Skip to main content
SpringerLink
Log in

Endocrine regulation of fueling by hyperphagia in migratory birds

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

To support migratory endurance flight, birds accumulate large amounts of fat by hyperphagia (fueling). Whereas the factors influencing migrants’ motivation to fuel are well described, the physiological mechanism regulating fueling is largely unknown. Hormones are likely involved and arguably the best studied with respect to food intake and fueling is corticosterone. Corticosterone has a permissive effect, as blocking the hormone’s actions prohibits efficient fueling. There are no indications, though that corticosterone stimulates fueling, and some studies even observed negative correlations between corticosterone level and food intake and speed of fueling. The latter is unexpected as slow fueling could reduce the overall speed of migration. To test the causality of these negative correlations, I non-invasively increased circulating corticosterone levels in captive migrants and determined its effect on food intake and fuel accumulation. Neither food intake nor fuel accumulation differed between corticosterone-treated and control-treated individuals. This indicates that corticosterone does not hamper food intake and fueling during stopovers, nor does it stimulate these processes. Promising alternative candidates for the regulation of migratory hyperphagia are ‘appetite regulating’ hormones secreted by the adipose tissue, gut, or gastro-intestinal tract. The advance of next-generation sequencing will facilitate a bottom-up approach when investigating these.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Bauchinger U, Van’t Hof T, Biebach H (2008) Migratory stopover conditions affect the developmental state of male gonads in garden warblers (Sylvia borin). Horm Behav 54:312–318

    Article  CAS  PubMed  Google Scholar 

  • Bayly NJ (2006) Optimality in avian migratory fuelling behavior: a study of a trans-Saharan migrant. Anim Behav 71:173–182

    Article  Google Scholar 

  • Bayly NJ (2007) Extreme fattening by sedge warblers, Acrocephalus schoenobaenus, is not triggered by food availability alone. Anim Behav 74:471–479

    Article  Google Scholar 

  • Berthold P, Fiedler W, Querner U (2000) Migratory restlessness or Zugunruhe in birds—a description based on video recordings under infrared illumination. J Ornithol 141:285–299

    Article  Google Scholar 

  • Biebach H (1985) Sahara stopover in migratory flycatchers: fat and food affect the time program. Experientia 41:695–697

    Article  Google Scholar 

  • Boswell T, Dunn IC (2015) Regulation of the avian central melanocortin system and the role of leptin. Gen Comp Endocrinol 221:278–283

    Article  CAS  PubMed  Google Scholar 

  • Breuner CW, Greenberg AL, Wingfield JC (1998) Noninvasive corticosterone treatment rapidly increases activity in Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii). Gen Comp Endocrin 111:386–394

    Article  CAS  Google Scholar 

  • Chernetsov N (2012) Passerine migration: stopovers and flight. Springer, Berlin

    Book  Google Scholar 

  • Conway-Campbell BL, Pooley JR, Hager GL, Lightman SL (2012) Molecular dynamics of ultradian glucocorticoid receptor action. Mol Cell Endocrinol 348:383–393

    Article  CAS  PubMed  Google Scholar 

  • Corman AM, Bairlein F, Schmaljohann H (2014) The nature of the migration route shapes physiological traits and aerodynamic properties in a migratory songbird. Behav Ecol Sociobiol 68:391–402

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dakin CL, Small CJ, Batterham RL, Neary NM, Cohen MA, Patterson M, Ghatei MA, Bloom SR (2004) Peripheral oxyntomodulin reduces food intake and body weight gains in rats. Endocrinology 145:687–2695

    Article  Google Scholar 

  • Delingat J, Dierschke V, Schmaljohann H, Mendel B, Bairlein F (2006) Daily stopovers as optimal migration strategy in a long-distance migrating passerine: the northern wheatear Oenanthe oenanthe. Ardea 94:593–605

    Google Scholar 

  • Denbow DM (1989) Centrally and peripherally administered bombesin decreases food intake in turkeys. Peptide 10:275–279

    Article  CAS  Google Scholar 

  • Dickmeis T, Weger BD, Weger M (2013) The circadian clock and glucocorticoids—Interactions across many time scales. Mol Cell Endocrinol 380:2–15

    Article  CAS  PubMed  Google Scholar 

  • Eikenaar C, Schläfke JL (2013) Size and accumulation of fuel reserves at stopover predict nocturnal restlessness in a migratory bird. Biol Lett 9:20130712

