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Circannual Rhythms: History, Present Challenges, Future Directions

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Annual, Lunar, and Tidal Clocks

Abstract

Circannual rhythms are endogenous biological oscillations that underlie a wide range of seasonal processes. Without knowledge of these underlying mechanisms, it is difficult to fully understand what drives the ways organisms change over the course of a year and to predict how they will respond to environmental conditions. The study of circannual rhythms is particularly timely given the substantial interest in seasonal processes in relationship to environmental change, and further given insights that seasonal change in human physiology and behavior is greater than previously thought. The present chapter outlines basic definitions and ideas on circannual rhythms, summarizes ground-laying work, and highlights some current developments. It then addresses challenges in this field and the opportunities that arise from the rapid development of new technologies.

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References

  • Altshuler DL, Cockle KL, Boyle WA (2013) North American ornithology in transition. Biol Lett 9:1

    Google Scholar 

  • Anderson DM, Keafer BA (1987) An endogenous annual clock in the toxic marine dinoflagellate Gonyaulax tamarensis. Nature (Lond) 325:616–617

    Article  CAS  Google Scholar 

  • Aschoff J (1955) Jahresperiodik der Fortpflanzung bei Warmblütern. Stud Gen 8:742–776

    Google Scholar 

  • Aschoff J (1958) Tierische Periodik unter dem Einfluß von Zeitgebern. Z Tierpsychol 15:1–30

    Article  Google Scholar 

  • Avigdor M, Sullivan SD, Heideman PD (2005) Response to selection for photoperiod responsiveness on the density and location of mature GnRH-releasing neurons. Am J Physiol Regul Integr Comp Physiol 288:R1226–R1236

    Article  CAS  PubMed  Google Scholar 

  • Berthold P (2001) Bird migration: a general survey, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Berthold P, Gwinner E, Klein H (1972) Circannuale Periodik bei Grasmücken. II. Periodik der Gonadengröße bei Sylvia atricapilla und S. borin unter verschiedenen konstanten Bedingungen. J Ornithol 113:407–417

    Article  Google Scholar 

  • Blake GM (1958) Diapause and the regulation of development in Anthrenus verbasci (L.) (Col. Dermestidae). Bull Entomol Res 49:751–775

    Article  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2007) Evolution of animal photoperiodism. Annu Rev Ecol Evol Syst 38:1–25

    Article  Google Scholar 

  • Brown FA, Woodland Hastings J, Palmer JD (1970) The biological clock, two views. Academic, New York

    Google Scholar 

  • Bünning E (1949) Zur Physiologie der endogenen Jahresrhythmik in Pflanzen, speziell in Samen. Z Naturforsch 4b:167–176

    Google Scholar 

  • Butler MP, Turner KW, Park JH, Schoomer EE, Zucker I, Gorman MR (2010) Seasonal regulation of reproduction: altered role of melatonin under naturalistic conditions in hamsters. Proc R Soc Lond B 277:2867–2874

    Article  Google Scholar 

  • Cech TR, Steitz JA (2014) The noncoding RNA revolution: trashing old rules to forge new ones. Cell 157:77–94

    Article  CAS  PubMed  Google Scholar 

  • Chapin JP (1954) The calendar of Wideawake Fair. Auk 71:1–15

    Article  Google Scholar 

  • Concannon P, Roberts P, Baldwin B, Tennant B (1997) Long-term entrainment of circannual reproductive and metabolic cycles by Northern and Southern hemisphere photoperiods in woodchucks (Marmota monax). Biol Reprod 57:1008–1015

    Article  CAS  PubMed  Google Scholar 

  • Costas E, López Rodas V (1991) Evidence for an annual rhythm in cell ageing in Spirogyra insignis (Chlorophyceae). Phycologia 30:597–599

    Article  Google Scholar 

  • Dawson A (2007) Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods. Proc R Soc Lond B 274:721–725

    Article  Google Scholar 

  • Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380

    Article  CAS  PubMed  Google Scholar 

  • Dunlap JC, Loros JJ, DeCoursey P (eds) (2004) Chronobiology: biological timekeeping. Sinauer, Sunderland

    Google Scholar 

  • Ebling FJP (2014) On the value of seasonal mammals for identifying mechanisms underlying the control of food intake and body weight. Horm Behav 66:56–65

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Emlen ST, Emlen JT (1966) A technique for recording migratory orientation of captive birds. Auk 83:361–367

    Article  Google Scholar 

  • Fonken LK, Aubrecht TG, Meléndez-Fernández OH, Weil ZM, Nelson RJ (2013) Dim light at night disrupts molecular circadian rhythms and increases body weight. J Biol Rhythms 28:262–271

