2022.940989

García-Fernández J.M., Cernuda-Cernuda R., Davies W.I.L., Rodgers J., Turton M., Peirson S.N., Follett B.K., Halford S., Hughes S., Hankins M.W. and Foster R.G. 2015. The hypothalamic photoreceptors regulating seasonal reproduction in birds: A prime role for VA opsin. Frontiers in Neuroendocrinology, 37: 13–28. https://doi.org/10.1016/j.yfrne.2014.11.001

Geng T., Yang B., Li F., Xia L., Wang Q., Zhao X. and Gong D. 2016. Identification of protective components that prevent the exacerbation of goose fatty liver: Characterization, expression and regulation of adiponectin receptors. Comparative Biochemistry and Physiology B, 194–195: 32–38. https://doi.org/10.1016/j.cbpb.2016.01.006

George J., John T. and Mitchell M. 1989. Flight Effects on Plasma Levels of Lipid, Glucagon and Thyroid Hormones in Homing Pigeons. Hormone and Metabolic Research, 21(10): 542–545. https://doi.org/10.1055/s-2007-1009283

Gill R.E., Tibbitts T.L., Douglas D.C., Handel C.M., Mulcahy D.M., Gottschalck J.C., Warnock N., McCaffery B.J., Battley P.F. and Piersma T. 2009. Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proceedings of the Royal Society B, 276(1656): 447–457. https://doi.org/10.1098/rspb.2008.1142

Giossi J.T. 2017. Regulation of seasonal changes in gene expression mediated by adiponectin signaling in a migratory bird species. Master thesis. The Pennsylvania State University, 60 p.

Goymann W., Lupi S., Kaiya H., Cardinale M. and Fusani L. 2017. Ghrelin affects stopover decisions and food intake in a long-distance migrant. Proceedings of the National Academy of Sciences of the U.S.A.: 201619565. https://doi.org/10.1073/pnas.1619565114

Goymann W., Spina F., Ferri A. and Fusani L. 2010. Body fat influences departure from stopover sites in migratory birds: evidence from whole-island telemetry. Biology Letters, 6(4): 478–481. https://doi.org/10.1098/rsbl.2009.1028

Gray J.M., Yarian D. and Ramenofsky M. 1990. Corticosterone, foraging behavior, and metabolism in dark-eyed juncos, Junco hyemalis. General and Comparative Endocrinology, 79(3): 375–384. https://doi.org/10.1016/0016-6480(90)90067-V

Guglielmo C.G. 2018. Obese super athletes: fat-fueled migration in birds and bats. The Journal of Experimental Biology, 221 (Suppl. 1): jeb165753. https://doi.org/10.1242/jeb.165753

Gumus A., Lee S., Ahsan S.S., Karlsson K., Gabrielson R., Guglielmo C.G., Winkler D.W. and Erickson D. 2015. Lab-on-a-Bird: Biophysical Monitoring of Flying Birds. PLoS ONE, 10(4): e0123947. https://doi.org/10.1371/journal.pone.0123947

Gupta N.J. and Kumar V. 2013. Testes play a role in termination but not in initiation of the spring migration in the night-migratory blackheaded bunting. Animal Biology, 63(3): 321–329. https://doi.org/10.1163/15707563-00002415

Gwinner E. 1989. Photoperiod as a modifying and limiting factor in the expression of avian circannual rhythms. Journal of Biological Rhythms, 4: 125–138. https://doi.org/10.1177/074873048900400210

Gwinner E. 1996. Circadian and circannual programmes in avian migration. Journal of Experimental Biology, 199: 39–48. https://doi.org/10.1242/jeb.199.1.39

Gwinner E., Biebach H. and Kries I.V. 1985. Food availability affects migratory restlessness in caged garden warblers (Sylvia borin). Naturwissenschaften, 72(1): 51–52. https://doi.org/10.1007/BF00405336

Gwinner E. and Brandstätter R. 2001. Complex bird clocks. Philosophical Transactions of the Royal Society of London B, 356(1415): 1801–1810. https://doi.org/10.1098/rstb.2001.0959

Gwinner E., Schwabl-Benzinger I., Schwabl H. and Dittami J. 1993. Twenty-Four Hour Melatonin Profiles in a Nocturnally Migrating Bird during and between Migratory Seasons. General and Comparative Endocrinology, 90(1): 119–124. https://doi.org/10.1006/gcen.1993.1066

Gwinner E., Schwabl H. and Schwabl-Benzinger I. 1988. Effects of food-deprivation on migratory restlessness and diurnal activity in the garden warbler Sylvia borin. Oecologia, 77(3): 321–326. https://doi.org/10.1007/BF00378037

Gwinner E. and Wiltschko W. 1978. Endogenously controlled changes in migratory direction of the garden warbler, Sylvia borin. Journal of Comparative Physiology, 125(3): 267–273. https://doi.org/10.1007/BF00656605

Hahn S., Bauer S. and Liechti F. 2009. The natural link between Europe and Africa – 2.1 billion birds on migration. Oikos, 118: 624–626. https://doi.org/10.1111/j.1600-0706.2008.17309.x

Harvey S., Phillips J.G., Rees A. and Hall T.R. 1984. Stress and adrenal function. Journal of Experimental Biology, 232: 633–645. https://doi.org/10.1002/jez.1402320332

Hashinaga T., Wada N., Otabe S., Yuan X., Kurita Y., Kakino S., Tanaka K., Sato T., Kojima M., Ohki T., Nakayama H., Egashira T., Tajiri Y. and Yamada K. 2013. Modulation by adiponectin of circadian clock rhythmicity in model mice for metabolic syndrome. Endocrine Journal, 60(4): 483–492. https://doi.org/10.1507/endocrj.EJ12-0305

Hasselquist D., Lindstrom A., Jenni-Eiermann S., Koolhaas A. and Piersma T. 2007. Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment. Journal of Experimental Biology, 210(7): 1123–1131. https://doi.org/10.1242/jeb.02712

Hau M. and Goymann W. 2015. Endocrine mechanisms, behavioral phenotypes and plasticity: known relationships and open questions. Frontiers in Zoology, 12(1): S7. https://doi.org/10.1186/1742-9994-12-S1-S7

