Skip to main content
SpringerLink
Log in

Clocks and Calendars in Birds

  • Chapter
  • First Online:
Neuroendocrine Clocks and Calendars

Part of the book series: Masterclass in Neuroendocrinology ((MANEURO,volume 10))

Abstract

Among research on biological rhythms, avian studies stand out through their embedding of neuroendocrinology in evolutionary and ecological contexts. Birds differ from mammals by generally being diurnal, by using input pathways of photic information to daily and annual timing that may not require the eyes, and by an interconnected multiple pacemaker system in the brain. Although there are considerable differences among avian species, the pineal gland and retina can function as complete mini-clocks featuring photoreception, sustained rhythm generation, and output generation. Melatonin is produced mainly in the pineal gland and, in many avian species, plays an important role in circadian rhythmicity, but not in annual cyclicity. The avian suprachiasmatic nucleus (SCN) is less critical for rhythmicity than in mammals, although most clock functions are available within its two paired nuclei. Possibly facilitated by the multiple pacemaker system, avian circadian clocks are remarkably plastic, especially during migration seasons when many species spontaneously assume nocturnal activity. The annual cycles of birds are underpinned by an interaction of circannual rhythms with strong photoperiodism. It is unclear how these ancient timing mechanisms will cope with rapidly changing temporal environments as circadian disruption by artificial light at night and annual cycle shifts in response to global warming become ever more evident.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abraham U, Albrecht U, Gwinner E, Brandstatter R (2002) Spatial and temporal variation of passer Per2 gene expression in two distinct cell groups of the suprachiasmatic hypothalamus in the house sparrow (Passer domesticus). Eur J Neurosci 16:429–436

    Article  PubMed  Google Scholar 

  • Agarwal N, Mishra I, Komal R, Rani S, Kumar V (2017) Circannual testis and moult cycles persist under photoperiods that disrupt circadian activity and clock gene cycles in spotted munia. J Exp Biol 220:4162–4168

    Article  PubMed  Google Scholar 

  • Akesson S, Ilieva M, Karagicheva J, Rakhimberdiev E, Tomotani B, Helm B (2017) Timing avian long-distance migration: from internal clock mechanisms to global flights. Philos Trans R Soc Lond Ser B Biol Sci 372

    Google Scholar 

  • Aschoff J (1967) Circadian rhythms in birds. Proc. XIVth Intern. Orn. Congr, Oxford

    Google Scholar 

  • Ashley NT, Ubuka T, Schwabl I, Goymann W, Salli BM, Bentley GE, Buck CL (2014) Revealing a circadian clock in captive arctic-breeding songbirds, Lapland longspurs (Calcarius lapponicus), under constant illumination. J Biol Rhythm 29:456–469

    Article  CAS  Google Scholar 

  • Ball GF, Ketterson ED (2008) Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philosophical Transactions of the Royal Society B: Biological Sciences 363:231–246

    Article  Google Scholar 

  • Bartell PA, Gwinner E (2005) A separate circadian oscillator controls nocturnal migratory restlessness in the songbird Sylvia borin. J Biol Rhythm 20:538–549

    Article  Google Scholar 

  • Besharse JC, Mcmahon DG (2016) The retina and other light-sensitive ocular clocks. J Biol Rhythm 31:223–243

    Article  CAS  Google Scholar 

  • Bluhm CK, Schwabl H, Schwabl I, Perera A, Follett BK, Goldsmith AR, Gwinner E (1991) Variation in hypothalamic gonadotrophin-releasing hormone content, plasma and pituitary LH, and in-vitro testosterone release in a long-distance migratory bird, the garden warbler (Sylvia borin), under constant photoperiods. J Endocrinol 128:339–345

    Article  CAS  PubMed  Google Scholar 

  • Caro SP, Schaper SV, Hut RA, Ball GF, Visser ME (2013) The case of the missing mechanism: how does temperature influence seasonal timing in endotherms? PLoS Biol 11:e1001517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cassone VM (2014) Avian circadian organization: a chorus of clocks. Front Neuroendocrinol 35:76–88

    Article  PubMed  Google Scholar 

  • Cassone VM, Paulose JK, Harpole CE, Li Y, Whitfield-Rucker M (2017) Avian circadian organization. In: Kumar V (ed) Biological timekeeping: clocks, rhythms and behavior. New Delhi, Springer India

