Abstract
Migration in songbirds (order – Passeriformes) is a periodic movement between the breeding and overwintering grounds, located apart by several 1000 km. The migrating individuals face physiological challenges to cope with the demands imposed by long travels. The particularly important challenge is to meet energy cost of flight, in-flight supply of fuel, for which they need to store energy reserves in the form of fat. Long and uninterrupted migratory flight is facilitated by seasonal reduction in different organ weights and is made more efficient by enhancing the efficiency of metabolism, particularly the tricarboxylic acid (TCA) cycle. Most diurnal birds migrate at night, and with this they undergo shifts from diurnal to nocturnal patterns both in their behavioral and neural activities. Several of these seasonal alterations are under the circadian clock. In this chapter, our focus is on the brief mechanistic explanation for physiological, behavioral, biochemical, and molecular changes that occur during transition from the nonmigratory to migratory state in songbirds.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Shaffer SA, Tremblay Y, Weimerskirch H, Scott D, Thompson DR, Sagar PM, Moller H, Taylor GA, Foley DG, Block BA, Costa DP (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc Natl Acad Sci U S A 103:12799–12802
Gill REJ, Piersma T, Hufford G, Servranckx R, Riegen A (2005) Crossing the ultimate ecological barrier: evidence for a 11,000-km-long non-stop flight from Alaska to New Zealand and Eastern Australia by bar-tailed godwits. Condor 107:1–20
Moreau RE (1972) The Palaearctic-African bird migration system. Academic Press, London
Newton I (2008) The migration ecology of birds. Academic Press, London
Ramenofsky M, Wingfield JC (2007) Regulation of migration. Bioscience 57:135–143
Srivastava S, Rani S, Kumar V (2014) Photoperiodic induction of pre-migratory phenotype in a migratory songbird: identification of metabolic proteins in flight muscles. J Comp Physiol B 184:741–751
Trivedi AK, Kumar J, Rani S, 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. J Biol Rhythm 29:332–345
Trivedi AK, Malik S, Rani S, Kumar V (2015) Adaptation of oxidative phosphorylation to photoperiod-induced seasonal metabolic states in migratory songbirds. Comp Biochem Physiol A 184:34–40
Jain N, Kumar V (1995) Changes in food intake, body weight, gonads and plasma concentrations of thyroxine, luteinizing hormone and testosterone in captive male buntings exposed to natural day lengths at 29 N. J Biosci 20:417–426
Rani S, Malik S, Trivedi AK, Singh S, Kumar V (2006) A circadian clock regulates migratory restlessness in the blackheaded bunting, Emberiza melanocephala. Curr Sci 91:1093–1096
Rastogi A, Kumari Y, Rani S, Kumar V (2011) Phase inversion of neural activity in the olfactory and visual systems of a night-migratory bird during migration. Eur J Neurosci 34:99–109
Rastogi A, Kumari Y, Rani S, 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:e70065
Berthold P (1993) Physiological bases and control of bird migration. In: Berthold P (ed) Bird migration: a general survey. Oxford University Press, New York, pp 89–137
Bairlein F, Gwinner E (1994) Nutritional mechanisms and temporal control of migratory energy accumulation in birds. Annu Rev Nutr 14:187–215
Misra M, Rani S, Singh S, Kumar V (2004) Regulation of seasonality in the migratory male blackheaded bunting (Emberiza melanocephala). Reprod Nutr Dev 44:341–352
Herrera CM (1981) Fruit food of robins wintering in southern Spanish Mediterranean scrubland. Bird Study 28:115–122
Bairlein F (1998) The effect of diet composition on migratory fuelling in garden warblers Sylvia borin. J Avian Biol 29:546–551
Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528
Ramenofsky M (1990) Fat storage and fat metabolism in relation to migration. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer, New York, pp 214–231
Klasing KC (1998) Comparative avian nutrition. Cabi Publishing, CAB International, New York
Piersma T, Lindstrom A (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138
Gaunt AS, Hikida RS, Jehl JR, Fenbert L (1990) Rapid atrophy and hypertrophy of an avian flight muscle. Auk 107:649–659
Sabat P, Novoa F, Bozinovic F, Martinez del Rio C (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiol Zool 71:226–236
Piersma T (2002) Energetic bottlenecks and other design constraints in avian annual cycles. Integr Comp Biol 42:51–67
Dykstra CR, Karasov WH (1992) Changes in gut structure and function of house wrens (Troglodytes aedon) in response to increased energy demands. Physiol Zool 65:422–442
Egeler O, Williams TD, Guglielmo CG (2000) Modulation of lipogenic enzymes, fatty acid synthase and D9- desaturase, in relation to migration in the western sandpiper (Calidris mauri). J Comp Physiol B 170:169–174
Guglielmo CG, Haunerland NH, Williams TD (1998) Fatty acid binding protein, a major protein in the flight muscle of migrating western sandpipers. Comp Biochem Physiol B 119:549–555
McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940
Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am J Physiol 282:R1405–R1413
Wittenberg JB, Wittenberg BA (2003) Myoglobin function reassessed. J Exp Biol 206:2011–2020
Gessaman JA (1990) Body temperatures of migrant accipiter hawks just after flight. Wilson Bull 102:133–137
Fogden MPL (1972) Premigratory dehydration in the reed warbler Acrocephalus scirpaceus and water as a factor limiting migratory range. Ibis 114:548–552
Johnson OW, Morton ML, Bruner PL, Johnson PM (1989) Fat cyclicity predicted migratory flight ranges, and features of wintering behavior in Pacific Golden plovers. Condor 91:156–177
Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Costs of migration in free-flying songbirds. Nature 423:704
Carpenter FL, Hixon MA (1988) A new function for torpor: fat conservation in a wild migrant hummingbird. Condor 90:373–378
Gwinner E (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48
Helm B, Gwinner E, Trost L (2005) Flexible seasonal timing and migratory behavior: results from stonechat breeding programs. Ann N Y Acad Sci 1046:216–227
Helm B (2006) Zugunruhe of migratory and non-migratory birds in a circannual context. J Avian Biol 37:533–540
Bazzi G, Ambrosini R, Caprioli M, Constanzo A, Liechti F, Gatti E, Gianfranceschi L, Podofilllini S, Romano A, Romano M, Scandolara C, Saino N, Rubolini D (2015) Clock gene polymorphism and scheduling of migration: a geolocator study of the barn swallow Hirundo rustica. Sci Report 5:12443
McMillan JP, Gauthreaux SA, Helms CW (1970) Spring migratory restlessness in caged birds: a circadian rhythm. Bioscience 20:1256–1260
Bartell P, Gwinner E (2005) A separate circadian oscillator controls nocturnal migratory restlessness in a songbird, Sylvia borin. J Biol Rhythm 20:538–549
Kumar V, Singh BP, Rani S (2004) The Bird Clock: a complex multi-oscillatory and highly diversified system. Biol Rhythm Res 35:121–144
MacMillan JP (1972) Pinealectomy abolishes the circadian rhythm of migratory restlessness. J Comp Physiol 79:105–112
Trivedi AK, Malik S, Rani S, 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. Physiol Behav 156:156–163
Coverdill AJ, Bentley GE, Ramenofsky M (2008) Circadian and masking control of migratory restlessness in Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii). J Biol Rhythm 23:59–68