Hedenström A. and Lindström Å. 2017. Wind tunnel as a tool in bird migration research. Journal of Avian Biology, 48(1): 37–48. https://doi.org/10.1111/jav.01363

Hegemann A., Matson K.D., Both C. and Tieleman B.I. 2012. Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years. Oecologia, 170(3): 605–618. https://doi.org/10.1007/s00442-012-2339-3

Helm B., Ben-Shlomo R., Sheriff M.J., Hut R.A., Foster R., Barnes B.M. and Dominoni D. 2013. Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proceedings of the Royal Society B, 280(1765): 20130016–20130016. https://doi.org/10.1098/rspb.2013.0016

Helm B., Gwinner E., Koolhaas A., Battley P., Schwabl I., Dekinga A. and Piersma T. 2012. Avian migration: temporal multitasking and a case study of melatonin cycles in waders. Progress in Brain Research, 199: 457–479. https://doi.org/10.1016/B978-0-444-59427-3.00026-5

Henderson L.J., Cockcroft R.C., Kaiya H., Boswell T. and Smulders T.V. 2018. Peripherally injected ghrelin and leptin reduce food hoarding and mass gain in the coal tit (Periparus ater). Proceedings of the Royal Society B, 285(1879): 20180417. https://doi.org/10.1098/rspb.2018.0417

Hendricks G.L., Hadley J.A., Krzysik-Walker S.M., Prabhu K.S., Vasilatos-Younken R. and Ramachandran R. 2009. Unique Profile of Chicken Adiponectin, a Predominantly Heavy Molecular Weight Multimer, and Relationship to Visceral Adiposity. Endocrinology, 150(7): 3092–3100. https://doi.org/10.1210/en.2008-1558

Hiatt E.S., Goldsmith A.R. and Farner D.S. 1987. Plasma levels of prolactin and gonadotropins during the reproductive cycle of the white-crowned sparrows (Zonotrichia leucophrys). Auk, 104(2): 208–217. https://doi.org/10.1093/auk/104.2.208

Hintz J.V. 2000. The hormonal regulation of premigratory fat deposition and winter fattening in red-winged blackbirds. Comparative Biochemistry and Physiology A, 125(2): 239–249. https://doi.org/10.1016/S1095-6433(99)00179-8

Holberton R.L., Boswell T. and Hunter M.J. 2008. Circulating prolactin and corticosterone concentrations during the development of migratory condition in the Dark-eyed Junco, Junco hyemalis. General and Comparative Endocrinology, 155(3): 641–649. https://doi.org/10.1016/j.ygcen.2007.11.001

Holberton R.L., Parrish J.D. and Wingfield J.C. 1996. Modulation of the adrenocortical stress response in neortopical migrants during autumn migration. Auk, 113(3): 558–564. https://doi.org/10.2307/4088976

Horton W.J., Jensen M., Sebastian A., Praul C.A., Albert I. and Bartell P.A. 2019. Transcriptome Analyses of Heart and Liver Reveal Novel Pathways for Regulating Songbird Migration. Scientific Reports, 9(1): 6058. https://doi.org/10.1038/s41598-019-41252-8

Imbesi M., Arslan A.D., Yildiz S., Sharma R., Gavin D., Tun N., Manev H. and Uz T. 2009. The melatonin receptor MT1 is required for the differential regulatory actions of melatonin on neuronal ‘clock’ gene expression in striatal neurons in vitro. Journal of Pineal Research, 46(1): 87–94. https://doi.org/10.1111/j.1600-079X.2008.00634.x

Jacobs J.D. and Wingfield J.C. 2000. Endocrine control of life-cycle stages: a constraint on response to the environment? Condor, 102: 35–51. https://doi.org/10.1093/condor/102.1.35

Jenni-Eiermann S., Hasselquist D., Lindström Å., Koolhaas A. and Piersma T. 2009. Are birds stressed during long-term ﬂights? A wind-tunnel study on circulating corticosterone in the red knot. General and Comparative Endocrinology, 164(2): 101–106. https://doi.org/10.1016/j.ygcen.2009.05.014

Jenni-Eiermann S., Jenni L., Kvist A., Lindström Å., Piersma T. and Visser G.H. 2002. Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. Journal of Experimental Biology, 205(16): 2453–2460. https://doi.org/10.1242/jeb.205.16.2453

Jenni-Eiermann S., Jenni L. and Piersma T. 2002. Temporal uncoupling of thyroid hormones in Red Knots: T3 peaks in cold weather, T4 during moult. Journal of Ornitholoy, 143: 331–340. https://doi.org/10.1007/BF02465483

Jenni L., Jenni-Eiermann S., Spina F. and Schwabl H. 2000. Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 278(5): R1182–R1189. https://doi.org/10.1152/ajpregu.2000.278.5.R1182

John T.M., George J.C. and Etches R.J. 1984. Seasonal changes in the concentration of plasma prolactin in the migratory Canada goose (Branta canadensis interior). Comparative Biochemistry and Physiology A, 79(1): 127–131. https://doi.org/10.1016/0300-9629(84)90719-9

Johnston R.A., Paxton K.L., Moore F.R., Wayne R.K. and Smith T.B. 2016. Seasonal gene expression in a migratory songbird. Molecular Ecology, 25(22): 5680–5691. https://doi.org/10.1111/mec.13879

Kaiya H., Darras V.M. and Kangawa K. 2007. Ghrelin in birds: its structure, distribution and function. The Journal of Poultry Science, 44(1): 1–18. https://doi.org/10.2141/jpsa.44.1

Kaiya H., Furuse M., Miyazato M. and Kangawa K. 2009. Current knowledge of the roles of ghrelin in regulating food intake and energy balance in birds. General and Comparative Endocrinology, 163(1–2): 33–38. https://doi.org/10.1016/j.ygcen.2008.11.008

Kanfi Y., Peshti V., Gozlan Y.M., Rathaus M., Gil R. and Cohen H.Y. 2008. Regulation of SIRT1 protein levels by nutrient availability. FEBS Letters, 582(16): 2417–2423. https://doi.org/10.1016/j.febslet.2008.06.005