    Article  PubMed  PubMed Central  Google Scholar 

  • Eikenaar C, Fritzsch A, Bairlein F (2013) Corticosterone and migratory fueling in northern wheatears facing different barrier crossings. Gen Comp Endocrin 186:181–186

    Article  CAS  Google Scholar 

  • Eikenaar C, Klinner T, Szostek KL, Bairlein F (2014a) Migratory restlessness in captive individuals predicts actual departure in the wild. Biol Lett 10:20140154

    Article  PubMed  PubMed Central  Google Scholar 

  • Eikenaar C, Bairlein F, Stöwe M, Jenni-Eiermann S (2014b) Corticosterone, food intake and refueling in a long-distance migrant. Horm Behav 65:480–487

    Article  CAS  PubMed  Google Scholar 

  • Eikenaar C, Klinner T, Stöwe M (2014c) Corticosterone predicts nocturnal restlessness in a long-distance migrant. Horm Behav 66:324–329

    Article  CAS  PubMed  Google Scholar 

  • Eikenaar C, Tsvey A, Schmaljohann H (2015) Faster spring migration in northern wheatears is not explained by an endogenous seasonal difference in refueling rates. J Avian Biol 46:616–621

    Article  Google Scholar 

  • Forlenza GP, Calhoun A, Beckman KB, Halvorsen T, Hamdoun E, Zierhut H, Sarafoglou K, Plogreen LE, Miller, BS, Nathan B, Petryk A (2015) Next generation sequencing in endocrine practice. Mol Genet Metab 115:61–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fransson T (1998) Patterns of migratory fueling in whitethroats Sylvia communis in relation to departure. J Avian Biol 29:569–573

    Article  Google Scholar 

  • Friedman JM, Halaas JM (1998) Leptin and the regulation of body weight in mammals. Nature 395:763–770

    Article  CAS  PubMed  Google Scholar 

  • Fusani L, Coccon F, Rojas Mora A, Goymann W (2013) Melatonin reduces migratory restlessness in Sylvia warblers during autumnal migration. Front Zool 10:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibbs J, Fauser DJ, Rowe EA, Rolls BJ, Rolls ET, Maddison SP (1979) Bombesin suppresses feeding in rats. Nature 282:208–210

    Article  CAS  PubMed  Google Scholar 

  • Gwinner E, Schwabl H, Schwabl-Benzinger I (1988) Effects of food-deprivation on migratory restlessness and diurnal activity in the garden warbler. Oecologia 77:321–326

    Article  CAS  PubMed  Google Scholar 

  • Hameed S, Dhillo WS, Bloom SR (2009) Gut hormones and appetite control. Oral Dis 15:18–26

    Article  CAS  PubMed  Google Scholar 

  • Holberton RL, Wilson CM, Hunter MJ, Cash WB, Sims CG (2007) The role of corticosterone in supporting migratory lipogenesis in the dark-eyed junco, Junco hyemalis: a model for central and peripheral regulation. Phys Biochem Zool 80:125–137

    Article  CAS  Google Scholar 

  • Hume ID, Biebach H (1996) Digestive tract function in the long-distance migratory garden warbler, Sylvia borin. J Comp Physiol B 166:388–395

    Article  Google Scholar 

  • Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528

    Article  Google Scholar 

  • Jenni L, Schaub M (2003) Behavioural and physiological reactions to environmental variation in bird migration: a review. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin, Heidelberg, pp 155–171

    Chapter  Google Scholar 

  • Kaiya H, Kangawa K, Miyazato M (2013) What is the general action for ghrelin in vertebrates?—Comparisons of ghrelin’s effects across vertebrates. Gen Comp Endocrinol 181:187–191

    Article  CAS  PubMed  Google Scholar 

  • Kraus RHS, Wink M (2015) Avian genomics: fledging into the wild! J Ornithol 156:851–865

    Article  Google Scholar 

  • Landys MM, Ramenofsky M, Guglielmo CG, Wingfield JC (2004) The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii. J Exp Biol 207:143–154

    Article  CAS  PubMed  Google Scholar 

  • Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149

    Article  CAS  PubMed  Google Scholar 

  • Landys-Cianelli MM, Ramenofsky M, Piersma T, Jukema J, Castricum Ringing Group, Wingfield JC (2002) Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Phys Biochem Zool 75:101–110

