Abstract
In a seasonal environment, mammals time their reproductive phase so that the offspring are born in spring and summer. Two strategies have evolved to ensure accurate seasonal timing of reproduction, but both share a common Zeitgeber, the seasonal changes in photoperiod. The reproductive axis might be directly controlled, as in photoperiodic species, which require photoperiodic input to show seasonal changes in reproductive competence. In contrast, in circannual species photoperiodic changes act indirectly, namely, on an endogenous circannual clock that then times reproduction. This circannual clock generates self-sustained rhythms with a period length of about 1 year, and photoperiodic information is only needed to synchronize these rhythms. Concerning the mechanism that imparts the photoperiodic message internally, so far no differences between photoperiodic and circannual mammals have been reported. Recent results however, strongly suggest that the circannual European hamster (Cricetus cricetus) uses a fundamentally different mechanism than photoperiodic species. In the latter, photoperiod induces a change in the reproductive state via a melatonin-dependent pathway, whereas the circannual clock of the European hamsters can be synchronized via a melatonin-independent pathway. Instead, a circadian mechanism based on a specific organizational state is involved. Juvenile European hamsters use probably both pathways: the melatonin-dependent photoperiodic pathway for the short-term timing in the year of birth and the melatonin-independent circannual pathway for long-term timing of the seasonal events in the next year.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Albert M (2013) Erfassung des Reproduktionserfolges des Feldhamsters (Cricetus cricetus) in Hessen [Reproductive success of female Common hamster (Cricetus cricetus) in Hesse]. Abteilung Fließgewässerökologie und Naturschutzforschung, Fachgebiet Naturschutzgenetik, Forschungsinstitut Senckenberg
Arnold W, Ruf T, Reimoser S, Tataruch F, Onderscheka K, Schober F (2004) Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus). Am J Physiol Regul Integr Comp Physiol 286:R174–R181
Arnold W, Ruf T, Frey-Roos F, Bruns U (2011) Diet-independent remodeling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS One 6:e18641
Asa CS, Seal US, Letellier M, Plotka ED, Peterson EK (1987) Pinealectomy or superior cervical ganglionectomy do not alter reproduction in the wolf (Canis lupus). Biol Reprod 37:14–21
Banaszek A, Jadwiszczak KA, Ratkiewicz M, Ziomek J (2009) Low genetic diversity and significant structuring of the common hamster populations Cricetus cricetus in Poland revealed by the mtDNA control region sequence variation. Acta Theriol 54:289–295
Barnes BM, York AD (1990) Effect of winter high temperatures on reproduction and circannual rhythms in hibernating ground squirrels. J Biol Rhythms 5:119–130
Bartness TJ, Goldman BD (1989) Mammalian pineal melatonin: a clock for all seasons. Experientia (Basel) 45:939–945
Beersma DGM, Daan S, Hut RA (1999) Accuracy of circadian entrainment under fluctuating light conditions: contributions of phase and period responses. J Biol Rhythms 14:320–329
Bekenov AB (1998) Ecology of common hamster (Cricetus cricetus L., 1758) in Kazakhstan. In: Stubbe M, Stubbe A (eds) Ecology and protection of the common hamster. Martin-Luther-Universität Halle-Wittenberg, Halle/Saale, pp 81–86
Bittman EL, Dempsey RJ, Karsch FJ (1983) Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113:2276–2283
Bloch R, Canguilhem B (1966) Cycle saisonnier d’elimination urinaire de l’aldostérone chez un hibernant, Cricetus cricetus. Influence de la température [Seasonal cycle of urinary elimination of aldosterone in a hibernant, Cricetus cricetus. Influence of temperature]. C R Soc Biol 160:1500–1503
Bloch G, Barnes BM, Gerkema MP, Helm B (2013) Animal activity around the clock with no overt circadian rhythms: patterns, mechanisms and adaptive value. Proc R Soc B 280:20130019
Boissin J, Canguilhem B (1988) Les rythmes circannuels chez les mammifères [Circannual rhythms in mammals]. Arch Int Physiol Biochim 96:A289–A345
Brandes K, Fend F, Monecke S, Teifke JP, Breuer W, Hermanns W (2004) Comparative morphologic and immunohistochemical investigation of spontaneously occurring thymomas in a colony of European hamsters. Vet Pathol 41:346–352
Buijs RM, Pévet P, Masson-Pévet M, Pool CW, deVries GJ, Canguilhem B, Vivien-Roels B (1986) Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus). Brain Res 371:193–196
Canguilhem B (1985) Rythmes circannuels chez les mammifères hibernants sauvages [Circannual rhythms in wild hibernating mammals]. Can J Zool 63:453–463