Kim J.E., Bennett D.C., Wright K. and Cheng K.M. 2022. Seasonal and sexual variation in mRNA expression of selected adipokine genes affecting fat deposition and metabolism of the emu (Dromaius novaehollandiae). Scientific Reports, 12(1): 6325. https://doi.org/10.1038/s41598-022-10232-w

Klaassen R.H.G., Alerstam T., Carlsson P., Fox J.W. and Lindström Å. 2011. Great flights by great snipes: long and fast non-stop migration over benign habitats. Biology Letters, 7(6): 833–835. https://doi.org/10.1098/rsbl.2011.0343

Kojima M., Hamamoto A. and Sato T. 2016. Ghrelin O-acyltransferase (GOAT), a specific enzyme that modifies ghrelin with a medium-chain fatty acid. Journal of Biochemistry, 160(4): 189–194. https://doi.org/10.1093/jb/mvw046

Krause J.S., Meddle S.L. and Wingfield J.C. 2015. The Effects of Acute Restraint Stress on Plasma Levels of Prolactin and Corticosterone across Life-History Stages in a Short-Lived Bird: Gambel’s White-Crowned Sparrow (Zonotrichia leucophrys gambelii). Physiological and Biochemical Zoology, 88(6): 589–598. https://doi.org/10.1086/683321

Krause J.S., Watkins T., Reid A.M.A., Cheah J.C., Pérez J.H., Bishop V.R., Ramenofsky M., Wingfield J.C. and Meddle S.L. 2022. Gene expression of sex steroid metabolizing enzymes and receptors in the skeletal muscle of migrant and resident subspecies of white-crowned sparrow (Zonotrichia leucophrys). Oecologia, 199(3): 549–562. https://doi.org/10.1007/s00442-022-05204-w

Kumar V. and Sharma A. 2018. Common features of circadian timekeeping in diverse organisms. Current Opinion in Physiology, 5: 58–67. https://doi.org/10.1016/j.cophys.2018.07.004

Kumar V., Wingfield J.C., Dawson A., Ramenofsky M., Rani S. and Bartell P. 2010. Biological clocks and regulation of seasonal reproduction and migration in birds. Physiological and Biochemical Zoology, 83: 827–835. https://doi.org/10.1086/652243

Kuz'mina V.V. 2020. Melatonin. Multifunctionality. Fish. Journal of Evolutionary Biochemistry and Physiology, 56(2): 89–101. https://doi.org/10.1134/S0022093020020015

Landys-Ciannelli M.M., Ramenofsky M., Piersma T., Jukema J., Group C.R. and Wingfield J.C. 2002. Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Physiological and Biochemical Zoology, 75(1): 101–110. https://doi.org/10.1086/338285

Landys M.M., Piersma T., Guglielmo C.G., Jukema J., Ramenofsky M. and Wingfield J.C. 2005. Metabolic profile of long-distance migratory flight and stopover in a shorebird. Proceedings of the Royal Society B, 272(1560): 295–302. https://doi.org/10.1098/rspb.2004.2952

Landys M.M., Ramenofsky M., Guglielmo C.G. and Wingfield J.C. 2004. The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii. Journal of Experimental Biology, 207: 143–154. https://doi.org/10.1242/jeb.00734

Landys M.M., Ramenofsky M. and Wingfield J.C. 2006. Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. General and Comparative Endocrinology, 148(2): 132–149. https://doi.org/10.1016/j.ygcen.2006.02.013

Lemke H.W., Tarka M., Klaassen R.H.G., Åkesson M., Bensch S., Hasselquist D. and Hansson B. 2013. Annual Cycle and Migration Strategies of a Trans-Saharan Migratory Songbird: A Geolocator Study in the Great Reed Warbler. PLoS ONE, 8(10): e79209. https://doi.org/10.1371/journal.pone.0079209

Lewis J.E. and Ebling F.J.P. 2017. Tanycytes As Regulators of Seasonal Cycles in Neuroendocrine Function. Frontiers in Neurology, 8(79). https://doi.org/10.3389/fneur.2017.00079

Liechti F. 2006. Birds: blowin’ by the wind? Journal of Ornithology, 147(2): 202–211. https://doi.org/10.1007/s10336-006-0061-9

Lincoln G. 2019. A brief history of circannual time. Journal of Neuroendocrinology, 31(3): e12694. https://doi.org/10.1111/jne.12694

Linscott J.A. and Senner N.R. 2021. Beyond refueling: Investigating the diversity of functions of migratory stopover events. The Condor, 123(1): 1–14. https://doi.org/10.1093/ornithapp/duaa074

Lõhmus M., Sundstrom L.F. and Moore F.R. 2006a. Non-invasive corticosterone treatment changes foraging intensity in red-eyed vireos Vireo olivaceus. Journal of Avian Biology, 37(5): 523–526. https://doi.org/10.1111/j.0908-8857.2006.03733.x

Lõhmus M., Sundström L.F. and Silverin B. 2006b. Chronic administration of leptin in Asian Blue Quail. Journal of Experimental Zoology Part A: Comparative Experimental Biology, 305A(1): 13–22. https://doi.org/10.1002/jez.a.240

López-López P., Limiñana R., Mellone U. and Urios V. 2010. From the Mediterranean Sea to Madagascar: Are there ecological barriers for the long-distance migrant Eleonora’s falcon? Landscape Ecology, 25(5): 803–813. https://doi.org/10.1007/s10980-010-9460-7

Loshchagina J., Tsvey A. and Naidenko S. 2018. Baseline and stress-induced corticosterone levels are higher during spring than autumn migration in European robins. Hormones and Behavior, 98: 96–102. https://doi.org/10.1016/j.yhbeh.2017.12.013

Lumineau S., Guyomarc’h C., Boswell T., Richard J.-P. and Leray D. 1998. Induction of Circadian Rhythm of Feeding Activity by Testosterone Implantations in Arrhythmic Japanese Quail Males. Journal of Biological Rhythms, 13(4): 278–287. https://doi.org/10.1177/074873098129000110