    Article  PubMed Central  PubMed  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

    Google Scholar 

  • Foster RG, Roenneberg T (2008) Human responses to the geophysical daily, annual and lunar cycles. Curr Biol 18:R784–R794

    Article  CAS  PubMed  Google Scholar 

  • Gwinner E (1967) Circannuale Periodik der Mauser und der Zugunruhe bei einem Vogel. Naturwissenschaften 54:447

    Article  CAS  PubMed  Google Scholar 

  • Gwinner E (1968) Circannuale Periodik als Grundlage des jahreszeitlichen Funktionswandels bei Zugvögeln. Untersuchungen am Fitis (Phylloscopus trochilus) und am Waldlaubsänger (P. sibilatrix). J Ornithol 109:70–95

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Gwinner E (1988) Photorefractoriness in equatorial migrants. In: Proceedings of the 19th International Ornithological Congress, Ottawa, pp 626–633

    Google Scholar 

  • Gwinner E (1996) Circannual clocks in avian reproduction and migration. Ibis 138:47–63

    Article  Google Scholar 

  • Gwinner E, Helm B (2003) Circannual and circadian contributions to the timing of avian migration. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer-Verlag, Berlin, pp 81–95

    Chapter  Google Scholar 

  • Gwinner E, Wozniak J (1982) Circannual rhythms in European starlings: why do they stop under long photoperiods? J Comp Physiol 146:419–421

    Article  Google Scholar 

  • Hahn TP, MacDougall-Shackleton SA (2008) Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos Trans R Soc Lond B 363:267–286

    Article  Google Scholar 

  • Hahn TP, Boswell T, Wingfield JC, Ball GF (1997) Temporal flexibility in avian reproduction. In: Nolan V (ed) Current ornithology, vol 14. Plenum Press, New York, pp 39–80

    Chapter  Google Scholar 

  • Hamner WM, Stocking J (1970) Why don’t bobolinks breed in Brazil? Ecology 51:743–751

    Article  Google Scholar 

  • Hazlerigg DG, Lincoln GA (2011) Hypothesis: cyclical histogenesis is the basis of circannual timing. J Biol Rhythms 26:471–485

    Article  PubMed  Google Scholar 

  • Hazlerigg DG, Wyse CA, Dardente H, Hanon EA, Lincoln GA (2013) Photoperiodic variation in CD45-positive cells and cell proliferation in the mediobasal hypothalamus of the Soay sheep. Chronobiol Int 30:548–558

    Article  CAS  PubMed  Google Scholar 

  • Heideman PD, Bronson FH (1994) An endogenous circannual rhythm of reproduction in a tropical bat, Anoura geoffroyi, is not entrained by photoperiod. Biol Reprod 50:607–614

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

    Article  PubMed  Google Scholar 

  • Helm B, Gwinner E, Koolhaas A, Battley P, Schwabl I, Dekinga A et al (2012) Avian migration: temporal multitasking and a case study of melatonin cycles in waders. Prog Brain Res 199:457–479

    Article  PubMed  Google Scholar 

  • Helm B, Ben-Shlomo R, Sheriff MJ, Hut RA, Foster R, Barnes BM et al (2013) Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proc R Soc B Biol Sci 280:20130016

    Article  Google Scholar 

  • Holberton RL, Able KP (1992) Persistence of circannual cycles in a migratory bird held in constant dim light. J Comp Physiol A 171:477–481

    Article  Google Scholar 

  • Immelmann K (1971) Ecological aspects of periodic reproduction. In: Farner DS, King JR (eds) Avian biology, vol 1. Academic, New York, pp 341–389

    Google Scholar 

  • Jacobs J, Wingfield JC (2000) Endocrine control of life-cycle stages: a constraint on response to the environment? Condor 102:35–51

    Article  Google Scholar 

  • Johnson CH, Elliott JA, Foster R (2003) Entrainment of circadian programs. Chronobiol Int 20:741–774

    Article  PubMed  Google Scholar 

  • Johnston JD, Messager S, Barrett P, Hazlerigg DG (2003) Melatonin action in the pituitary: neuroendocrine synchronizer and developmental modulator? J Neuroendocrinol 15:405–408

    Article  CAS  PubMed  Google Scholar 

  • Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T (2006) Circannual control of hibernation by HP complex in the brain. Cell 125:161–172

    Article  CAS  PubMed  Google Scholar 

  • Lincoln GA, Johnston JD, Andersson H, Wagner G, Hazlerigg DG, Lincoln GA et al (2005) Photorefractoriness in mammals: dissociating a seasonal timer from the circadian-based photoperiod response. Endocrinology 146:3782–3790