Canguilhem B, Bloch R (1966) Évolution saisonnière de l’elimination des hormones surrénaliennes chez un hibernant, Cricetus cricetus [Seasonal development in the excretion of adrenal hormones in a hibernating animal, Cricetus cricetus]. C R Séances Soc Biol Fil [Arch Sci Physiol (Paris)] 21:27–44
Canguilhem B, Petrovic A (1974) Effets de la photopériode et de la température ambiante sur les rythmes circannuels du poids et de la cortico-surrénale du hamster d’Europe (Cricetus cricetus) [Effects of photoperiod and ambient temperature on circannual rhythms of body weight and adrenal cortex activity in European hamster (Cricetus cricetus)]. Arch Sci Physiol 28:113–126
Canguilhem B, Schieber JP, Koch A (1973) Rythme circannuel pondéral du hamster d’Europe (Cricetus cricetus). Influences respectives de la photopériode et de la température externe sur son déroulement [Circannual weight rhythm of the European hamster (Cricetus cricetus). Respective influence of the photoperiod and external temperature during its course]. Arch Sci Physiol 27:67–90
Canguilhem B, Schmitt P, Mack G, Kempf E (1977) Comportement alimentaire, rythmes circannuels ponderal et d’hibernation chez le hamster d’Europe porteur de lesions des faisceaux noradrenergiques ascendants [Feeding behavior, circannual body weight and hibernation rhythms in European hamsters lesioned in the noradrenergic ascending bundles]. Physiol Behav 18:1067–1074
Canguilhem B, Vivien-Roels B, Demeneix B, Miro JL, Masson-Pévet M, Pévet P (1986) Seasonal and endogenous variations of plasma testosterone (T), thyroxine (T4) and triiodothyronine (T3) in the European hamster. In: Assenmacher I, Boissin J (eds) Endocrine regulations as adaptive mechanisms to the environment. CNRS, Bordeaux, pp 291–295
Canguilhem B, Vaultier J-P, Pévet P, Coumaros G, Masson-Pévet M, Bentz I (1988) Photoperiodic regulation of body mass, food intake, hibernation, and reproduction in intact and castrated male European hamsters, Cricetus cricetus. J Comp Physiol A 163:549–557
Canguilhem B, Masson-Pévet M, Pévet P, Bentz I (1992) Endogenous, photoperiodic and hormonal control of the body weight rhythm in the female European hamster, Cricetus cricetus. Comp Biochem Physiol 101:465–470
Canguilhem B, Malan A, Masson-Pévet M, Nobelis P, Kirsch R, Pévet P, Le Minor J (1994) Search for rhythmicity during hibernation in the European hamster. J Comp Physiol B 163:690–698
Ciesielski L, Miro JL, Lorentz JG, Canguilhem B, Mandel P (1985) Circannual variations of GABA content in cytosolic and crude synaptosomal fractions in some brain areas of the European hamster. Brain Res 344:146–149
Daan S, Aschoff J (1975) Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia (Berl) 18:269–316
Dardente H, Klosen P, Pevet P, Masson-Pevet M (2003) MT1 melatonin receptor mRNA expressing cells in the pars tuberalis of the European hamster: effect of photoperiod. J Neuroendocrinol 15:778–786
Duston J, Bromage N (1988) The entrainment and gating of the endogenous circannual rhythm of reproduction in the female rainbow trout (Salmo gairdneri). J Comp Physiol A 164:259–268
Duval-Erny A, Kayser C (1964) Bilans calciques saisonniers chez un hibernant, le hamster d’Europe (Cricetus cricetus) [Seasonal calcium balances in a hibernator, the European hamster (Cricetus cricetus)]. C R Séances Soc Biol Fil 158:1945–1947
Elliott JA, Stetson MH, Menaker M (1972) Regulation of testis function in golden hamsters: a circadian clock measures photoperiodic time. Science 178:771–773
Ernst H, Kunstyr I, Rittinghausen S, Mohr U (1989) Spontaneous tumours of the European hamster (Cricetus cricetus L.). Z Versuchstierkd 32:87–96
Everts LG, Strijkstra AM, Hut RA, Hoffmann IE, Millesi E (2004) Seasonal variation in daily activity patterns of free-ranging European ground squirrels (Spermophilus citellus). Chronobiol Int 21:57–71
Franceschini C, Millesi E (2004) Reproductive timing and success in common hamsters. In: Losinger I (ed) 12th meeting of the international hamster workgroup. ONCFS, Strasbourg, pp 63–66
Franceschini C, Siutz C, Palme R, Millesi E (2007) Seasonal changes in cortisol and progesterone secretion in common hamsters. Gen Comp Endocrinol 152:14–21
Franceschini-Zink C, Millesi E (2008) Reproductive performance in female common hamsters. Zoology 111:76–83
Freeman DA, Zucker I (2000) Temperature-independence of circannual variations in circadian rhythms of golden-mantled ground squirrels. J Biol Rhythms 15:336–343
Garidou ML, Vivien-Roels B, Pevet P, Miguez J, Simonneaux V (2003) Mechanisms regulating the marked seasonal variation in melatonin synthesis in the European hamster pineal gland. Am J Physiol Regul Integr Comp Physiol 284:R1043–R1052
Gaston S, Menaker M (1967) Photoperiodic control of hamster testis. Science 158:925–928
Gattermann R (1985) Zur Biorhythmik des Goldhamsters (Mesocricetus auratus Waterhouse 1839). IV. Annuale Rhythmen [On the biorhythm of the Syrian hamster (Mesocricetus auratus Waterhouse 1839). IV. Annual rhythms]. Zool Jahrb Physiol 89:279–285