Lupi S., Canoine V., Pedrini P. and Fusani L. 2019a. Temporary caging results in reduced levels of circulating melatonin in migratory robins. The Journal of Experimental Biology, 222(24): jeb.210914. https://doi.org/10.1242/jeb.210914

Lupi S., Morbey Y.E., MacDougall-Shackleton S.A., Kaiya H., Fusani L. and Guglielmo C.G. 2022. Experimental ghrelin administration affects migratory behaviour in a songbird. Hormones and Behavior, 141: 105139. https://doi.org/10.1016/j.yhbeh.2022.105139

Lupi S., Slezacek J. and Fusani L. 2019b. The physiology of stopover decisions: food, fat and zugunruhe on a Mediterranean island. Journal of Ornithology, 160: 1205–1212. https://doi.org/10.1007/s10336-019-01693-4

Madadi S., Hasasnpour S., Zendehdel M., Vazir B. and Jahandideh A. 2023. Role of central adiponectin and its interactions with NPY and GABAergic systems on food intake in neonatal layer chicken. Neuroscience Letters, 808: 137283. https://doi.org/10.1016/j.neulet.2023.137283

Maggini I. and Bairlein F. 2010. Endogenous Rhythms of Seasonal Migratory Body Mass Changes and Nocturnal Restlessness in Different Populations of Northern Wheatear Oenanthe oenanthe. Journal of Biological Rhythms, 25(4): 268–276. https://doi.org/10.1177/0748730410373442

Majumdar G., Rani S. and Kumar V. 2015. Hypothalamic gene switches control transitions between seasonal life history states in a night-migratory photoperiodic songbird. Molecular and Cellular Endocrinology, 399: 110–121. https://doi.org/10.1016/j.mce.2014.09.020

Majumdar G., Yadav G., Malik S., Rani S., Balthazart J. and Kumar V. 2021. Hypothalamic plasticity in response to changes in photoperiod and food quality: An adaptation to support pre-migratory fattening in songbirds? European Journal of Neuroscience, 53(2): 430–448. https://doi.org/10.1111/ejn.14994

Malisch J.L. and Breuner C.W. 2010. Steroid-binding proteins and free steroids in birds. Molecular and Cellular Endocrinology, 316(1): 42–52. https://doi.org/10.1016/j.mce.2009.09.019

Maney D.L., Hahn T.P., Schoech S.J., Sharp P.J., Morton M.L. and Wingfield J.C. 1999. Effects of ambient temperature on photo-induced prolactin secretion in three subspecies of white-crowned sparrow, Zonotrichia leucophrys. General and Comparative Endocrinology, 113(3): 445–456. https://doi.org/10.1006/gcen.1998.7219

Marasco V., Kaiya H., Pola G. and Fusani L. 2023. Ghrelin, not corticosterone, is associated with transitioning of phenotypic states in a migratory Galliform. Frontiers in Endocrinology, 13: 3256. https://doi.org/10.3389/fendo.2022.1058298

Marcheva B., Ramsey K.M., Buhr E.D., Kobayashi Y., Su H., Ko C.H., Ivanova G., Omura C., Mo S., Vitaterna M.H., Lopez J.P., Philipson L.H., Bradfield C.A., Crosby S.D., JeBailey L., Wang X., Takahashi J.S. and Bass J. 2010. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature, 466(7306): 627–631. https://doi.org/10.1038/nature09253

Mattocks P.W., Jr. 1976. The role of gonadal hormones in the regulation of the premigratory fat deposition in the white-crowned sparrow, Zonotrichia leucophrys gambelli. MS Thesis. University of Washington, Seattle, 73 p.

McFarlan J.T., Bonen A. and Guglielmo C.G. 2009. Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). Journal of Experimental Biology, 212(18): 2934–2940. https://doi.org/10.1242/jeb.031682

McWilliams S.R., Ramenofsky M. and Pierce B.J. 2022. Physiological challenges of migration. In: C.G. Scanes and S. Dridi (Eds). Sturkie's Avian Physiology (Seventh Edition). Academic Press, San Diego: 1331–1372. https://doi.org/10.1016/B978-0-12-819770-7.00017-7

Mishra I., Singh D. and Kumar V. 2017. Daily levels and rhythm in circulating corticosterone and insulin are altered with photostimulated seasonal states in night-migratory blackheaded buntings. Hormones and Behavior, 94: 114–123. https://doi.org/10.1016/j.yhbeh.2017.07.004

Mukhin A., Kobylkov D., Kishkinev D. and Grinkevich V. 2018. Interrupted breeding in a songbird migrant triggers development of nocturnal locomotor activity. Scientific Reports, 8(1): 5520. https://doi.org/10.1038/s41598-018-23834-0

Müller F., Taylor P.D., Sjöberg S., Muheim R., Tsvey A., Mackenzie S.A. and Schmaljohann H. 2016. Towards a conceptual framework for explaining variation in nocturnal departure time of songbird migrants. Movement Ecology, 4: 24. https://doi.org/10.1186/s40462-016-0089-2

Nakane Y. and Yoshimura T. 2019. Photoperiodic regulation of reproduction in vertebrates. Annual Review of Animal Biosciences, 7: 173–194. https://doi.org/10.1146/annurev-animal-020518-115216

Nilsson A.L.K. and Sandell M.I. 2009. Stress hormone dynamics: an adaptation to migration? Biology Letters, 5(4): 480–483. https://doi.org/10.1098/rsbl.2009.0193

Norris D.O. and Carr J.A. 2013. Vertebrate Endocrinology. Academic Press, London, 599 p.

Noskov G.A. and Rymkevich T.A. 2010. Regulation of annual cycle parameters and its role in microevolution of birds. Uspechi sovremennoy biologii, 130(4): 346–359. [In Russian].

