Migratory Species Show Distinct Patterns in Corticosterone Levels during Spring and Autumn Migrations

References

[1] Hahn S., Bauer S., Liechti F., The natural link between Europe and Africa - 2.1 billion birds on migration, Oikos, 2009, 118, 624–62610.1111/j.1600-0706.2008.17309.xSearch in Google Scholar

[2] Newton I., The Migration ecology of birds, Academic Press, London, 2008Search in Google Scholar

[3] Newton I., Obligate and facultative migration in birds: ecological aspects, Journal of Ornithology, 2012, 153, 171–18010.1007/s10336-011-0765-3Search in Google Scholar

[4] Berthold P., Migration: control and metabolic physiology, In: Farner, D.S., King, J.R. (Eds.), Avian Biology, Academic Press, New York, 1975, 77–12810.1016/B978-0-12-249405-5.50010-0Search in Google Scholar

[5] Dolnik V.R., Migratsionnoe sostoyanie ptits (The Migratory Disposition of Birds), Nauka, Moscow, 1975Search in Google Scholar

[6] Ramenofsky M., Wingfield J.C., Regulation of migration, Bioscience, 2007, 57, 135–14310.1641/B570208Search in Google Scholar

[7] Jacobs J.D., Wingfield J.C., Endocrine control of life-cycle stages: a constraint on response to the environment?, Condor, 2000, 102, 35–5110.1093/condor/102.1.35Search in Google Scholar

[8] Wingfield J.C., Organization of vertebrate annual cycles: implications for control mechanisms, Philosophical Transactions of the Royal Society B: Biological Sciences, 2008, 363, 425–44110.1098/rstb.2007.2149Search in Google Scholar PubMed PubMed Central

[9] Cornelius J.M., Boswell T., Jenni-Eiermann S., Breuner C.W., Ramenofsky M., Contributions of endocrinology to the migration life history of birds, General and Comparative Endocrinology, 2013, 190, 47–6010.1016/j.ygcen.2013.03.027Search in Google Scholar PubMed

[10] Horton K.G., Van Doren B.M., Stepanian P.M., Farnsworth A., Kelly J.F., Seasonal differences in landbird migration strategies, The Auk, 2016, 133, 761–76910.1642/AUK-16-105.1Search in Google Scholar

[11] Nilsson C., Klaassen R.H.G., Alerstam T., Differences in speed and duration of bird migration between spring and autumn, The American Naturalist, 2013, 181, 837–84510.1086/670335Search in Google Scholar PubMed

[12] Schmaljohann H., Proximate mechanisms affecting seasonal differences in migration speed of avian species, Scientific Reports, 2018, 8, 410610.1038/s41598-018-22421-7Search in Google Scholar PubMed PubMed Central

[13] Ramenofsky M., Agatsuma R., Ramfar T., Environmental conditions affect the behavior of captive, migratory white-crowned sparrows, Condor, 2008, 110, 658–67110.1525/cond.2008.8523Search in Google Scholar

[14] Sharma A., Singh D., Malik S., Gupta N.J., Rani S., Kumar V., 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, 2018, 285, 2018153110.1098/rspb.2018.1531Search in Google Scholar PubMed PubMed Central

[15] Dawson A., King V.M., Bentley G.E., Ball G.F., Photoperiodic control of seasonality in birds, Journal of Biological Rhythms, 2001, 16, 365–38010.1177/074873001129002079Search in Google Scholar PubMed

[16] Ramenofsky M., Wingfield J.C., Behavioral and physiological conflicts in migrants: the transition between migration and breeding, Journal of Ornithology, 2006, 147, 135–14510.1007/s10336-005-0050-4Search in Google Scholar

[17] Wingfield D.C., Schwabl H., Mattocks P.W.Jr., Endocrine mechanisms of migration, In: Gwinner, E. (Ed.), Bird Migration: Physiology and Ecophysiology, Springer, Berlin, 1990, 232–256Search in Google Scholar

[18] Dyachenko V.P., The role of prolactin in regulation of seasonal migrations in some species of Passeriformes, PhD thesis, Zoological institute of Sovet Union academy of sciences, 1979, (in Russian)Search in Google Scholar

[19] Wingfield J.C., Flexibility in annual cycles of birds: implications for endocrine control mechanisms, Journal of Ornithology, 2005, 146, 291–30410.1007/s10336-005-0002-zSearch in Google Scholar