Geiser F, Turbill C (2009) Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96:1235–1240
Georgii B (1981) Activity patterns of female red deer (Cervus elaphus L.) in the Alps. Oecologia (Berl) 49:127–136
Georgii B, Schröder W (1983) Home range and activity patterns of male red deer (Cervus elaphus L.) in the Alps. Oecologia (Berl) 58:238–248
Ghadially FN, Illman O (1965) Naturally occurring thymomas in the European hamster. J Pathol Bacteriol 90:465–469
Goldman BD (2001) Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 16:283–301
Górecki A, Grygielska M (1975) Consumption and utilization of natural foods by the common hamster. Acta Theriol 20:237–246
Gorman MR, Goldman BD, Zucker I (2001) Mammalian photoperiodism. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioral neurobiology: circadian clocks. Kluwer Academic/Plenum, New York, pp 481–508
Goymann W, Helm B, Jensen W, Schwabl I, Moore IT (2012) A tropical bird can use the equatorial change in sunrise and sunset times to synchronize its circannual clock. Proc R Soc B 279:3527–3534
Gwinner E (1986) Circannual rhythms. Springer-Verlag, Berlin
Hanon EA, Routledge K, Dardente H, Masson-Pévet M, Morgan PJ, Hazlerigg DG (2010) Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J Neuroendocrinol 22:51–55
Harberey P, Canguilhem B, Kayser C (1967) Evolution saisonnière de l’élimination urinaire du sodium et du potassium chez le Hamster d’Europe (Cricetus cricetus) [Seasonal variations of sodium and potassium excretion in the European hamster (Cricetus cricetus)]. C R Séances Soc Biol Fil 161:2044–2049
Hiebert SM, Thomas EM, Lee TM, Pelz KM, Yellon SM, Zucker I (2000) Photic entrainment of circannual rhythms in golden-mantled ground squirrels: role of the pineal gland. J Biol Rhythms 15:126–134
Hildebrand JC (1769) Wahrnehmungen von den Hamstern und deren ohne Fäulniß und Lebensgefahr einige Monate hindurch dauernden Ohnmacht oder Schlafsucht [Observations of the hamsters and their without rottenness and life-threatening some months lasting unconsciousness or somnolence]. Neues Hamburgisches Magazin 5:87–96
Hilfrich J, Züchner H, Reznik-Schüller R (1977) Studies of the ovaries of hibernating and non-hibernating European hamsters (Cricetus cricetus). Z Versuchstierkd 19:304–308
Hoffmann K (1982) The critical photoperiod in the Djungarian hamster Phodopus sungorus. In: Aschoff J, Daan S, Groos GA (eds) Vertebrate circadian systems. Springer-Verlag, Berlin, pp 297–304
Hoogenboom I, Daan S, Dallingia JH, Schoenmakers M (1984) Seasonal change in the daily timing of behaviour of the common vole, Microtus arvalis. Oecologia (Berl) 61:18–31
Horton TH, Stetson MH (1992) Maternal transfer of photoperiodic information in rodents. Anim Reprod Sci 30:29–44
Hufnagl S, Franceschini-Zink C, Millesi E (2011) Seasonal constraints and reproductive performance in female common hamsters (Cricetus cricetus). Mamm Biol 76:124–128
Hut RA, Van Oort BEH, Daan S (1999) Natural entrainment without dawn and dusk: the case of the European ground squirrel (Spermophilus citellus). J Biol Rhythms 14:290–299
Illnerová H, Hoffmann K, Vanecek J (1984) Adjustment of pineal melatonin and N-acetyltransferase rhythms to change from long to short photoperiod in the Djungarian hamster Phodopus sungorus. Neuroendocrinology 38:226–231
Isaac JL (2009) Effects of climate change on life history: implications for extinction risk in mammals. Endang Species Res 7:115–123
Jallageas M, Mas N, Saboureau M, Roussel JP, Lacroix A (1993) Effects of bilateral superior cervical ganglionectomy on thyroid and gonadal functions in the edible dormouse Glis glis. Comp Biochem Physiol 104:299–304
Johnson CH (1999) Forty years of PRCs: what have we learned? Chronobiol Int 16:711–743
Johnson CH, Elliott JA, Foster RG, Homna KI, Kronauer R (2004) Fundamental properties of circadian rhythms. In: Dunlap JC, Loros JJ, DeCoursey PJ (eds) Chronobiology: biological timekeeping. Sinauer Associates, Sunderland, pp 67–103
Johnston PG, Boshes M, Zucker I (1982) Photoperiodic inhibition of testicular development is mediated by the pineal gland in white-footed mice. Biol Reprod 26:597–602
Karaseva EV (1962) A study of the pecularities of territory utilization by the hamster in the Altai territory carried out with the use of labelling. Zool Zh 41:275–285
Kayser A, Stubbe M, Weinhold U (2003) Mortality factors of the common hamster Cricetus cricetus at two sites in Germany. Acta Theriol 48:47–57
Kayser C (1964) La dépense d’ènergie des mammifères en hibernation [The energy expenditure of mammals during hibernation]. Arch Sci Physiol 18:137–150
Kayser C (1971) La dépense d’énergie des hibernants au cours du cycle circannien [Energy expenditure in hibernating animals during the circanual cycle]. C R Séances Soc Biol Fil 165:1145–1147