Ovid D., Hayes T.B. and Bentley G.E. 2018. Melatonin Administration Methods for Research in Mammals and Birds. Journal of Biological Rhythms, 33: 567–588. https://doi.org/10.1177/0748730418795802

Owen J.C., Garvin M.C. and Moore F.R. 2014. Elevated testosterone advances onset of migratory restlessness in a nearctic-neotropical landbird. Behavioral Ecology and Sociobiology, 68(4): 561–569. https://doi.org/10.1007/s00265-013-1671-x

Owen J.C. and Moore F.R. 2008. Swainson’s thrushes in migratory disposition exhibit reduced immune function. Journal of Ethology, 26(3): 383–388. https://doi.org/10.1007/s10164-008-0092-1

Pant K. and Chandola-Saklani A. 1993. A role for thyroid hormones in the development of premigratory disposition in redheaded bunting, Emberiza bruniceps. Journal of Comparative Physiology B, 163(5): 389–394. https://doi.org/10.1007/BF00265643

Parrish J.D. 1997. Patterns of Frugivory and Energetic Condition in Nearctic Landbirds during Autumn Migration. The Condor, 99(3): 681–697. https://doi.org/10.2307/1370480

Parrish J.D. 2000. Behavioral, energetic, and conservation implications of foraging plasticity during migration. Studies in Avian Biology, 20: 53–70.

Pathak V.K. and Chandola A. 1982. Seasonal variations in extrathyroidal conversion of thyroxine to tri-iodothyronine and migratory disposition in redheaded bunting. General and Comparative Endocrinology, 47(4): 433–439. https://doi.org/10.1016/0016-6480(82)90121-6

Pérez J.H., Furlow J.D., Wingfield J.C. and Ramenofsky M. 2016. Regulation of vernal migration in Gambel's white-crowned sparrows: role of thyroxine and triiodothyronine. Hormones and Behavior, 84: 50–56. https://doi.org/10.1016/j.yhbeh.2016.05.021

Pérez J.H., Swanson R.E., Lau H.J., Cheah J., Bishop V.R., Snell K.R.S., Reid A.M.A., Meddle S.L., Wingfield J.C. and Krause J.S. 2019a. Tissue specific expression of 11β-HSD and its effects on plasma corticosterone during the stress response. The Journal of Experimental Biology: jeb.209346. https://doi.org/10.1242/jeb.209346

Pérez J.H., Tolla E., Bishop V.R., Foster R.G., Peirson S.N., Dunn I.C., Meddle S.L. and Stevenson T.J. 2023. Functional inhibition of deep brain non-visual opsins facilitates acute long day induction of reproductive recrudescence in male Japanese quail. Hormones and Behavior, 148: 105298. https://doi.org/10.1016/j.yhbeh.2022.105298

Pérez J.H., Tolla E., Dunn I.C., Meddle S.L. and Stevenson T.J. 2019b. A Comparative Perspective on Extra-retinal Photoreception. Trends in Endocrinology and Metabolism, 30(1): 39–53. https://doi.org/10.1016/j.tem.2018.10.005

Piersma T., Gill R.E. and Ruthrauff D.R. 2021. Physiomorphic Transformation in Extreme Endurance Migrants: Revisiting the Case of Bar-Tailed Godwits Preparing for Trans-Pacific Flights. Frontiers in Ecology and Evolution, 9: 685764. https://doi.org/10.3389/fevo.2021.685764

Piersma T., Reneerkens J. and Ramenofsky M. 2000. Baseline Corticosterone Peaks in Shorebirds with Maximal Energy Stores for Migration: A General Preparatory Mechanism for Rapid Behavioral and Metabolic Transitions? General and Comparative Endocrinology, 120(1): 118–126. https://doi.org/10.1006/gcen.2000.7543

Pohl H. 2000. Circadian control of migratory restlessness and the effects of exogenous melatonin in the brambling, Fringilla montifringilla. Chronobiology International, 17(4): 471–488. https://doi.org/10.1081/CBI-100101058

Pradhan D.S., Ma C., Schlinger B.A., Soma K.K. and Ramenofsky M. 2019. Preparing to migrate: expression of androgen signaling molecules and insulin-like growth factor-1 in skeletal muscles of Gambel’s white-crowned sparrows. Journal of Comparative Physiology A, 205(1): 113–123. https://doi.org/10.1007/s00359-018-1308-7

Price E.R., Bauchinger U., Zajac D.M., Cerasale D.J., McFarlan J.T., Gerson A.R., McWilliams S.R. and Guglielmo C.G. 2011. Migration- and exercise-induced changes to flight muscle size in migratory birds and association with IGF1 and myostatin mRNA expression. Journal of Experimental Biology, 214(17): 2823–2831. https://doi.org/10.1242/jeb.057620

Prost S., Elbers J.P., Slezacek J., Fuselli S., Smith S. and Fusani L. 2023. The unexpected loss of the "hunger hormone" ghrelin in true passerines: A game changer in migration physiology. bioRxiv: 2023–2005. https://doi.org/10.1101/2023.05.23.541918

Qi Y., Takahashi N., Hileman S.M., Patel H.R., Berg A.H., Pajvani U.B., Scherer P.E. and Ahima R.S. 2004. Adiponectin acts in the brain to decrease body weight. Nature Medicine, 10(5): 524–529. https://doi.org/10.1038/nm1029

Quispe R., Trappschuh M., Gahr M. and Goymann W. 2015. Towards more physiological manipulations of hormones in field studies: Comparing the release dynamics of three kinds of testosterone implants, silastic tubing, time-release pellets and beeswax. General and Comparative Endocrinology, 212: 100–105. https://doi.org/10.1016/j.ygcen.2015.01.007

Ramenofsky M. 1990. Fat storage and fat metabolism in relation to migration. In: E. Gwinner (Ed.). Bird migration: physiology and ecophysiology. Springer, Berlin, Heidelberg, New-York: 214–231. https://doi.org/10.1007/978-3-642-74542-3_15

Ramenofsky M. 2011. Hormones in migration and reproductive cycles of birds. In: D.O. Norris and K.H. Lopez (Eds). Hormones and Reproduction of Vertebrates. Elsevier: 205–237. https://doi.org/10.1016/B978-0-12-374929-1.10008-3