    Article  CAS  PubMed  Google Scholar 

  • Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG (2006) Characterizing a mammalian circannual pacemaker. Science 314:1941–1944

    Article  CAS  PubMed  Google Scholar 

  • Lüning K, Kadel P (1993) Daylength range for circannual rhythmicity in Pterygophora californica (Alariaceae, Phaeophyta) and synchronization of seasonal growth by daylength cycles in several other brown algae. Phycologia 32:379–387

    Article  Google Scholar 

  • MacDougall-Shackleton SA, Stevenson TJ, Watts HE, Pereyra ME, Hahn TP (2009) The evolution of photoperiod response systems and seasonal GnRH plasticity in birds. Integr Comp Biol 49:580–589

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Bakker M, Bakker KM, King AA, Rohani P (2014) Human birth seasonality: latitudinal gradient and interplay with childhood disease dynamics. Proc R Soc B 281:20132438

    Article  PubMed  Google Scholar 

  • Matrai P, Thompson B, Keller M (2005) Circannual excystment of resting cysts of Alexandrium spp. from eastern Gulf of Maine populations. Deep Sea Res II 52:2560–2568

    Article  Google Scholar 

  • Menaker M (1974) Circannual rhythms in circadian perspective. In: Pengelley ET (ed) Circannual clocks. Academic, New York, pp 507–520

    Chapter  Google Scholar 

  • Metzker ML (2010) Sequencing technologies: the next generation. Nat Rev Genet 11:31–46

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki Y, Nisimura T, Numata H (2005) A phase response curve for circannual rhythm in the varied carpet beetle Anthrenus verbasci. J Comp Physiol A 191:883–887

    Article  CAS  Google Scholar 

  • Miyazaki Y, Nisimura T, Numata H (2006) Phase responses in the circannual rhythm of the varied carpet beetle, Anthrenus verbasci, under naturally changing day length. Zool Sci 23:1031–1037

    Article  PubMed  Google Scholar 

  • Miyazaki Y, Nisimura T, Numata H (2007) Phase resetting and phase singularity of an insect circannual oscillator. J Comp Physiol A 193:1169–1176

    Article  Google Scholar 

  • Monecke S, Saboureau M, Malan A, Bonn D, Masson-Pevet M, Pevet P (2009) Circannual phase response curves to short and long photoperiod in the European hamster. J Biol Rhythms 24:413–426

    Article  PubMed  Google Scholar 

  • Monecke S, Amann B, Lemuth K, Wollnik F (2014) Dual control of seasonal time keeping in male and female juvenile European hamsters. Physiol Behav 130:66–74

    Article  CAS  PubMed  Google Scholar 

  • Mrosovsky N (1970) Mechanism of hibernation cycles in ground squirrels: circannian rhythm or sequence of stages? Pennsyl Acad Sci 44:172–175

    Google Scholar 

  • Mukai M, Replogle K, Drnevich J, Wang G, Wacker D, Band M et al (2009) Seasonal differences of gene expression profiles in song sparrow (Melospiza melodia) hypothalamus in relation to territorial aggression. PLoS One 4:e8182

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K et al (2008) Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature (Lond) 452:317–322

    Article  CAS  Google Scholar 

  • Nelson RJ, Denlinger DL, Somers DE (eds) (2010) Photoperiodism: the biological calendar. Oxford University Press, Oxford

    Google Scholar 

  • Newton I (2008) The migration ecology of birds. Academic, London

    Google Scholar 

  • Nicholls TJ, Goldsmith AR, Dawson A (1988) Photorefractoriness in birds and comparison with mammals. Physiol Rev 68:133–176

    CAS  PubMed  Google Scholar 

  • Olson JM, Jinka TR, Larson LK, Danielson JJ, Moore JT, Carpluck J et al (2013) Circannual rhythm in body temperature, torpor, and sensitivity to A(1) adenosine receptor agonist in arctic ground squirrels. J Biol Rhythms 28:201–207

    Article  CAS  PubMed  Google Scholar 

  • Paul M, Zucker I, Schwartz WJ (2008) Tracking the seasons: the internal calendars of vertebrates. Philos Trans R Soc Lond B Biol Sci 363:341–361

    Article  PubMed Central  PubMed  Google Scholar 

  • Pengelley ET, Fisher KC (1957) Onset and cessation of hibernation under constant temperature and light in the golden-mantled ground squirrel, Citellus lateralis. Nature (Lond) 180:1371–1372