[20] Eikenaar C., Klinner T., Stöwe M., Corticosterone predicts nocturnal restlessness in a long-distance migrant, Hormones and Behavior, 2014, 66, 324–32910.1016/j.yhbeh.2014.06.013Search in Google Scholar PubMed

[21] Eikenaar C., Ballstaedt E., Hessler S., Klinner T., Müller F., Schmaljohann H., Cues, corticosterone and departure decisions in a partial migrant, General and Comparative Endocrinology, 2018, 261, 59–6610.1016/j.ygcen.2018.01.023Search in Google Scholar PubMed

[22] Eikenaar C., Endocrine regulation of fueling by hyperphagia in migratory birds, Journal of Comparative Physiology A, 2017, 203, 439–44510.1007/s00359-017-1152-1Search in Google Scholar PubMed

[23] Landys M.M., Ramenofsky M., Guglielmo C.G., Wingfield J.C., 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, 2004, 207, 143–15410.1242/jeb.00734Search in Google Scholar PubMed

[24] Lõhmus M., Sundstrom L.F., Moore F.R., Non-invasive corticosterone treatment changes foraging intensity in red-eyed vireos Vireo olivaceus, Journal of Avian Biology, 2006, 37, 523–52610.1111/j.0908-8857.2006.03733.xSearch in Google Scholar

[25] 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, Physiological and Biochemical Zoology, 2007, 80, 125–13710.1086/508816Search in Google Scholar

[26] Dolnik V.R., Blyumental T.I., Autumnal premigratory and migratory periods in the chaffinch (Fringilla coelebs coelebs) and some other temperate zone passerine birds, Condor, 1967, 69, 435–46810.2307/1366146Search in Google Scholar

[27] Lõhmus M., Sandberg R., Holberton R.L., Moore F.R., Corticosterone levels in relation to migratory readiness in red-eyed vireos (Vireo olivaceus), Behavioral Ecology and Sociobiology, 2003, 54, 233–23910.1007/s00265-003-0618-zSearch in Google Scholar

[28] Landys M.M., Wingfield J.C., Ramenofsky M., Plasma corticosterone increases during migratory restlessness in the captive white-crowned sparrow Zonotrichia leucophrys gambelli, Hormones and Behavior, 2004, 46, 574–58110.1016/j.yhbeh.2004.06.006Search in Google Scholar

[29] Eikenaar C., Müller F., Leutgeb C., Hessler S., Lebus K., Taylor P.D., et al., Corticosterone and timing of migratory departure in a songbird, Proceedings of the Royal Society B, 2017, 284, 2016230010.1098/rspb.2016.2300Search in Google Scholar

[30] Jenni L., Jenni-Eiermann S., Spina F., Schwabl H., Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight, Am J Physiol Regulatory Integrative Comp Physiol, 2000, 278, R1182–R118910.1152/ajpregu.2000.278.5.R1182Search in Google Scholar

[31] Falsone K., Jenni-Eiermann S., Jenni L., Corticosterone in migrating songbirds during endurance flight, Hormones and Behavior, 2009, 56, 548–55610.1016/j.yhbeh.2009.09.009Search in Google Scholar

[32] Romero L.M., Wingfield J.C., Tempests, poxes, predators, and people: stress in wild animals and how they cope, Oxford University Press, 201510.1093/acprof:oso/9780195366693.001.0001Search in Google Scholar

[33] Wingfield J.C., Romero L.M., Adrenocortical responses to stress and their modulation in free-living vertebrates, In: McEwen, B.C., Goodman, H.M. (Eds.), Handbook of Physiology; Section 7: The Endocrine System, Coping with the Environment: Neural and Endocrine Mechanisms, Oxford University Press, New York, 2001, 211–234Search in Google Scholar

[34] Romero L.M., Ramenofsky M., Wingfield J.C., Season and migration alters the corticosterone response to capture and handling in an Arctic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelii), Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 1997, 116, 171–17710.1016/S0742-8413(96)00208-3Search in Google Scholar

[35] Romero L.M., Wingfield J.C., 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, 1999, 122, 13–2010.1016/S0305-0491(98)10161-XSearch in Google Scholar

