The Circadian Organization of Reptiles

  • C. Bertolucci
  • A. Foà
  • G. Tosini


The present review summarizes the current knowledge of the circadian organization of Reptiles. This taxonomic group has provided (and continue to provide) a very useful experimental model for the understanding of the vertebrate circadian system. The circadian organization of reptiles is multioscillatory in nature. The retinas, the pineal and the parietal eye (and, possibly, the SCN) contain circadian clocks. Of particular interest is the observation that the role these structures play in the circadian organization varies considerably among species and within the same species in different seasons. Another remarkable feature of this class is the redundancy of circadian photoreceptors: retinas of the lateral eyes, pineal, parietal eye and the brain all contain photoreceptors.


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  1. Aschoff, J. (1960) Exogenous and endogenous components in circadian rhythms. Cold Spr. Harb. Symp. Quant. Biol. 25: 11–28.Google Scholar
  2. Bartell, P., Miranda-Anaya, M., Menaker, M. (1999) Effects of light, pinealectomy and enucleation on the circadian organization of the green iguana. International Congress on Chronobiology Abs.: 49.Google Scholar
  3. Berk, M.L., Heath, J.E. (1975) Effects of preoptic, hypothalamic and telencephalic lesion on thermoregulation in lizards, Dipsosaurus dorsalis. J. Therm. Biol. 1: 65–78.Google Scholar
  4. Bertolucci, C., Foà, A. (1998) Seasonality and role of the SCN in entrainment of lizard circadian locomotor rhythms to daily melatonin injections. Am. J. Physiol. 274(43): R1004 — R1014.PubMedGoogle Scholar
  5. Casini, G., Petrini, P., Foà, A., Bagnoli, P. (1993) Pattern of organization of primary visual pathways in the European lizard Podarcis sicula Rafinesque. J. Hirnforsch. 34: 361–374.PubMedGoogle Scholar
  6. Cassone, V.M. (1990) Effetcs of melatonin on vertebrate circadian systems. Trends in Neurosci. 13: 457–464. Cowgell, G., Underwood, H. (1979) Behavioral theroregulation in lizards: circadian rhythm. J. Exp. Zool. 210: 189–194.Google Scholar
  7. Firth, B.T., Kennaway, D.J., Rozenbilds, M.A.M. (1979) Plasma melatonin in the scincid lizard, Thachydosaurus rugosus: diel rhythms, seasonality, and the effects of constant light and constant darkness. Gen. Comp. Endocrinol. 37: 493–500.Google Scholar
  8. Firth, B.T., Kennaway, D.J. (1980) Plasma melatonin levels in the scincid lizard Thachydosaurus rugosus: effect of constant and fluctuating temperature. Brain Res. 404: 313–318.CrossRefGoogle Scholar
  9. Firth, B.T., Kennaway, D.J. (1987) Melatonin content of pineal, parietal eye and blood plasma of the lizard, Thachydosaurus rugosus: effect of constant and fluctuating temperature. Brain Res. 404: 313–318.PubMedCrossRefGoogle Scholar
  10. Firth, B.T., Thompson, M.B., Kennaway, D.J. (1989) Thermal sensitivity of reptilian melatonin rhythms “cold” tuatara vs. “warm” skink. Am. J. Physiol. 256: R1160 — R1163.PubMedGoogle Scholar
  11. Firth, B.T., Belan, I., Kennaway, D.J., Moyer, R.W. (1999) Thermocyclic entrainment of lizard blood plasma melatonin rhythms in constant and cyclic photic environments. Am. J. Physiol. 277: R1620 — R1626.PubMedGoogle Scholar
  12. Foà, A. (1991) The role of the pineal and the retinae in the expression of circadian locomotor rhythmicity in the ruin lizard, Podarcis sicula. J. Comp. Physiol. A 169: 201–207.Google Scholar
  13. Foà, A., Janik, D., Minutini, L. (1992a) Circadian rhythms of plasma melatonin in the ruin lizard Podarcis sicula: effetcs of pinealectomy. J. Pineal Res. 12: 109–113.PubMedCrossRefGoogle Scholar
  14. Foà, A., Minutini, L., Innocenti A (1992b) Melatonin: a coupling device between oscillators in the circadian system of the ruin lizard Podarcis sicula. Comp. Biochem. Physiol. A 103: 719–723.Google Scholar
  15. Foà, A., Flamini, M., Innocenti, A., Minutini, L., Monteforti, G. (1993) The role of extraretinal photoreception in the circadian system of the ruin lizard Podarcis sicula. Comp. Biochem. Physiol. A 105: 223–230.Google Scholar