    Google Scholar 

  • Chandola-Saklani A, Negi K, Kathait A (2015) A brief exposure to thyroxine synchronizes the circannual testicular cycle and associated molt in the subtropical spotted munia (Lonchura punctulata). J Ornithol 156:453–461

    Article  Google Scholar 

  • Davies WIL, Turton M, Peirson SN, Follett BK, Halford S, Garcia-Fernandez JM, Sharp PJ, Hankins MW, Foster RG (2012) Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol Lett 8:291–294

    Article  PubMed  Google Scholar 

  • Dominoni D, Goymann W, Helm B, Partecke J (2013a) Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds. Front Zool 10:60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dominoni DM, Helm B, Lehmann M, Dowse HB, Partecke J (2013b) Clocks for the city: circadian differences between forest and city songbirds. Proc Biol Sci 280:20130593

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dominoni DM, Quetting M, Partecke J (2013c) Long-term effects of chronic light pollution on seasonal functions of European blackbirds (Turdus merula). PLoS One 8:e85069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Falchi F, Cinzano P, Duriscoe D, Kyba CCM, Elvidge CD, Baugh K, Portnov BA, Rybnikova NA, Furgoni R (2016) The new world atlas of artificial night sky brightness. Sci Adv 2

    Google Scholar 

  • Foster RG, Follett BK (1985) The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J Comp Physiol A 157:519–528

    Article  CAS  Google Scholar 

  • Foster RG, Kreitzman L (2009) Seasons of life: The biological rhythms that enable living things to thrive and survive. Yale University Press, New Haven, CT

    Google Scholar 

  • Fusani L, Gahr M (2015) Differential expression of melatonin receptor subtypes MelIa, MelIb and MelIc in relation to melatonin binding in the male songbird brain. Brain Behav Evol 85:4–14

    Article  PubMed  Google Scholar 

  • Gänshirt G, Daan S, Gerkema MP (1984) Arrhythmic perch hopping and rhythmic feeding of starlings in constant light: separate circadian oscillators? J Comp Physiol A 154:669–674

    Article  Google Scholar 

  • Gwinner E (1966) Entrainment of a circadian rhythm in birds by species-specific song cycles (Aves, Fringillidae: Carduelis spinus, Serinus serinus). Experientia (Basel) 22:765

    Article  Google Scholar 

  • Gwinner E (1974) Testosterone induces "splitting" of circadian Locomotor activity rhythms in birds. Science 185:72–74

    Article  CAS  PubMed  Google Scholar 

  • Gwinner E (1986) Circannual rhythms. Berlin, Springer, Heidelberg

    Book  Google Scholar 

  • Gwinner E (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48

    CAS  PubMed  Google Scholar 

  • Gwinner E, Brandstätter R (2001) Complex bird clocks. Philos Trans R Soc Lond B 356:1801–1810

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hau M, Wikelski M, Wingfield JC (1998) A neotropical forest bird can measure the slight changes in tropical photoperiod. Proceedings of the Royal Society of London Series B- Biological Sciences 265:89–95

    Article  Google Scholar 

  • Helfer G, Barrett P, Morgan PJ (2019) A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals. J Neuroendocrinol 31:e12680

    Article  PubMed  CAS  Google Scholar 

  • Helm B (2009) Geographically distinct reproductive schedules in a changing world: costly implications in captive stonechats. Integr Comp Biol 49:563–579

    Article  CAS  PubMed  Google Scholar 

  • Helm B, Ben-Shlomo R, Sheriff MJ, Hut RA, Foster R, Barnes BM, Dominoni D (2013) Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Biological Sciences, Proceedings of the Royal Society B, p 280

    Google Scholar 

  • Helm B, Schwabl I, Gwinner E (2009) Circannual basis of geographically distinct bird schedules. J Exp Biol 212:1259–1269

    Article  PubMed  Google Scholar 

  • Helm B, Visser ME, Schwartz W, Kronfeld-Schor N, Gerkema M, Piersma T, Bloch G (2017) Two sides of a coin: ecological and chronobiological perspectives of timing in the wild. Philosophical Transactions of the Royal Society B: Biological Sciences 372:1734

    Article  Google Scholar 

  • Johnsen A, Fidler AE, Kuhn S, Carter KL, Hoffmann A, Barr IR, Biard C, Charmantier A, Eens M, Korsten P, Siitari H, Tomiuk J, Kempenaers B (2007) Avian clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol Ecol 16:4867–4880