Kayser C, Aron M (1938) Cycle d’activité saisonnière des glandes endocrines chez un hibernant, le hamster (Cricetus frumentarius) [Cycle of seasonal activity in the endocrine glands of a hibernator (Cricetus frumentarius)]. C R Séances Soc Biol Fil 129:225–226
Kayser C, Aron M (1950) Le cycle saisonnier des glandes endocrines chez les hibernants [Seasonal cycles of enocrine glands in hibernators]. Arch Anat Histol Embriol 33:21–42
Kayser C, Frank RM (1963) Comportement des tissus calcifies du hamster d’Europe Cricetus cricetus au cours de l’hibernation [Behavior of calcified tissues of the European hamster Cricetus cricetus in the course of hibernation]. Arch Oral Biol 8:703–713
Kayser C, Haug AM (1969) Evolution saisonnière des bilans calciques chez un hibernant, le Hamster d’Europe (Cricetus cricetus) [Seasonal development of calcium balance in a hibernator, the European hamster (Cricetus cricetus)]. C R Séances Soc Biol Fil 162:1834–1837
Kayser C, Schwartz J (1960) Evolution saisonnière de l’élimination urinaire des 17-cétostéroides et des stéroides formadéhydogéniques chez le Hamster ordinaire (Cricetus cricetus) [Seasonal evolution of the urinary elimination of 17-ketosteroids and formaldehydrogenic steroids in the hamster (Cricetus cricetus)]. C R Séances Soc Biol Fil 154:778–780
Kayser C, Petrovic A, Porte A (1961) Variations ultrastructurales de la parathyroide du Hamster ordinaire (Cricetus cricetus) au cours du cycle saisonnier [Ultrastructural variations of the parathyroid of the Common hamster (Cricetus cricetus)]. C R Séances Soc Biol Fil 155:2178–2181
Kempf E, Mack G, Canguilhem B, Mandel P (1978) Seasonal changes in the levels and the turnover of brain serotonin and noradrenalin in the European hamster kept under constant environment. Experientia (Basel) 34:1032–1033
Kirn N (2004) Ontogenese des Europäischen Feldhamsters (Cricetus cricetus) unter dem Einfluß verschiedener prä- und postnataler Photoperioden [Ontogeny in the European hamster (Cricetus cricetus) in different pre- and postnatal photoperiods]. Inaugural dissertation. Institut of Zoology, University of Veterinary Medicine, Hannover
Kowalczyk R, Jędrzejewska B, Zalewski A (2003) Annual and circadian activity patterns of badgers (Meles meles) in Białowieża Primeval Forest (eastern Poland) compared with other palaearctic populations. J Biogeogr 30:463–472
Krsmanovic L, Mikes M, Habijan V, Mikes B (1984) Reproductive activity of Cricetus cricetus L. in Vojvodina-Yugoslavia. Acta Zool Fenn 171:173–174
La Haye MJJ, Neumann K, Koelewijn HP (2012) Strong decline of gene diversity in local populations of the highly endangered common hamster (Cricetus cricetus) in the western part of its European range. Conserv Gen 13:311–322
Lee TM, Zucker I (1995) Seasonal variations in circadian rhythms persist in gonadectomized golden-mantled ground squirrels. J Biol Rhythms 10:188–195
Lee TM, Carmichael MS, Zucker I (1986) Circannual variations in circadian rhythms of ground squirrels. Am J Physiol 250:R831–R836
Lincoln GA, Libre EA, Merriam GR (1989) Long-term reproductive cycles in rams after pinealectomy or superior cervical ganglionectomy. J Reprod Fertil 85:687–704
Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG (2006) Characterizing a mammalian circannual pacemaker. Science 314:1941–1944
Martinet L, Allain D (1985) Role of the pineal gland in the photoperiodic control of reproductive and non-reproductive functions in mink (Mustela vison). In: Evered D, Clark S (eds) Photoperiodism, melatonin and the pineal. Ciba Foundation Symposium, vol 17. Bath Press, Avon, pp 170–187
Masson-Pévet M, Gauer F (1994) Seasonality and melatonin receptors in the pars tuberalis in some long day breeders. Biol Signals 3:63–70
Masson-Pévet M, Pévet P, Vivien-Roels B (1987) Pinealectomy and constant release of melatonin or 5-methoxytryptamine induce testicular atrophy in the European hamster (Cricetus cricetus L.). J Pineal Res 4:79–88
Masson-Pévet M, Naimi F, Canguilhem B, Saboureau M, Bonn D, Pévet P (1994) Are the annual reproductive and body weight rhythms in the male European hamster (Cricetus cricetus) dependent upon a photoperiodically entrained circannual clock? J Pineal Res 17:151–163
Millesi E, Lebl K, Pflaum C, Franceschini C (2004) Reproductive effort in male common hamsters. In: Losinger I (ed) 12th meeting of the international hamster workgroup. ONCFS, Strasbourg, pp 67–69
Miro JL, Canguilhem B, Schmitt P (1980) Effects of bulbectomy on hibernation, food intake and body weight in the European hamster, Cricetus cricetus. Physiol Behav 24:859–862
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
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