Ramenofsky M. and Agatsuma R. 2006. Migratory behaviour of captive white-crowned sparrows, Zonotrichia leucophrys gambelii, differs during autumn and spring migration. Behaviour, 143(10): 1219–1240. https://doi.org/10.1163/156853906778691586

Ramenofsky M., Campion A.W., Pérez J.H., Krause J.S. and Németh Z. 2017. Behavioral and physiological traits of migrant and resident white-crowned sparrows: a common garden approach. The Journal of Experimental Biology: jeb.148171. https://doi.org/10.1242/jeb.148171

Ramenofsky M., Cornelius J.M. and Helm B. 2012. Physiological and behavioral responses of migrants to environmental cues. Journal of Ornithology, 153(S1): 181–191. https://doi.org/10.1007/s10336-012-0817-3

Ramenofsky M. and Hahn T.P. 2019. Behavioral endocrinology of migration. In: Encyclopedia of Animal Behavior (Second Edition). Elsevier, 553–563 p. https://doi.org/10.1016/B978-0-12-809633-8.20816-9

Ramenofsky M. and Németh Z. 2014. Regulatory mechanisms for the development of the migratory phenotype: roles for photoperiod and the gonad. Hormones and Behavior, 66(1): 148–158. https://doi.org/10.1016/j.yhbeh.2014.04.012

Ramenofsky M. and Wingfield J.C. 2007. Regulation of migration. Bioscience, 57(2): 135–143. https://doi.org/10.1641/B570208

Rastogi A., Kumari Y., Rani S. and Kumar V. 2013. Neural Correlates of Migration: Activation of Hypothalamic Clock(s) in and out of Migratory State in the Blackheaded Bunting (Emberiza melanocephala). PLoS ONE, 8(10): e70065. https://doi.org/10.1371/journal.pone.0070065

Remage-Healey L. and Romero L.M. 2001. Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 281(3): R994–R1003. https://doi.org/10.1152/ajpregu.2001.281.3.R994

Robles M.S., Boyault C., Knutti D., Padmanabhan K. and Weitz C.J. 2010. Identification of RACK1 and Protein Kinase Cα as Integral Components of the Mammalian Circadian Clock. Science, 327(5964): 463–466. https://doi.org/10.1126/science.1180067

Romero L.M. 2004. Physiological stress in ecology: lessons from biomedical research. Trends in Ecology and Evolution, 19(5): 249–255. https://doi.org/10.1016/j.tree.2004.03.008

Romero L.M. and Wingfield J.C. 1999. Alterations in hypothalamic–pituitary–adrenal function associated with captivity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 122(1): 13–20. https://doi.org/10.1016/S0305-0491(98)10161-X

Romero L.M. and Wingfield J.C. 2016. Tempests, poxes, predators, and people: stress in wild animals and how they cope. Oxford University Press, Oxford; New York, 614 p. https://doi.org/10.1093/acprof:oso/9780195366693.001.0001

Ronanki S., Hegemann A. and Eikenaar C. 2023. Constitutive immune function is not associated with fuel stores in spring migrating passerine birds. Authorea. https://doi.org/10.22541/au.168396134.49302243/v1

Rowan W. 1925. Relation of light to bird migration and developmental changes. Nature, 115: 494–495. https://doi.org/10.1038/115494b0

Rowan W. 1926. On photoperiodism, reproductive periodicity, and the annual migrations of birds and certain fishes. Proceedings of the Boston Society of Natural History, 38: 147.

Rowan W. 1932. Experiments in bird miration. III. The effects of artificial light, castration and certain extracts on the autumn movements of the American crow (Corvus brachyrhynchos). Proceedings of the National Academy of Sciences, 18: 639–654. https://doi.org/10.1073/pnas.18.11.639

Saito E.-S., Kaiya H., Tachibana T., Tomonaga S., Denbow D.M., Kangawa K. and Furuse M. 2005. Inhibitory effect of ghrelin on food intake is mediated by the corticotropin-releasing factor system in neonatal chicks. Regulatory Peptides, 125(1): 201–208. https://doi.org/10.1016/j.regpep.2004.09.003

Sapolsky R.M., Romero L.M. and Munck A.U. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1): 55–89. https://doi.org/10.1210/edrv.21.1.0389

Schmaljohann H. 2018. Proximate mechanisms affecting seasonal differences in migration speed of avian species. Scientific Reports, 8(1): 4106. https://doi.org/10.1038/s41598-018-22421-7

Schmaljohann H., Eikenaar C. and Sapir N. 2022. Understanding the ecological and evolutionary function of stopover in migrating birds. Biological Reviews, 97(4): 1231–1252. https://doi.org/10.1111/brv.12839

Schmaljohann H., Kämpfer S., Fritzsch A., Kima R. and Eikenaar C. 2015. Start of nocturnal migratory restlessness in captive birds predicts nocturnal departure time in free-flying birds. Behavioral Ecology and Sociobiology, 69(6): 909–914. https://doi.org/10.1007/s00265-015-1902-4

Schmaljohann H., Liechti F. and Bruderer B. 2009. Trans-Sahara migrants select flight altitudes to minimize energy costs rather than water loss. Behavioral Ecology and Sociobiology, 63(11): 1609–1619. https://doi.org/10.1007/s00265-009-0758-x

Schwabl H., Bairlein F. and Gwinner E. 1991. Basal and stress-induced corticosterone levels of garden warblers, Sylvia borin, during migration. Journal of Comparative Physiology B, 161: 576–580. https://doi.org/10.1007/BF00260747

Schwabl H. and Farner D.S. 1989a. Dependency on Testosterone of Photoperiodically-Induced Vernal Fat Deposition in Female White-Crowned Sparrows. The Condor, 91(1): 108–112. https://doi.org/10.2307/1368153

Schwabl H. and Farner D.S. 1989b. Endocrine and Environmental Control of Vernal Migration in Male White-Crowned Sparrows, Zonotrichia leucophrys gambelli. Physiological Zoology, 62(1): 1–10. https://doi.org/10.1086/physzool.62.1.30159994