  16. Foà, A., Monteforti, G., Minutini, L., Innocenti, A., Quaglieri, C., Flamini, M. (1994) Seasonal changes of locomotor activity patterns in ruin lizards Podarcis sicula. I. Endogenous control by the circadian system Behay. Ecol. Sociobiol. 34: 227–274.Google Scholar
  17. Foà, A., Bertolucci, C., Marsanich, A., Innocenti, A. (1997) Pineal transplantation to the brain of pinealectomized lizards: effects on circadian rhythms of locomotor activity. Behay. Neurosc. 111: 1123–1132.Google Scholar
  18. Foster, R.G., Garcia-Fernandez, J.M., Provencio, I., DeGrip, W.J. (1993) Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J. Comp. Physiol. A 172: 33–45.Google Scholar
  19. Grace, M.S., Alones, V., Menaker, M., Foster, R.G. (1996) Light perception in the vertebrate brain: an ultrastructural analysis of opsin-and vasoactive intestinal polypeptide-immunoreactive neurons in iguanid lizards. J. Comp. Neurol. 367: 575–594.Google Scholar
  20. Hyde, L.L., Underwood, H. (1995) Daily melatonin infusions entrain the locomotor activity of pinealectomized lizards. Physiol. Behay. 58: 953–951.Google Scholar
  21. Hoffmann, K. (1960) Versuche zur Analyse der Tagesperiodik, I. Der Einfluss der Lichtintensitaet. Z. Vergl. Physiol. 43: 544–566.Google Scholar
  22. Hoffmann, K. (1970) Zur Syncronisation biologischer Rhythmen. Verh. Dtsch. Zool. Ges. pp. 166–273. Innocenti, A., Minutini, L., Foà, A. (1993) The pineal and circadian rhythms of temperature selection and locomotion in lizards. Physiol. Behay. 53: 911–915.Google Scholar
  23. Innocenti, A., Minutini, L., Foà, A. (1994) Seasonal changes of locomotor activity patterns in ruin lizards Podarcis sicula. II. Involvement of the pineal. Behay. Ecol. Sociobiol. 35: 27–32.Google Scholar
  24. Innocenti, A., Bertolucci, C., Minutini, L., Foà, A. (1996) Seasonal variations of pineal involvement in the circadian organization of ruin lizards Podarcis sicula. J. Exp. Biol. 199: 1189–1194.Google Scholar
  25. Janik, D.S., Menaker, M. (1990) Circadian locomotor rhythms in the desert iguana I. The role of the eyes and the pineal. J. Comp. Physiol. A 166: 803–810Google Scholar
  26. Janik, D.S., Pickard, G.E., Menaker, M. (1990) Circadian locomotor rhythms in the desert iguana. II: Effects of electrolytic lesions to the hypothalamus. J. Comp. Physiol. A 166: 811–816Google Scholar
  27. Janik, D.S., Cassone, V.M., Pickard, G.E., Menaker, M. (1994) Retinohypothalamic projections and immunocytochemical analysis of the suprachiasmatic region of the desert iguana Dipsosaurus dorsalis. Cell Tiss. Res. 275: 399–406.Google Scholar
  28. Jailing, C., Scarperi, M., Bleichert, A. (1989) Circadian rhythm in the temperature preference of the turtle, Chrysemys (= Pseudemys) scripta elegans, in a thermal gradient. J. Therm. Biol. 14: 173–178.Google Scholar
  29. Kasai, C., Menaker, M., Perez-Polo, R. (1979) Circadian clock in culture: N-acetyltransferase activity of chick pineal glands oscillates in vitro. Science 203: 656–658.CrossRefGoogle Scholar
  30. Kavaliers, M., Ralph, C.L. (1981) Encephalic photoreceptor involvement in the entrainment and control of circadian activity of young American alligators. Physiol. Behay. 26: 413–418.Google Scholar
  31. Menaker, M. (1982) The search for principles of physiological organization in vertebrate circadian system. In: Aschoff, J., Daan, S., Groos, G.A. (eds.) Vertebrate circadian system. Springer-Verlag, Berlin, pp. 1–12.Google Scholar
  32. Menaker, M. (1985) Eyes—the second (and third) pineal gland? In: Evered, D., Clark, S. (eds.) Photoperiodism, melatonin and pineal. Pitman, London, pp. 39–52.Google Scholar
  33. Menaker, M., Wisner, S. (1983) Temperature-compensated circadian clock in the pineal of Anolis. Proc. Natl. Acad. Sci. USA 80: 6119–6121.Google Scholar
  34. Menaker, M., Tosini, G. (1996). The Evolution of Vertebrate Circadian System. In: Honma, K., Honma, S. (eds.) Circadian Organization and Oscillatory Coupling. Hokkaido University Press, Sapporo, pp. 39–52.Google Scholar
  35. Minutini, L. Innocenti, A., Bertolucci, C., Foà, A. (1994) Electrolytic lesions to the optic chiasma affect circadian locomotor rhythms in lizard. Neuroreport 5:525–527.Google Scholar