Miyazaki Y, Nisimura T, Numata H (2007) Phase resetting and phase singularity of an insect circannual oscillator. J Comp Physiol A 193:1169–1176
Mletzko I, Raths P (1972) Temperaturadaptation und Stoffwechselrhythmik beim Hamster (Cricetus cricetus L.) [Temperature adaptations and metabolic rhythm in the hamster (Cricetus cricetus L.)]. Zool Jahrb Physiol 76:531–553
Møller M, Masson-Pevet M, Pevet P (1998) Annual variations of the NPYergic innervation of the pineal gland in the European hamster (Cricetus cricetus): a quantitative immunohistochemical study. Cell Tissue Res 291:423–431
Monecke S (2013) All things considered? Alternative reasons for hamster extinction. Zool Pol 58:41–47
Monecke S, Wollnik F (2004) European hamsters (Cricetus cricetus) show a transient phase of insensitivity to long photoperiods after gonadal regression. Biol Reprod 70:1438–1443
Monecke S, Wollnik F (2005) Seasonal variations in circadian rhythms coincide with a phase of sensitivity to short photoperiods in the European hamster. J Comp Physiol B 175:167–183
Monecke S, Wollnik F (2008) How to increase the reproductive success in European hamsters: shiftwork in the breeding colony. In: Millesi E, Winkler H, Hengsberger R (eds) 13th meeting of the international hamster workgroup (2005). The common hamster (Cricetus cricetus): perspectives on an endangered species. Austrian Academy of Sciences Press, Illmitz/Vienna, pp 97–114
Monecke S, Malan A, Wollnik F (2006) Asymmetric control of short day response in European hamsters. J Biol Rhythms 21:290–300
Monecke S, Saboureau M, Malan A, Bonn D, Masson-Pévet M, Pévet P (2009) Circannual phase response curves to short and long photoperiod in the European hamster. J Biol Rhythms 24:413–426
Monecke S, Malan A, Saboureau M, Pévet P (2010) Phase shift of the circannual reproductive rhythm in European hamsters by 2 days of long photoperiod. Neuroendocrinol Lett 31:738–742
Monecke S, Bonn D, Reibel-Foisset S, Pévet P (2011a) Breeding success in aged female common hamsters (Cricetus cricetus). Säugetierkd Inf 8:121–129
Monecke S, Malan A, Pévet P (2011b) Longterm temperature recordings in European hamsters. In: Monecke S, Pévet P (eds) 18th meeting of the International Hamster Workgroup (2011). From fundamental research to population management: refining conservation strategies for the European hamster [Cricetus cricetus L.]. INCI-CNRS, Strasbourg, pp 17–19
Monecke S, Sage-Ciocca D, Wollnik F, Pévet P (2013) Photoperiod can entrain circannual rhythms in pinealectomized European hamsters. J Biol Rhythms 28:278–290
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
Morano I, Adler K, Agostini B, Hasselbach W (1992) Expression of myosin heavy and light chains and phosphorylation of the phosphorylatable myosin light chain in the heart ventricle of the European hamster during hibernation and in summer. J Muscle Res Cell Motil 13:64–70
Mrosovsky N (1985) Thermal effetcs on the periodicity, phasing, and persistence of circannual cycles. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations. Proceedings of the 7th international symposium on natural mammalian hibernation 1985. Elsevier, Fallen Leaf Lake, CA, pp 403–410
Nechay G (2000) Status of hamsters Cricetus cricetus, Cricetus migratorius, Mesocricetus newtoni and other hamster species in Europe. Council of Europe, Strasbourg Cedex
Nechay G, Hamar M, Grulich L (1977) The common hamster (Cricetus cricetus [L.]); a review. EPPO Bull 7:255–276
Neumann K, Kayser A, Mundt G, Gattermann R, Michaux JR, Maak S, Jansman HAH (2005) Genetic spatial structure of European common hamsters (Cricetus cricetus): a result of repeated range expansion and demographic bottlenecks. Mol Ecol 14:1473–1483
Nisimura T, Numata H (2001) Endogenous timing mechanism controlling the circannual pupation rhythm of the varied carpet beetle Anthrenus verbasci. J Comp Physiol A 187:433–440
Paul MJ, Zucker I, Schwartz WJ (2008) Tracking the seasons: the internal calendars of vertebrates. Philos Trans R Soc Lond B Biol Sci 363(1490):341–361
Pengelley ET (1974) Circannual rhythmicity in hibernating mammals. In: Pengelley ET (ed) Circannual clocks: annual biological rhythms. Academic, New York, pp 95–160
Petrovic A, Kayser C (1957) L’activité gonadotrope de la préhypophyse du hamster (Cricetus cricetus) au cours de l’année [Gonadotropic activity of the anterior pituitary in hamster (Cricetus cricetus) during the course of the year]. C R Seances Soc Biol Fil 151:996–998
Petrovic A, Kayser C (1958) Variations saisonnières du seuil réactionnel de la thyroide à la thyréostimuline chez le hamster (Cricetus cricetus) [Seasonal variations of reaction threshold of the thyroid to thyrostimuline in hamster (Cricetus cricetus)]. J Physiol 50:446–450
Petterborg LJ, Reiter RJ, Brainard GC (1981) Ovarian response of pinealectomized and intact white-footed mice kept under naturally short photoperiods. Experientia (Basel) 37:247