Schwabl H., Schwabl B., Goldsmith A.R. and Farner D.S. 1988. Effects of ovariectomy on long day-induced premigratory fat deposition, plasma levels of luteinizing hormone and prolactin, and molt in white-crowned sparrows, Zonotrichia leucophrys gambelli. General and Comparative Endocrinology, 71: 398–405. https://doi.org/10.1016/0016-6480(88)90268-7

Seroussi E., Knytl M., Pitel F., Elleder D., Krylov V., Leroux S., Morisson M., Yosefi S., Miyara S., Ganesan S., Ruzal M., Andersson L. and Friedman-Einat M. 2019. Avian Expression Patterns and Genomic Mapping Implicate Leptin in Digestion and TNF in Immunity, Suggesting That Their Interacting Adipokine Role Has Been Acquired Only in Mammals. International Journal of Molecular Sciences, 20(18): 4489. https://doi.org/10.3390/ijms20184489

Sharma A. and Kumar V. 2019. Metabolic plasticity mediates differential responses to spring and autumn migrations: Evidence from gene expression patterns in migratory buntings. Experimental Physiology: EP087974. https://doi.org/10.1113/EP087974

Sharma A., Singh D., Malik S., Gupta N.J., Rani S. and Kumar V. 2018. Difference in control between spring and autumn migration in birds: insight from seasonal changes in hypothalamic gene expression in captive buntings. Proceedings of the Royal Society B, 285: 20181531. https://doi.org/10.1098/rspb.2018.1531

Sharma A., Tripathi V. and Kumar V. 2022. Control and adaptability of seasonal changes in behavior and physiology of latitudinal avian migrants: Insights from laboratory studies in Palearctic-Indian migratory buntings. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337(9–10): 902–918. https://doi.org/10.1002/jez.2631

Sharp P.J., Dawson A. and Lea R.W. 1998. Control of luteinizing hormone and prolactin secretion in birds. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 119(3): 275–282. https://doi.org/10.1016/S0742-8413(98)00016-4

Shostak A., Meyer-Kovac J. and Oster H. 2013. Circadian Regulation of Lipid Mobilization in White Adipose Tissues. Diabetes, 62(7): 2195–2203. https://doi.org/10.2337/db12-1449

Singh D., Trivedi A.K., Rani S., Panda S. and Kumar V. 2015. Circadian timing in central and peripheral tissues in a migratory songbird: dependence on annual life-history states. The FASEB Journal, 29(10): 4248–4255. https://doi.org/10.1096/fj.15-275339

Sjöberg S., Malmiga G., Nord A., Andersson A., Bäckman J., Tarka M., Willemoes M., Thorup K., Hansson B., Alerstam T. and Hasselquist D. 2021. Extreme altitudes during diurnal flights in a nocturnal songbird migrant. Science, 372(6542): 646–648. https://doi.org/10.1126/science.abe7291

Smith J.P. 1982. Changes in blood levels of thyroid hormones in two species of passerine birds. The Condor, 84(2): 160–167. https://doi.org/10.2307/1367659

Sokolov L.V. and Tsvey A.L. 2016. Mechanisms controling the timing of spring migration in birds. Biology Bulletin, 43(9): 1148–1160. https://doi.org/10.1134/S1062359016110145

Sokolovskis K., Bianco G., Willemoes M., Solovyeva D., Bensch S. and Åkesson S. 2018. Ten grams and 13,000 km on the wing – route choice in willow warblers Phylloscopus trochilus yakutensis migrating from Far East Russia to East Africa. Movement Ecology, 6(1): 20. https://doi.org/10.1186/s40462-018-0138-0

Stevenson T.J. and Kumar V. 2017. Neural control of daily and seasonal timing of songbird migration. Journal of Comparative Physiology A, 203(6–7): 399–409. https://doi.org/10.1007/s00359-017-1193-5

Stevenson T.J., Liddle T.A., Stewart C., Marshall C.J. and Majumdar G. 2022. Neural programming of seasonal physiology in birds and mammals: A modular perspective. Hormones and Behavior, 142: 105153. https://doi.org/10.1016/j.yhbeh.2022.105153

Stuber E.F., Verpeut J., Horvat-Gordon M., Ramachandran R. and Bartell P.A. 2013. Differential Regulation of Adipokines May Influence Migratory Behavior in the White-Throated Sparrow (Zonotrichia albicollis). PLoS ONE, 8(6): e59097. https://doi.org/10.1371/journal.pone.0059097

Titov N. 2000. Interaction between foraging strategy and autumn migratory strategy in the Robin Erithacus rubecula. Avian Ecology and Behavior, 5: 35–44.

Tonra C.M., Marra P.P. and Holberton R.L. 2011. Early elevation of testosterone advances migratory preparation in a songbird. Journal of Experimental Biology, 214(16): 2761–2767. https://doi.org/10.1242/jeb.054734

Tonra C.M., Marra P.P. and Holberton R.L. 2013. Experimental and observational studies of seasonal interactions between overlapping life history stages in a migratory bird. Hormones and Behavior, 64(5): 825–832. https://doi.org/10.1016/j.yhbeh.2013.10.004

Tøttrup A.P., Klaassen R.H.G., Strandberg R., Thorup K., Kristensen M.W., Jorgensen P.S., Fox J., Afanasyev V., Rahbek C. and Alerstam T. 2012. The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration. Proceedings of the Royal Society B: Biological Sciences, 279(1730): 1008–1016. https://doi.org/10.1098/rspb.2011.1323

Totzke U., Hübinger A. and Bairlein F. 1997. A Role for Pancreatic Hormones in the Regulation of Autumnal Fat Deposition of the Garden Warbler (Sylvia borin)? General and Comparative Endocrinology, 107(2): 166–171. https://doi.org/10.1006/gcen.1997.6909

Totzke U., Hübinger A. and Bairlein F. 1998. Glucose utilization rate and pancreatic hormone response to oral glucose loads are influenced by the migratory condition and fasting in the garden warbler (Sylvia borin). Journal of Endocrinology, 158(2): 191–196. https://doi.org/10.1677/joe.0.1580191