[36] Raja-aho S., Lehikoinen E., Suorsa P., Nikinmaa M., Vainio M., Vosloo D., et al., Corticosterone secretion patterns prior to spring and autumn migration differ in free-living barn swallows (Hirundo rustica L.), Oecologia, 2013, 173, 689–69710.1007/s00442-013-2669-9Search in Google Scholar

[37] Eikenaar C., Müller F., Klinner T., Bairlein F., Baseline corticosterone levels are higher in migrating than sedentary common blackbirds in autumn, but not in spring, General and Comparative Endocrinology, 2015, 224, 121–12510.1016/j.ygcen.2015.07.003Search in Google Scholar

[38] Bauer C.M., Graham J.L., Greives T.J., Corticosterone negative feedback is weaker during spring vs. autumn migration in a songbird (Junco hyemalis), General and Comparative Endocrinology, 2019, S001664801930043710.1016/j.ygcen.2019.04.008Search in Google Scholar

[39] O’Reilly K.M., Wingfield J.C., Seasonal, age, and sex differences in weight, fat reserves, and plasma corticosterone in Western Sandpipers, The Condor, 2003, 105, 13–2610.1093/condor/105.1.13Search in Google Scholar

[40] Tsipoura N., Scanes C.G., Burger J., Corticosterone and growth hormone levels in shorebirds during spring and fall migration stopover, Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 1999, 284, 645–65110.1002/(SICI)1097-010X(19991101)284:6<645::AID-JEZ6>3.0.CO;2-PSearch in Google Scholar

[41] Loshchagina J., Tsvey A., Naidenko S., Baseline and stress-induced corticosterone levels are higher during spring than autumn migration in European robins, Hormones and Behavior, 2018, 98, 96–10210.1016/j.yhbeh.2017.12.013Search in Google Scholar

[42] Ramenofsky M., Cornelius J.M., Helm B., Physiological and behavioral responses of migrants to environmental cues, Journal of Ornithology, 2012, 153, 181–19110.1007/s10336-012-0817-3Search in Google Scholar

[43] Watts H.E., Cornelius J.M., Fudickar A.M., Pérez J., Ramenofsky M., Understanding variation in migratory movements: A mechanistic approach, General and Comparative Endocrinology, 2017, 256, 112–12210.1016/j.ygcen.2017.07.027Search in Google Scholar

[44] Nilsson C., Bäckman J., Alerstam T., Seasonal modulation of flight speed among nocturnal passerine migrants: differences between short- and long-distance migrants, Behavioral Ecology and Sociobiology, 2014, 68, 1799–180710.1007/s00265-014-1789-5Search in Google Scholar

[45] Schaub M., Jenni L., Fuel deposition of three passerine bird species along the migration route, Oecologia, 2000, 122, 306–31710.1007/s004420050036Search in Google Scholar

[46] Jenni-Eiermann S., Energy metabolism during endurance flight and the post-flight recovery phase, J Comp Physiol A, 2017, 203, 431–43810.1007/s00359-017-1150-3Search in Google Scholar PubMed

[47] Gwinner E., Circadian and circannual programmes in avian migration, Journal of Experimental Biology, 1996, 199, 39–4810.1242/jeb.199.1.39Search in Google Scholar PubMed

[48] Berthold P., Genetics of Migration, In: Gwinner, E. (Ed.), Bird Migration, Springer, Berlin, Heidelberg, 1990, 269–28010.1007/978-3-642-74542-3_18Search in Google Scholar

[49] Wikelski M., Martin L.B., Scheuerlein A., Robinson M.T., Robinson N.D., Helm B., et al., Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control, Philosophical Transactions of the Royal Society B: Biological Sciences, 2008, 363, 411–42310.1098/rstb.2007.2147Search in Google Scholar PubMed PubMed Central

[50] Sokolov L.V., Tsvey A.L., Mechanisms controling the timing of spring migration in birds, Biology Bulletin, 2016, 43, 1148–116010.1134/S1062359016110145Search in Google Scholar

[51] Romero L.M., Bauer C.M., de Bruijn R., Lattin C.R., Seasonal Rhythms, In: Stress: Neuroendocrinology and Neurobiology, Elsevier, 2017, 421–42710.1016/B978-0-12-802175-0.00042-5Search in Google Scholar

[52] Ramenofsky M., Wingfield J.C., Regulation of complex behavioural transitions: migration to breeding, Animal Behaviour, 2016, 124, 299–30610.1016/j.anbehav.2016.09.015Search in Google Scholar