    Article  Google Scholar 

  • Perfito N, Jeong SY, Silverin B, Calisi RM, Bentley GE, Hau M (2012) Anticipating spring: wild populations of great tits (Parus major) differ in expression of key genes for photoperiodic time measurement. PLoS One 7:e34997

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Piersma T, Brugge M, Spaans B, Battley PF (2008) Endogenous circannual rhythmicity in body mass, molt, and plumage of great knots (Calidris tenuirostris). Auk 125:140–148

    Article  Google Scholar 

  • Prendergast BJ, Nelson RJ, Zucker I (2002) Mammalian seasonal rhythms: behavior and neuroendocrine substrates. In: Pfaff DW (ed) Hormones, brain and behavior. Elsevier Science, Amsterdam, pp 93–156

    Chapter  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 

  • Rensing L, Ruoff P (2002) Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular basis. Chronobiol Int 19:807–864

    Article  CAS  PubMed  Google Scholar 

  • Revel FG, Ansel L, Klosen P, Saboureau M, Pevet P, Mikkelsen JD et al (2007) Kisspeptin: a key link to seasonal breeding. Rev Endocr Metab Disord 8:57–65

    Article  CAS  PubMed  Google Scholar 

  • Reynolds SJ, Martin GR, Dawson A, Wearn CP, Hughes BJ (2014) The sub-annual breeding cycle of a tropical seabird. PLoS One 9:e93582

    Article  PubMed Central  PubMed  Google Scholar 

  • Ross AW, Webster CA, Mercer JG, Moar KM, Ebling FJ, Schuhler S et al (2004) Photoperiodic regulation of hypothalamic retinoid signaling: association of retinoid X receptor gamma with body weight. Endocrinology 145:13–20

    Article  CAS  PubMed  Google Scholar 

  • Rowan W (1925) Relation of light to bird migration and developmental changes. Nature (Lond) 115:494–495

    Article  Google Scholar 

  • Rowan W (1926) On photoperiodism, reproductive periodicity, and the annual migrations of birds and certain fishes. Proc Boston Soc Nat Hist 38:147–189

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schwartz C, Andrews MT (2013) Circannual transitions in gene expression: lessons from seasonal adaptations. Curr Top Dev Biol 105:247–273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stevenson TJ, Prendergast BJ (2013) Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci USA 110:16651–16656

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stevenson TJ, Replogle K, Drnevich J, Clayton DF, Ball GF (2012a) High throughput analysis reveals dissociable gene expression profiles in two independent neural systems involved in the regulation of social behavior. BMC Neurosci 13:126

    Article  PubMed Central  PubMed  Google Scholar 

  • Stevenson TJ, Hahn TP, MacDougall-Shackleton SA, Ball GF (2012b) Gonadotropin-releasing hormone plasticity: a comparative perspective. Front Neuroendocrinol 33:287–300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stevenson TJ, Onishi KG, Bradley SP, Prendergast BJ (2014) Cell-autonomous iodothyronine deiodinase expression mediates seasonal plasticity in immune function. Brain Behav Immun 36:61–70

    Article  CAS  PubMed  Google Scholar 

  • Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251–258

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui K, Ubuka T, Bentley GE, Kriegsfeld LJ (2013) Review: regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front Neurosci 7:60

    Article  PubMed Central  PubMed  Google Scholar 

  • Visser ME, Caro SP, van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc Lond B Biol Sci 365:3113–3127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wikelski M, Martin LB, Scheuerlein A, Robinson MT, Robinson ND, Helm B et al (2008) Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control. Philos Trans R Soc Lond B Biol Sci 363:411–423

    Article  PubMed Central  PubMed  Google Scholar 

  • Wingfield JC (1993) Control of testicular cycles in the song sparrow, Melospiza melodia melodia: interaction of photoperiod and an endogenous program? Gen Comp Endocrinol 92:388–401

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Hastings MH, Green EW, Tauber E, Sladek M, Webster SG et al (2013) Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra. Curr Biol 23:1863–1873

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors acknowledge the help and support of Helga Gwinner, who allowed us to view the legacy of Ebo Gwinner (1938–2004). This chapter has been written in friendship to Ebo Gwinner, to whom the book is dedicated, and whose vision and insights will continue to inspire research on biological rhythms in the years to come.

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Correspondence to Barbara Helm .

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Helm, B., Stevenson, T.J. (2014). Circannual Rhythms: History, Present Challenges, Future Directions. In: Numata, H., Helm, B. (eds) Annual, Lunar, and Tidal Clocks. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55261-1_11

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