    Article  CAS  PubMed  Google Scholar 

  • Karagicheva J, Rakhimberdiev E, Dekinga A, Brugge M, Koolhaas A, Ten Horn J, Piersma T (2016) Seasonal time keeping in a long-distance migrating shorebird. J Biol Rhythm 31:509–521

    Article  Google Scholar 

  • Kramer G (1957) Experiments on bird orientation and their interpretation. Ibis 99:196–227

    Article  Google Scholar 

  • Kuenzel WJ, Kang SW, Zhou ZJ (2015) Exploring avian deep-brain photoreceptors and their role in activating the neuroendocrine regulation of gonadal development1. Poult Sci 94:786–798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar V, Singh BP, Rani S (2004) The bird clock: a complex, multi-oscillatory and highly diversified system. Biol Rhythm Res 35:121–144

    Article  Google Scholar 

  • Menaker M, Eskin A (1966) Entrainment of circadian rhythms by sound in Passer domesticus. Science 154:1579–1581

    Article  CAS  PubMed  Google Scholar 

  • Menaker M, Moreira LF, Tosini G (1997) Evolution of circadian organization in vertebrates. Braz J Med Biol Res 30:305–313

    Article  CAS  PubMed  Google Scholar 

  • Menaker M, Underwood H (1976) Extraretinal photoreception in birds. Photochem Photobiol 23:299–306

    Article  CAS  Google Scholar 

  • Nakane Y, Shimmura T, Abe H, Yoshimura T (2014) Intrinsic photosensitivity of a deep brain photoreceptor. Curr Biol 24:R596–R597

    Article  CAS  PubMed  Google Scholar 

  • Nakane Y, Yoshimura T (2019) Photoperiodic regulation of reproduction in vertebrates. Annual Review of Animal Biosciences 7:173–194

    Article  PubMed  Google Scholar 

  • Okano T, Yoshizawa T, Fukada Y (1994) Pinopsin is a chicken pineal photoreceptive molecule. Nature 372:94–97

    Article  CAS  PubMed  Google Scholar 

  • Oshima I, Yamada H, Goto M, Sato K, Ebihara S (1989) Pineal and retinal melatonin is involved in the control of circadian locomotor activity and body temperature rhythms in the pigeon. J Comp Physiol A 166:217–226

    Article  Google Scholar 

  • Padget O, Bond SL, Kavelaars MM, Van Loon E, Bolton M, Fayet AL, Syposz M, Roberts S, Guilford T (2018) In situ clock shift reveals that the sun compass contributes to orientation in a pelagic seabird. Curr Biol 28:275–279. e2

    Article  CAS  PubMed  Google Scholar 

  • Perfito N, Guardado D, Williams TD, Bentley GE (2015) Social cues regulate reciprocal switching of hypothalamic Dio2/Dio3 and the transition into final follicle maturation in European starlings (Sturnus vulgaris). Endocrinology 156:694–706

    Article  CAS  PubMed  Google Scholar 

  • Rani S, Kumar V (2013) Avian circannual systems: persistence and sex differences. Gen Comp Endocrinol 190:61–67

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Renthlei Z, Gurumayum T, Borah BK, Trivedi AK (2019) Daily expression of clock genes in central and peripheral tissues of tree sparrow (Passer montanus). Chronobiol Int 36:110–121

    Article  CAS  PubMed  Google Scholar 

  • Rich EL, Romero LM (2001) Daily and photoperiod variations of basal and stress-induced corticosterone concentrations in house sparrows (Passer domesticus). J Comp Physiol B 171:543–547

    Article  CAS  PubMed  Google Scholar 

  • Rowan W (1937) Effects of traffic disturbance and light illumination on London starlings. Nature 139:668–669

    Article  Google Scholar 

  • Shimmura T, Ohashi S, Yoshimura T (2015) The highest-ranking rooster has priority to announce the break of dawn. Sci Rep 5:11683

    Article  PubMed  PubMed Central  Google Scholar 

  • Stevenson TJ, Lincoln GA (2017) Epigenetic mechanisms regulating Circannual rhythms. In: Kumar V (ed) Biological timekeeping: clocks, rhythms and behavior. Springer India, New Delhi

    Google Scholar 

  • Thackeray SJ, Henrys PA, Hemming D, Bell JR, Botham MS, Burthe S, Helaouet P, Johns DG, Jones ID, Leech DI, Mackay EB, Massimino D, Atkinson S, Bacon PJ, Brereton TM, Carvalho L, Clutton-Brock TH, Duck C, Edwards M, Elliott JM, HALL SJ, Harrington R, Pearce-Higgins JW, Hoye TT, Kruuk LE, Pemberton JM, Sparks TH, Thompson PM, White I, Winfield IJ, Wanless S (2016) Phenological sensitivity to climate across taxa and trophic levels. Nature 535:241–245