[53] Schmaljohann H., Lisovski S., Bairlein F., Flexible reaction norms to environmental variables along the migration route and the significance of stopover duration for total speed of migration in a songbird migrant, Frontiers in Zoology, 2017, 14, 1710.1186/s12983-017-0203-3Search in Google Scholar PubMed PubMed Central

[54] Long J.A., Holberton R.L., Corticosterone secretion, energetic condition, and test of the migration modulation hypothesis in the hermit thrush (Catharus guttatus), a short-distance migrant, The Auk, 2004, 121, 1094–110210.2307/4090478Search in Google Scholar

[55] Sandberg R., Moore F.R., Fat stores and arrival on the breeding grounds: reproductive consequences for passerine migrants, Oikos, 1996, 577–58110.2307/3545949Search in Google Scholar

[56] Deutschlander M.E., Muheim R., Fuel reserves affect migratory orientation of thrushes and sparrows both before and after crossing an ecological barrier near their breeding grounds, Journal of Avian Biology, 2009, 40, 85–8910.1111/j.1600-048X.2008.04343.xSearch in Google Scholar

[57] McCabe J.D., Leppold A.J., Holberton R.L., Olsen B.J., Coastal songbird condition on migratory stopover varies by geographical location and bird age, The Auk, 2019, 136, ukz02510.1093/auk/ukz025Search in Google Scholar

[58] Payevsky, V.A., Atlas of bird migration according to the banding data on the Courland Spit, In: Bird Migrations—Ecological and Physiological Factors, Willey, New York, 1973, 1–124Search in Google Scholar

[59] Payevsky V.A., Shapoval, A.P., Vysotsky, V.G., Spatial distribution of thrushes migrating through the Eastern Baltic area as shown by ring recoveries, OMPO Newsletter, 2005, 25, 5–12Search in Google Scholar

[60] Tsvey A.L., Migratory strategy of Robins (Erithacus rubecula) in Eastern Baltic, PhD Thesis, Zoological institute RAS, Saint-Petersburg, 2008 (in Russian)Search in Google Scholar

[61] Sinelschikova A., Griffiths M., Vorotkov M., Bulyuk V., Bolshakov C., Airspeed of the song thrush in relation to the wind during autumnal nocturnal migration, Ornis Fennica, 2019, 96, 64-76Search in Google Scholar

[62] Hall-Karlsson K.S.S., Fransson T., How far do birds fly during one migratory flight stage?, Ringing & Migration, 2008, 24, 95–10010.1080/03078698.2008.9674381Search in Google Scholar

[63] Chernetsov N., Titov N., Design of a trapping station for studying migratory stopovers by capture-mark-recapture analysis, Avain Ecology and Behaviour, 2000, 5, 27–33Search in Google Scholar

[64] Romero L.M., Physiological stress in ecology: lessons from biomedical research, Trends in Ecology & Evolution, 2004, 19, 249–25510.1016/j.tree.2004.03.008Search in Google Scholar PubMed

[65] R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/Search in Google Scholar

[66] Zuur A.F., Ieno E.N., Elphick C.S., A protocol for data exploration to avoid common statistical problems: Data exploration, Methods in Ecology and Evolution, 2010, 1, 3–1410.1111/j.2041-210X.2009.00001.xSearch in Google Scholar

[67] Zuur A.F., Ieno, E.N., Walker N.J., Saveliev, A.A., Smith, G.M., Mixed effects models and extensions in ecology with R, Springer, New York, 200910.1007/978-0-387-87458-6Search in Google Scholar

[68] Bates D., Martin M., Bolker B., Walker S., Fitting Linear Mixed-Effects Models Using lme4., Journal of Statistical Software, 2015, 67, 1–4810.18637/jss.v067.i01Search in Google Scholar

[69] Kuznetsova A., Brockhoff P.B., Christensen R.H.B., “lmerTest”: R package version 2.0-33, 2016Search in Google Scholar

[70] Korner-Nievergelt F., Von Felten S., Roth T., Almasi B., Guélat J., Korner-Nievergelt P., Bayesian data analysis in ecology using linear models with R, Bugs, and Stan, Elsevier/AP, Academic Press, Amsterdam ; Boston, 201510.1016/B978-0-12-801370-0.00004-6Search in Google Scholar