Pévet P, Pitrosky B (1997) The nocturnal melatonin peak and the photoperiodic response. Front Horm Res 23:14–24
Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J Comp Physiol A 106:333–355
Pleschka K, Nürnberger F (1997) Beta-adrenergic signal transduction in the hypothalamus of the European hamster: relation with the seasonal hibernation cycle and the diurnal activity cycle. Biol Cell 89:525–529
Pleschka K, Heinrich A, Witte K, Lemmer B (1996) Diurnal and seasonal changes in sympathetic signal transduction in cardiac ventricles of European hamsters. Am J Physiol Regul Integr Comp Physiol 270:R304–R309
Randall CF, Bromage NR, Duston J, Symes J (1998) Photoperiod-induced phase-shifts of the endogenous clock controlling reproduction in the rainbow trout: a circannual phase-response curve. J Reprod Fertil 112:399–405
Raths P, Mletzko I (1971) Die Stoffwechselrhythmik des Hamsters (Cricetus cricetus L.) im Sommer [The metabolic rhythm of the hamster (Cricetus cricetus) in summer]. Zool Jahrb Biol 106:198–208
Refinetti R (2012) Integration of biological clocks and rhythms. Compr Physiol 2:1213–1239
Reiners TE, Eidenschenk J, Neumann K, Nowak C (2014) Preservation of genetic diversity in a wild and captive population of a rapidly declining mammal, the common hamster of the French Alsace region. Mamm Biol 79:240–246
Reiter RJ (1974) Pineal mediated regression of the reproductive organs of female hamsters exposed to natural photoperiods during the winter months. Am J Obstet Gynecol 118:878–880
Reiter RJ (1975) Exogenous and endogenous control of the annual reproductive cycle in the male golden hamster: participation of the pineal gland. J Exp Zool 191:111–120
Reiter RJ (1993) The melatonin rhythm: both a clock and a calendar. Experientia (Basel) 49:654–664
Reznik G, Reznik-Schüller H, Mohr U (1976) Clinical anatomy of the European hamster Cricetus cricetus L. U.S. Department of Health, Education and Welfare, Public Health Services, National Institute of Health, Washington, DC
Reznik-Schüller H, Reznik G (1973) Comparative histometric investigations of the testicular function of European hamsters (Cricetus cricetus) with and without hibernation. Fertil Steril 24:698–705
Reznik-Schüller H, Reznik G (1974) The influence of hibernation upon the ultrastructure of the Leydig cells and spermatids of the European hamster. Fertil Steril 25:621–635
Rhodes DH (1989) The influence of multiple photoperiods and pinealectomy on gonads, pelage and body weight in male meadow voles, Microtus pennsylvanicus. Comp Biochem Physiol A 93:445–449
Ribelayga C, Pévet P, Simonneaux V (1998) Possible involvement of neuropeptide Y in the seasonal control of hydroxyindole-O-methyltransferase activity in the pineal gland of the European hamster (Cricetus cricetus). Brain Res 777:247–250
Robinson RA, Crick HQP, Learmonth JA, Maclean IMD, Thomas CD, Bairlein F, Forchhammer MC, Francis CM, Gill JA, Godley BJ, Harwood J, Hays GC, Huntley B, Hutson AM, Pierce GJ, Rehfisch MM, Sims DW, Begona Santos M, Sparks TH, Stroud DA, Visser ME (2009) Travelling through a warming world: climate change and migratory species. Endang Species Res 7:87–99
Rusin MY, Banaszek A, Mishta AV (2013) The common hamster (Cricetus cricetus) in Ukraine: evidence for population decline. Folia Zool 62:207–213
Ružić A (1976) Neke osobenosti hibernacije hrčka (Cricetus cricetus L.) i njihov značaj za suzbijanje ove štetočine [Some peculiarities in the hibernation of the hamster (Cricetus cricetus L.) and their importance for the control of that pest]. Zastita Bilja (Beograd) 27:397–417
Saboureau M, Masson-Pévet M, Canguilhem B, Pévet P (1999) Circannual reproductive rhythm in the European hamster (Cricetus cricetus): demonstration of the existence of an annual phase of sensitivity to short photoperiod. J Pineal Res 26:9–16
Sáenz de Miera C, Monecke S, Bartzen-Sprauer J, Laran-Chich MP, Pévet P, Hazlerigg D, Simonneaux V (2014) A circannual clock drives expression of genes central for seasonal reproduction. Curr Biol 24(13):1500–1506
Scantlebury M, Danek-Gontard M, Bateman PW, Bennett NC, Manjerovic MB, Joubert KE, Waterman JM (2012) Seasonal patterns of body temperature daily rhythms in group-living Cape ground squirrels Xerus inauris. PLoS One 7:e36053
Scherbarth F, Steinlechner S (2008) The annual activity pattern of Djungarian hamsters (Phodopus sungorus) is affected by wheel-running activity. Chronobiol Int 25:905
Schmelzer E (2005) Aktivitätsmuster und Raumnutzung einer Feldhamsterpopulation (Cricetus cricetus) im urbanen Lebensraum [Activity patterns and spatial organisation in a colony of common hamsters (Cricetus cricetus) in an urban environment]. Diploma thesis. Faculty of Life Sciences, University of Vienna