Totzke U., Hübinger A., Dittami J. and Bairlein F. 2000. The autumnal fattening of the long-distance migratory garden warbler (Sylvia borin) is stimulated by intermittent fasting. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 170(8): 627–631. https://doi.org/10.1007/s003600000143

Trivedi A.K., Kumar J., Rani S. and Kumar V. 2014. Annual life history-dependent gene expression in the hypothalamus and liver of a migratory songbird: insights into the molecular regulation of seasonal metabolism. Journal of Biological Rhythms, 29(5): 332–345. https://doi.org/10.1177/0748730414549766

Trivedi A.K., Malik S., Rani S. and Kumar V. 2016. Pinealectomy abolishes circadian behavior and interferes with circadian clock gene oscillations in brain and liver but not retina in a migratory songbird. Physiology and Behavior, 156: 156–163. https://doi.org/10.1016/j.physbeh.2016.01.019

Trivedi A.K., Mishra I. and Kumar V. 2019. Temporal expression of genes coding for aryl-alkamine-N-acetyltransferase and melatonin receptors in circadian clock tissues: Circadian rhythm dependent role of melatonin in seasonal responses. Physiology and Behavior, 207: 167–178. https://doi.org/10.1016/j.physbeh.2019.05.009

Tsutsui K., Haraguchi S., Inoue K., Miyabara H., Suzuki S. and Ubuka T. 2012. Control of circadian activity of birds by the interaction of melatonin with 7α-hydroxypregnenolone, a newly discovered neurosteroid stimulating locomotion. Journal of Ornithology, 153: 235–243. https://doi.org/10.1007/s10336-011-0795-x

Tsvey A., Loshchagina J. and Naidenko S. 2019. Migratory Species Show Distinct Patterns in Corticosterone Levels during Spring and Autumn Migrations. Animal Migration, 6(1): 4–18. https://doi.org/10.1515/ami-2019-0003

Vaillancourt E. and Weber J.-M. 2015. Fuel metabolism in Canada geese: effects of glucagon on glucose kinetics. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 309(5): R535–R543. https://doi.org/10.1152/ajpregu.00080.2015

Van Doren B.M., Liedvogel M. and Helm B. 2017. Programmed and flexible: long-term Zugunruhe data highlight the many axes of variation in avian migratory behaviour. Journal of Avian Biology, 48(1): 155–172. https://doi.org/10.1111/jav.01348

Vandermeer C.L. 2013. The effect of testosterone on the spring migratory phenotype of a north american songbird (Zonotrichia albicollis). MS Thesis. The University of Western Ontario, Canada, 134 p.

Wang G., Ramenofsky M. and Wingfield J.C. 2013. Apparent dissociation of photoperiodic time measurement between vernal migration and breeding under dim green light conditions in Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii. Current Zoology, 59(3): 349–359. https://doi.org/10.1093/czoolo/59.3.349

Watts H.E., Cornelius J.M., Fudickar A.M., Pérez J. and Ramenofsky M. 2017. Understanding variation in migratory movements: A mechanistic approach. General and Comparative Endocrinology, 256: 112–122. https://doi.org/10.1016/j.ygcen.2017.07.027

Watts H.E., Rittenhouse J.L., Sewall K.B. and Bowers J.M. 2019. Migratory state is not associated with differences in neural glucocorticoid or mineralocorticoid receptor expression in pine siskins. Animal Migration, 6(1): 19–27. https://doi.org/10.1515/ami-2019-0001

Wikelski M., Tarlow E.M., Raim A., Diehl R.H., Larkin R.P. and Visser G.H. 2003. Costs of migration in free-flying songbirds: Avian metabolism. Nature, 423(6941): 704–704. https://doi.org/10.1038/423704a

Wingfield D.C., Schwabl H. and Mattocks P.W., Jr. 1990. Endocrine mechanisms of migration. In: E. Gwinner (Ed.). Bird migration: physiology and ecophysiology. Springer, Berlin, Heidelberg, New-York: 232–256. https://doi.org/10.1007/978-3-642-74542-3_16

Wingfield J.C. 2005. Flexibility in annual cycles of birds: implications for endocrine control mechanisms. Journal of Ornithology, 146(4): 291–304. https://doi.org/10.1007/s10336-005-0002-z

Wingfield J.C. and Farner D.S. 1975. The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding. Steroids, 26(3): 311–327. https://doi.org/10.1016/0039-128X(75)90077-X

Wingfield J.C., Hahn T.P., Wada M., Astheimer L.B. and Schoech S. 1996. Interrelationship of day length and temperature on the control of gonadal development, body mass, and fat score in white-crowned sparrows, Zonotrichia leucophrys gambelii. General and Comparative Endocrinology, 101(3): 242–255. https://doi.org/10.1006/gcen.1996.0027

Yan J., Yang H., Gan L. and Sun C. 2014. Adiponectin-impaired adipocyte differentiation negatively regulates fat deposition in chicken. Journal of Animal Physiology and Animal Nutrition, 98(3): 530–537. https://doi.org/10.1111/jpn.12107

Yang H., Yang T., Baur J.A., Perez E., Matsui T., Carmona J.J., Lamming D.W., Souza-Pinto N.C., Bohr V.A., Rosenzweig A., de Cabo R., Sauve A.A. and Sinclair D.A. 2007. Nutrient-Sensitive Mitochondrial NAD+ Levels Dictate Cell Survival. Cell, 130(6): 1095–1107. https://doi.org/10.1016/j.cell.2007.07.035

Zajac D.M., Cerasale D.J., Landman S. and Guglielmo C.G. 2011. Behavioral and physiological effects of photoperiod-induced migratory state and leptin on Zonotrichia albicollis: II. Effects on fatty acid metabolism. General and Comparative Endocrinology, 174(3): 269–275. https://doi.org/10.1016/j.ygcen.2011.08.024

Zinßmeister D., Troupin D. and Sapir N. 2022. Autumn migrating passerines at a desert edge: Do birds depart for migration after reaching a threshold fuel load or vary it according to the rate of fuel deposition? Frontiers in Ecology and Evolution, 10. https://doi.org/10.3389/fevo.2022.874923