    Article  Google Scholar 

  • Lerner HRL, Fleischer RC (2010) Prospects for the use of next generation sequencing methods in ornithology. Auk 127:4–15

    Article  Google Scholar 

  • Lõhmus M, Sandberg R, Holberton RL, Moore FR (2003) Corticosterone levels in relation to migratory readiness in red-eyed vireos (Vireo olivaceus). Behav Ecol Sociobiol 54:233–239

    Article  Google Scholar 

  • Lõhmus M, Sundström LF, Moore FR (2006) Non-invasive corticosterone treatment changes foraging intensity in red-eyed vireos. J Avian Biol 37:523–526

    Article  Google Scholar 

  • Owen JC, Garvin MC, Moore FR (2014) Elevated testosterone advances onset of migratory restlessness in a nearctic-neotropical landbird. Behav Ecol Sociobiol 68:561–569

    Article  Google Scholar 

  • Ramenofsky M (2011) Hormones in migration and reproductive cycles of birds. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates. Academic Press, London, pp 181–204

    Google Scholar 

  • Rasbash J, Steele F, Browne WJ, Goldstein H (2012) A user’s guide to MLwiN, version 2.26

  • Richardson RD, Boswell T, Weatherford SC, Wingfield JC, Woods SC (1993) Cholecystokinin octapeptide decreases food intake in white-crowned sparrows. Am J Physiol 264:R852–R856

    CAS  PubMed  Google Scholar 

  • Rodriguez-Sinovas A, Fernandez E, Manteca X, Fernandez G, Gonalons E (1997) CCK is involved in both peripheral and central mechanisms controlling food intake in chickens. Am J Physiol 272:R334–R340

    CAS  PubMed  Google Scholar 

  • Savory CJ (1987) An alternative explanation for apparent satiating properties of peripherally administered bombesin and cholecystokenin in domestic fowls. Physiol Behav 39:191–202

    Article  CAS  PubMed  Google Scholar 

  • Schaub M, Jenni L, Bairlein F (2008) Fuel stores, fuel accumulation, and the decision to depart from a migration stopover site. Behav Ecol 19:657–666

    Article  Google Scholar 

  • Schmaljohann H, Naef-Daenzer B (2011) Body condition and wind support initiate the shift of migratory direction and timing of nocturnal departure in a songbird. J Anim Ecol 80:1115–1122

    Article  PubMed  Google Scholar 

  • Shousha S, Nakahara K, Nasu T, Sakamoto T, Murakami N (2007) Effect of glucagon-like peptide-1 and -2 on regulation of food intake, body temperature and locomotor activity in the Japanese quail. Neurosci Lett 415:102–107

    Article  CAS  PubMed  Google Scholar 

  • Stanley S, Wynne K, McGowan B, Bloom S (2005) Hormonal regulation of food intake. Physiol Rev 85:1131–1158

    Article  CAS  PubMed  Google Scholar 

  • Stuber EF, Verpeut J, Horvat-Gordon M, Ramachandran R, Bartell PA (2013) Differential regulation of adipokines may influence migratory behavior in the white-throated sparrow (Zonotrichia albicollis). PLos One. doi:10.1371/journal.pone.0059097

    Google Scholar 

  • Tang-Christensen M, Vrang N, Larsen PJ (2001) Glucagon-like peptide containing pathways in the regulation of feeding behaviour. Int J Obes Relat Metab Disord 25:S42–S47

    Article  CAS  PubMed  Google Scholar 

  • Tonra CM, Marra PP, Holberton RL (2011) Early elevation of testosterone advances migratory preparation in a songbird. J Exp Biol 214:2761–2767

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Schwabl H, Mattock PW Jr (1990) Endocrine mechanisms of migration. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 232–256

    Chapter  Google Scholar 

  • Wynne K, Stanley S, McGowan B, Bloom S (2005) Appetite control. J Endocrinol 184:291–318

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I thank guest editors Franz Bairlein and Wolfgang Wiltschko for the invitation to write this paper, and Sven Hessler for help with the experiment. Three reviewers provided useful comments.

Author information

Authors and Affiliations

  1. Institute of Avian Research, An der Vogelwarte 21, 26386, Wilhelmshaven, Germany

    Cas Eikenaar

Authors
  1. Cas Eikenaar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cas Eikenaar.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-017-1152-1

Keywords

Search

Navigation