Schmelzer E, Millesi E (2003) Activity patterns in a population of European hamsters (Cricetus cricetus) in an urban environment. In: Nechay G (ed) 11th meeting of the international hamster workgroup. Budapest, Hungary, pp 19–22
Seluga K, Stubbe M, Mammen U (1996) Zur Reproduktion des Feldhamsters (Cricetus cricetus L.) und zum Ansiedlungsverhalten der Jungtiere. [Reproduction of the common hamster (Cricetus cricetus L.) and the settlement of the young]. Abh Ber Mus Heineanum 3:129–142
Sidorov GV, Kassal BY, Goncharova AV, Vakhrushev KV (2011) Theriofauna of Omsk oblast: game species of rodents [in Russian]. Nauka (Publishing House Amphora), Omsk
Siutz C, Pluch M, Ruf T, Millesi E (2012) Sex differences in foraging behaviour, body fat and hibernation patterns of free-ranging common hamsters. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world. Springer-Verlag, Berlin
Skene DJ, Masson-Pévet M, Pévet P (1993) Seasonal changes in melatonin binding sites in the pars tuberalis of male European hamsters and the effect of testosterone manipulation. Endocrinology 132:1682–1686
Steinlechner S (1992) Melatonin: an endocrine signal for the night length. Verh Dtsch Zool Ges 85:217–229
Steinlechner S (2011) Biologische Bedeutung saisonaler und circannualer Rhythmen bei Tier und Mensch [Biological significance of seasonal and circannual rhythms in animals and humans]. Nova Acta Leopoldina NF 114:85–109
Stoeckel ME, Petrovic A, Porte A, Kayser C (1964a) Etude ultrastructurale du cortex surrénalien chez un hibernant, le hamster ordinaire (Cricetus cricetus), au cours du cycle saisonnier [Ultrastructural study of the adrenal cortex in a hibernator, the common hamster (Cricetus cricetus)]. J Physiol 56:442–443
Stoeckel ME, Petrovic A, Porte A, Kayser C (1964b) Variations ultrastructurales du cortex surrénalien au cour du cycle saisonnier chez un hibernant, le Hamster ordinaire (Cricetus cricetus) [Ultrastructural variations of the adrenal cortex during the seasonal cycle of a hibernator, the common hamster (Cricetus cricetus)]. C R Séances Soc Biol Fil 158:1570–1572
Stoeckel ME, Porte A, Canguilhem B (1967) Sur l’ultrastructure des cellules parafolliculaires de la thyroide du hamster sauvage (Cricetus cricetus) [Ultrastructure of the parafollicular cells of the wild hamster (Cricetus cricetus)]. C R Acad Sci Paris 264D:2490–2492
Stubbe M, Stubbe A (1998) The European hamster (Cricetus cricetus L.) as prey of human and animal as well as its importance for the ecosystem. In: Stubbe M, Stubbe A (eds) Ecology and protection of the common hamster. Martin-Luther-Universität Halle-Wittenberg, Halle/Saale, pp 81–86
Surdacki S (1964) Über die Nahrung des Hamsters, Cricetus cricetus Linnaeus, 1758 [On the nutrition of hamsters, Cricetus cricetus Linnaeus, 1758]. Acta Theriol 9:384–386
Tournier BB, Dardente H, Simonneaux V, Vivien-Roels B, Pevet P, Masson-Pevet M, Vuillez P (2007) Seasonal variations of clock gene expression in the suprachiasmatic nuclei and pars tuberalis of the European hamster (Cricetus cricetus). Eur J Neurosci 25:1529–1536
Turek FW, Campbell CS (1979) Photoperiodic regulation of neuroendocrine-gonadal activity. Biol Reprod 20:32–50
van Oort BE, Tyler NJ, Gerkema MP, Folkow L, Blix AS, Stokkan KA (2005) Circadian organization in reindeer. Nature (Lond) 438:1095–1096
van Oort BEH, Tyler NJC, Gerkema MP, Folkow L, Stokkan KA (2007) Where clocks are redundant: weak circadian mechanisms in reindeer living under polar photic conditions. Naturwissenschaften 94:183–194
Visser ME, Caro SP, Oers KV, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc B 365:3113–3127
Vivien-Roels B, Pévet P, Masson-Pévet M, Canguilhem B (1992) Seasonal variations in the daily rhythm of pineal gland and/or circulating melatonin and 5-methoxytryptophol concentrations in the European hamster, Cricetus cricetus. Gen Comp Endocrinol 86:239–247
Vivien-Roels B, Pitrosky B, Zitouni M, Malan A, Canguilhem B, Bonn D, Pévet P (1997) Environmental control of the seasonal variations in the daily pattern of melatonin synthesis in the European hamster, Cricetus cricetus. Gen Comp Endocrinol 106:85–94
Vohralík V (1974) Biology of the reproduction of the common hamster, Cricetus cricetus (L.). Vest Cs Spol Zool 38:228–240
Vuillez P, Jacob N, Teclemariam-Mesbah R, Pévet P (1996) In Syrian and European hamsters, the duration of sensitive phase to light of the suprachiasmatic nuclei depends on the photoperiod. Neurosci Lett 208:37–40
Ware JV, Nelson OL, Robbins CT, Jansen HT (2012) Temporal organization of activity in the brown bear (Ursus arctos): roles of circadian rhythms, light, and food entrainment. Am J Physiol Regul Integr Comp Physiol 303:R890–R902
Wassmer T (2004) Body temperature and above-ground patterns during hibernation in European hamsters (Cricetus cricetus L.). J Zool Lond 262:281-288.