    Article  CAS  PubMed  Google Scholar 

  • Van der Veen DR, Riede SJ, Heideman PD, Hau M, Van der Vinne V, Hut RA (2017) flexible clock systems: adjusting the temporal programme. Philos Trans R Soc Lond Ser B Biol Sci 372:1734

    Google Scholar 

  • Van Doren BM, Horton KG, Dokter AM, Klinck H, Elbin SB, Farnsworth A (2017) High-intensity urban light installation dramatically alters nocturnal bird migration. Proc Natl Acad Sci 114:11175–11180

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Visser ME, Caro SP, Van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3113–3127

    Article  CAS  Google Scholar 

  • Visser ME, Gienapp P (2019) Evolutionary and demographic consequences of phenological mismatches. Nature Ecology & Evolution 3:879–885

    Article  Google Scholar 

  • Vivid D, Bentley G (2018) Seasonal reproduction in vertebrates: melatonin synthesis, binding, and functionality using Tinbergen’s four questions. Molecules 23:652

    Article  PubMed Central  CAS  Google Scholar 

  • Winkler DW, Gandoy FA, Areta JI, Iliff MJ, Rakhimberdiev E, Kardynal KJ, Hobson KA (2017) Long-distance range expansion and rapid adjustment of migration in a newly established population of barn swallows breeding in Argentina. Curr Biol 27:1080–1084

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura T, Yasuo S, Suzuki Y, Makino E, Yokota Y, Ebihara S (2001) Identification of the suprachiasmatic nucleus in birds. Am J Physiol Regul Integr Comp Physiol 280:R1185–R1189

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman NH, Menaker M (1979) The pineal gland: a pacemaker within the circadian system of the house sparrow. Proc Natl Acad Sci U S A 76:999–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Further Recommended Reading

  • Akesson S, Ilieva M, Karagicheva J, Rakhimberdiev E, Tomotani B, Helm B (2017) Timing avian long-distance migration: from internal clock mechanisms to global flights. Philos Trans R Soc Lond B Biol Sci 372, pii: 20160252.

    Google Scholar 

  • This article highlights the importance of clocks and calendars for real-world processes, by combining mechanistic overview and case studies of migration in the wild.

    Google Scholar 

  • Cassone VM (2014) Avian Circadian Organization: A Chorus of Clocks. Frontiers in neuroendocrinology 35:76–88

    Article  PubMed  Google Scholar 

  • Succinct overview of mechanistic studies into avian circadian rhythms, which leads to important literature.

    Google Scholar 

  • Gwinner E (1996) Circadian and circannual programmes in avian migration. Journal of Experimental Biology 199:39–48

    CAS  PubMed  Google Scholar 

  • Classic, nutshell review of key experiments and evidence for circadian and circannual regulation of migration.

    Google Scholar 

  • Nakane Y, Yoshimura T (2019) Photoperiodic Regulation of Reproduction in Vertebrates. Annual Review of Animal Biosciences 7:173–194

    Article  PubMed  Google Scholar 

  • This article reviews mechanistic insight into photoperiodism of birds in direct comparison with other vertebrates.

    Google Scholar 

Download references

Acknowledgments

The author thanks Julia Karagicheva, Paul Bartell, Davide Dominoni, Takashi Yoshimura, and Michiel Vellema for kindly sharing materials, insights, and thoughtful discussions.

Author information

Authors and Affiliations

  1. GELIFES - Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands

    Barbara Helm

Authors
  1. Barbara Helm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barbara Helm .

Editor information

Editors and Affiliations

  1. School of Life Sciences, University of Nottingham, Nottingham, UK

    Francis J. P. Ebling

  2. School of Life Sciences, University of Bristol, Bristol, UK

    Hugh D. Piggins

Rights and permissions

Reprints and permissions

Copyright information

© 2020 The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Helm, B. (2020). Clocks and Calendars in Birds. In: Ebling, F.J.P., Piggins, H.D. (eds) Neuroendocrine Clocks and Calendars. Masterclass in Neuroendocrinology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-030-55643-3_6

Download citation

Publish with us

Policies and ethics

Search

Navigation