Singh J, Rastogi A, Rani S, Kumar V (2012a) Food availability affects circadian clock-controlled activity and zugunruhe in the night migratory male blackheaded bunting (Emberiza melanocephala). Chronobiol Int 29:15–25
Singh J, Budki P, Rani S, Kumar V (2012b) Temperature alters the photoperiodically controlled phenologies linked with migration and reproduction in a night-migratory songbird. Proc R Soc B 279:509–515
Holland RA, Thorup K, Gagliardo A, Bisson IA, Knecht E, Mizrahi D, Wikelski M (2009) Testing the role of sensory systems in the migratory heading of a songbird. J Exp Biol 212:4065–4071
Wallraff HG, Kiepenheuer J, Neumann MF, Streng A (1995) Homing experiments with starlings deprived of the sense of smell. Condor 97:20–26
Liedvogel M, Feenders G, Wada K, Troje NF, Jarvis ED, Mouritsen H (2007) Lateralized activation of cluster N in the brains of migratory songbirds. Eur J Neurosci 25:1166–1173
Zapka M, Heyers D, Liedvogel M, Jarvis ED, Mouritsen H (2010) Night-time neuronal activation of cluster N in a day- and night-migrating songbird. Eur J Neurosci 32:619–624
Cornelius JM, Boswell T, Jenni-Eiermann S, Breuner CW, Ramenofsky M (2013) Contributions of endocrinology to the migration life history of birds. Gen Comp Endocrinol 190:47–60
Corbel H, Groscolas R (2008) A role for corticosterone and food restriction in the fledging of nestling white storks. Horm Behav 53:557–566
Ramenofsky M, Cornelius JM, Helm B (2012) Physiological and behavioral responses of migrants to environmental cues. J Ornithol 153:181–191
Holberton RL, Boswell T, Hunter MJ (2008) Circulating prolactin and corticosterone concentrations during the development of migratory condition in the dark-eyed Junco, Junco hyemalis. Gen Comp Endocrinol 155:641–649
McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol A 128:579–593
Pathak VK, Chandola A (1982) Involvement of thyroid gland in the development of migratory disposition in the redheaded bunting, Emberiza bruniceps. Horm Behav 16:46–58
Cerasale DJ, Zajac DM, Guglielmo CG (2011) Behavioral and physiological effects of photoperiod-induced migratory state and leptin on a migratory bird, Zonotrichia albicollis: I. Anorectic effects of leptin administration. Gen Comp Endocrinol 174:276–286
Bartell P, Moore A (2013) Avian migration: the ultimate red-eye flight. Am Sci 101:46–55
Fusani L, Gwinner E (2005) Melatonin and nocturnal migration. Ann N Y Acad Sci 1046:264–270
Helm B, Gwinner E, Koolhaus A, Battley P, Schwabl I, Dekinga A, Piersma T (2012) Avian migration: temporal multitasking and a case study of melatonin cycles in waders. Prog Brain Res 199:457–479
Wojciechowski MS, Pinshow B (2009) Heterothermy in small, migrating passerine birds during stopover: use of hypothermia at rest accelerates fuel accumulation. J Exp Biol 212:3068–3075
Fusani L, Coccon F, Mora AR, Goymann W (2013) Melatonin reduces migratory restlessness in Sylvia warblers during autumnal migration. Front Zool 10:79
Malik S, Singh J, Trivedi AK, Singh S, Rani S, Kumar V (2015) Nocturnal melatonin levels decode daily light environment and reflect seasonal states in night-migratory blackheaded bunting (Emberiza melanocephala). Photochem Photobiol Sci 14:963–971
Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6:544–556
Kumar V, Singh BP (2006) The timekeeping system in birds. Proc Indian Natl Sci Acad 6:259–273
Peek CB, Ramsey KM, Marcheva B, Bass J (2012) Nutrient sensing and the circadian clock. Trends Endocrinol Metab 23:312–318
Marcheva B, Ramsey KM, Peek CB, Affinati A, Maury E, Bass J (2013) Circadian clocks and metabolism. Handb Exp Pharmacol 217:127–155
Feng D, Liu T, Sun Z, Bugge A, Mullican SE, Alenghat T, Liu XS, Lazar MA (2011) A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 331:1315–1319
Duez H, Staels B (2008) Rev-erb alpha gives a time cue to metabolism. FEBS Lett 582:19–25