Waßmer T, Wollnik F (1997) Timing of torpor bouts during hibernation in European hamsters (Cricetus cricetus L.). J Comp Physiol B 167:270–279
Weidling A, Stubbe M (1998) Eine Standardmethode zur Feinkartierung von Feldhamsterbauen [A standard method for exact mapping of burrows of European hamsters]. In: Stubbe M, Stubbe A (eds) Ecology and protection of the common hamster. Martin-Luther-Universität Halle-Wittenberg, Halle/Saale, pp 259–276
Weinert D, Schöttner K, Surov AV, Fritzsche P, Feoktistova NY, Ushakova MV, Ryurikow GB (2009) Circadian activity rhythm of dwarf hamsters (Phodopus spp.) under laboratory and semi-natural conditions. Russ J Theriol 8:47–58
Weinhold U, Kayser A (2006) Der Feldhamster [The European hamster]. Westarp Wissenschaften-Verlagsgesellschaft, Hohenwarsleben
Wendt W (1989) Zum Aktivitätsverhalten des Feldhamsters, Cricetus cricetus L., im Freigehege [About the activity behaviour of European hamsters, Cricetus cricetus L., in outdoor enclosures. Säugetierkd Inf 3:3–12
Wendt W (1991) Der Winterschlaf des Feldhamsters Cricetus cricetus (L., 1758): energetische Grundlagen und Auswirkungen auf die Populationsdynamik [Hibernation in the European hamster Cricetus cricetus (L. 1758): energetic basics and the consequences on population dynamics]. Populationsökologie von Kleinsäugerarten. Wiss Beitr Univ Halle 1990/34 (P42):67–78
Williams CT, Barnes BM, Buck CL (2011a) Daily body temperature rhythms persist under the midnight sun but are absent during hibernation in free-living arctic ground squirrels. Biol Lett 8:31–34
Williams CT, Sheriff MJ, Schmutz JA, Kohl F, Tøien Ø, Buck CL, Barnes BM (2011b) Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living Arctic hibernator. J Comp Physiol B 181:1101–1109
Wollnik F, Schmidt B (1995) Seasonal and daily rhythms of body temperature in the European hamster (Cricetus cricetus) under semi-natural conditions. J Comp Physiol B 165:171–182
Wollnik F, Breit A, Reinke D (1991) Seasonal change in the temporal organization of wheel-running activity in the European hamster, Cricetus cricetus. Naturwissenschaften 78:419–422
Woodfill CJI, Wayne NL, Moenter SM, Karsch FJ (1994) Photoperiodic synchronization of a circannual reproductive rhythm in sheep: identification of season-specific time cues. Biol Reprod 50:965–976
Ziomek J (2011) Chomik europejski (Cricetus cricetus L.) w mozaikowym krajobrazie rolniczym południowej Polski [The European hamster (Cricetus cricetus L.) in a mosaic of arable fields in south Poland]. Dissertation. Department of Systematic Zoology, Adam Mickiewicz University of Poznan, Wroclaw
Zucker I (2001) Circannual rhythms: mammals. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioral neurobiology: circadian clocks. Kluwer Academic/Plenum, New York, pp 509–528
Acknowledgments
This work was mainly supported by the German Wildlife Foundation (Deutsche Wildtierstiftung). Further support came from the CNRS and the University of Stuttgart, as well as the German Research Foundation (DFG).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Japan
About this chapter
Cite this chapter
Monecke, S., Wollnik, F., Pévet, P. (2014). The Circannual Clock in the European Hamster: How Is It Synchronized by Photoperiodic Changes?. In: Numata, H., Helm, B. (eds) Annual, Lunar, and Tidal Clocks. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55261-1_14
Download citation
DOI: https://doi.org/10.1007/978-4-431-55261-1_14
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55260-4
Online ISBN: 978-4-431-55261-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)