[71] Eikenaar C., Fritzsch A., Bairlein F., Corticosterone and migratory fueling in Northern wheatears facing different barrier crossings, Gen. Comp. Endocrinol., 2013, 186, 181–18610.1016/j.ygcen.2013.02.042Search in Google Scholar PubMed

[72] Fanson K.V., Németh Z., Ramenofsky M., Wingfield J.C., Buchanan K.L., Inter-laboratory variation in corticosterone measurement: Implications for comparative ecological and evolutionary studies, Methods in Ecology and Evolution, 2017, 8, 1745-175410.1111/2041-210X.12821Search in Google Scholar

[73] Romero L.M., Gormally B.M.G., How truly conserved is the “well-conserved” vertebrate stress response?, Integrative and Comparative Biology, 2019, 59, 273–28110.1093/icb/icz011Search in Google Scholar

[74] Sapolsky R.M., Romero L.M., Munck A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions, Endocrine Reviews, 2000, 21, 55–8910.1210/edrv.21.1.0389Search in Google Scholar

[75] 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, General and Comparative Endocrinology, 2006, 148, 132–14910.1016/j.ygcen.2006.02.013Search in Google Scholar

[76] Romero L.M., Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates, General and Comparative Endocrinology, 2002, 128, 1–2410.1016/S0016-6480(02)00064-3Search in Google Scholar

[77] Wingfield J.C., Ramenofsky M., Hormone-behavior interrelationships of birds in response to weather, In: Advances in the Study of Behavior, Elsevier, 2011, 93–18810.1016/B978-0-12-380896-7.00003-4Search in Google Scholar

[78] Landys-Ciannelli M.M., Ramenofsky M., Piersma T., Jukema J., Group C.R., Wingfield J.C., Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica, Physiological and Biochemical Zoology, 2002, 75, 101–11010.1086/338285Search in Google Scholar PubMed

[79] Wagner D.N., Green D.J., Cooper J.M., Love O.P., Williams T.D., Variation in plasma corticosterone in migratory songbirds: a test of the migration-modulation hypothesis, Physiological and Biochemical Zoology, 2014, 87, 695–70310.1086/676937Search in Google Scholar PubMed

[80] Holberton R.L., Parrish J.D., Wingfield J.C., Modulation of the adrenocortical stress response in neortopical migrants during autumn migration, Auk, 1996, 113, 558–56410.2307/4088976Search in Google Scholar

[81] Romero L.M., Reed J.M., Collecting baseline corticosterone samples in the field: is under 3 min good enough?, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2005, 140, 73–7910.1016/j.cbpb.2004.11.004Search in Google Scholar PubMed

[82] Small T.W., Bebus S.E., Bridge E.S., Elderbrock E.K., Ferguson S.M., Jones B.C., et al., Stress-responsiveness influences baseline glucocorticoid levels: Revisiting the under 3 min sampling rule, General and Comparative Endocrinology, 2017, 247, 152–16510.1016/j.ygcen.2017.01.028Search in Google Scholar PubMed

[83] Raja-aho S., Suorsa P., Vainio M., Nikinmaa M., Lehikoinen E., Eeva T., Body condition is associated with adrenocortical response in the barn swallow (Hirundo rustica L.) during early stages of autumn migration, Oecologia, 2010, 163, 323–33210.1007/s00442-009-1553-0Search in Google Scholar PubMed

[84] Ramenofsky M., Piersma T., Jukema J., Plasma corticosterone in bar-tailed godwits at a major stop-over site during spring migration, The Condor, 1995, 97, 580–58510.2307/1369045Search in Google Scholar

[85] Huber N., Fusani L., Ferretti A., Mahr K., Canoine V., Measuring short-term stress in birds: Comparing different endpoints of the endocrine-immune interface, Physiology & Behavior, 2017, 182, 46–5310.1016/j.physbeh.2017.09.017Search in Google Scholar PubMed

[86] Breuner C.W., Patterson S.H., Hahn T.P., In search of relationships between the acute adrenocortical response and fitness, General and Comparative Endocrinology, 2008, 157, 288–29510.1016/j.ygcen.2008.05.017Search in Google Scholar PubMed

[87] Breuner C.W., Berk S.A., Using the van Noordwijk and de Jong resource framework to evaluate glucocorticoid-fitness hypotheses, Integrative and Comparative Biology, 2019, 59, 243–25010.1093/icb/icz088Search in Google Scholar PubMed