Sun C, Zhang F, Ge X, Yan T, Chen X, Shi X, Zhai Q (2007) SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metab 6:307–319
Matsumoto M, Han S, Kitamura T, Accili D (2006) Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism. J Clin Investig 116:2464–2472
Ramadori G, Lee CE, Bookout AL, Lee S, Williams KW, Anderson J, Elmquist JK, Coppari R (2008) Brain SIRT1: anatomical distribution and regulation by energy availability. J Neurosci 28:9989–9996
Sasaki T, Kim HJ, Kobayashi M, Kitamura YI, Yokota-Hashimoto H, Shiuchi T, Minokoshi Y, Kitamura T (2010) Induction of hypothalamic Sirt1 leads to cessation of feeding via agouti-related peptide. Endocrinology 151:2556–2566
Edwards PA, Muroya H, Gould RG (1972) In vivo demonstration of the circadian rhythm of cholesterol biosynthesis in the liver and intestine of the rat. J Lipid Res 13:396–401
Latruffe N, Cherkaoui MM, Nicolas-Frances V, Clemencet MC, Jannin B, Berlot JP (2000) Regulation of the peroxisomal beta-oxidation-dependent pathway by peroxisome proliferator-activated receptor alpha and kinases. Biochem Pharmacol 60:1027–1032
Lodhi IJ, Wei X, Semenkovich CF (2011) Lipoexpediency: de novo lipogenesis as a metabolic signal transmitter. Trends Endocrinol Metab 22:1–8
Marsh RL (1981) Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the gray catbird (Dumetella carolinensis). J Comp Physiol B 141:417–423
Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool 71:1602–1608
Lin CC, Cheng TL, Tsai WH, Tsai HJ, Hu KH, Chang HC, Yeh CW, Chen YC, Liao CC, Chang WT (2012) Loss of the respiratory enzyme citrate synthase directly links the Warburg effect to tumor malignancy. Sci Report 2:785
Hansford RG (1980) Control of mitochondrial substrate oxidation. Curr Top Bioenerg 10:217–278
Zhang S, Hulver MW, McMillan RP, Cline MA, Gilbert ER (2014) The pivotal role of pyruvate dehydrogenase kinases in metabolic flexibility. Nutr Metab 11:10
Ramenofsky M, Wingfield JC (2006) Behavioral and physiological conflicts in migrants: the transition between migration and breeding. J Ornithol 147:135–145
Kumar V, Rani S, Singh BP (2006) Biological clocks help reduce the physiological conflicts in avian migrants. J Ornithol 147:281–286
Bauchinger U, Van't Hof T, Biebach H (2007) Testicular development during long-distance spring migration. Horm Behav 51:295–305
Morton ML (2002) The mountain white-crowned sparrow: migration and reproduction at high altitude. In: Cooper Ornithological Society Studies in avian biology. Cooper Ornithological Society, Camarillo.
Crossin GT, Trathan PN, Phillips RA, Dawson A, Le Bouard F, Williams TD (2010) A carryover effect of migration underlies individual variation in reproductive readiness and extreme egg size dimorphism in Macaroni Penguins. Am Nat 176:357–366
Gupta NJ, Kumar V (2013) Testes play a role in termination but not in initiation of the spring migration in the night-migratory blackheaded bunting. Anim Biol 63:321–329
Acknowledgments
Financial assistance from the Department of Biotechnology, New Delhi (BT/PR4984/MED/30/752/2012) was utilized in the preparation of this chapter.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer (India) Pvt. Ltd.
About this chapter
Cite this chapter
Rani, S., Singh, S., Malik, S., Kumar, V. (2017). Insights into the Regulation of Spring Migration in Songbirds. In: Kumar, V. (eds) Biological Timekeeping: Clocks, Rhythms and Behaviour. Springer, New Delhi. https://doi.org/10.1007/978-81-322-3688-7_30
Download citation
DOI: https://doi.org/10.1007/978-81-322-3688-7_30
Published:
Publisher Name: Springer, New Delhi
Print ISBN: 978-81-322-3686-3
Online ISBN: 978-81-322-3688-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)