  36. Miranda-Anaya, M., Bartell, P., Yamasaki, S., Menaker, M. (1999) Circadian rhythm of electroretinographich response (ERG) and effect of pinealectomy in Iguana iguana. Soc. Neurosci. Abs. 25: 1132.Google Scholar
  37. Molina-Borja, M. (1996) Pineal-gland and circadian locomotor-activity rhythm in the lacertid Gallotia galloti eisentrauti, pinealectomy induces arrhythmicity. Biol. Rhythm Res. 27: 1–11.Google Scholar
  38. Moyer, R.B., Firth, B.T., Kennaway, D.J. (1995) Effect of constant temperatures, darkness and light on the secretion of melatonin by pineal explants and retinas in the gecko Christinus marmoratus. Brain Res. 675: 345–348.PubMedCrossRefGoogle Scholar
  39. Pasqualetti, M., Innocenti, A., Foà, A., Nardi, I. (1997) Cloning of a brain opsin from lizard Podarcis sicula. Biol. Rhythms Res. 28: 127.Google Scholar
  40. Pickard, G.E., Tang, W.X. (1993) Individual pineal cells exhibit a circadian rhythm in melatonin secretion. Brain Res. 627: 141–146.PubMedCrossRefGoogle Scholar
  41. Pittendrigh, C.S. (1981) Circadian system: entrainment. In: Aschoff, J. (ed.) Handbook of Behavioural Neurobiology. Biological Rhythms. Plenum Press, New York, 4: 95–124.Google Scholar
  42. Refinetti, R., Susalka, S.J. (1997). Circadian rhythm of temperature selection in a nocturnal lizard. Physiol. Behay. 62: 331–336.Google Scholar
  43. Shaw, A.P., Collazo, C.R., Easterling, K., Young, C.D., Karwoski, C.J. (1993). Circadian rhythm in the visual system of the lizard Anolis carolinensis. J. Biol. Rhythms 8: 107–124.PubMedCrossRefGoogle Scholar
  44. Tilden, A.R., Hutchison, V.H. (1993) Influence of photoperiod and temperature on serum melatonin in the diamondback water snake, Nerodia rhombifera. Gen. Comp. Endocr. 92: 347–354.Google Scholar
  45. Tosini, G. (1997) The pineal complex of Reptiles: physiological and behavioral roles: Ethol. Ecol. Evol. 9: 313–333.Google Scholar
  46. Tosini, G., Menaker, M. (1995) Circadian rhythm of body temperature in an ectotherm (Iguana iguana) J. Biol. Rhythms 10: 248–255.Google Scholar
  47. Tosini, G., Menaker, M. (1996) Pineal complex and melatonin affect the daily rhythm of temperature selection in the green iguana. J. Comp. Physiol. A 179: 135–142.Google Scholar
  48. Tosini, G., Menaker, M. (1998) Multioscillatory circadian organization in a vertebrate, Iguana iguana. J. Neurosc. 18: 1105–1114.Google Scholar
  49. Tosini, G., Moreira, L.F., Bartell, P., Menaker, M. (1998) Temperature compensation of circadian rhythms in a multioscillatory system. SRBR Meeting Abs. 6: 175.Google Scholar
  50. Underwood, H. (1973) Retinal and extraretinal photoreceptors mediate entrainment of the circadian locomotor rhythm in lizard. J. Comp. Physiol. 83: 187–222.Google Scholar
  51. Underwood, H. (1977) Circadian organization in lizards: The role of the pineal organ. Science 195: 587–589. Underwood, H. (1979) Melatonin affects circadian rhythmicity in lizard. J. Comp. Physiol. 130: 317–323.Google Scholar
  52. Underwood, H. (1981) Circadian organization in the lizard, Sceloporus occidentalis: the effects of blinding, pinealectomy and melatonin. J. Comp. Physiol. 141: 537–547.Google Scholar
  53. Underwood, H. (1983) Circadian organization in the lizard Anolis carolinensis: a multioscillatory system. J. Comp. Physiol. 152: 265–274.Google Scholar
  54. Underwood, H. (1985) Pineal melatonin rhythms in the lizard Anolis carolinensis: effects of light and temperature cycles. J. Comp. Physiol. A 157: 57–65.Google Scholar
  55. Underwood, H. (1986) Circadian rhythms in lizards: phase response curve for melatonin. J. Pineal Res. 3: 187–196.Google Scholar
  56. Underwood, H. (1990) The pineal and melatonin: regulators of circadian function in lower vertebrates. Experientia 46: 120–128.PubMedCrossRefGoogle Scholar
  57. Underwood, H. (1992) Endogenous rhythms. In: Gans, C. (ed.) Biology of Reptilia. The University of Chicago Press, Chicago and London, Vol. 18, pp. 22–29.Google Scholar
  58. Underwood, H., Menaker, M. (1970) Extraretinal light perception: entrainment of the biological clock controlling lizard locomotor activity. Science 170: 190–193.PubMedCrossRefGoogle Scholar
  59. Underwood, H., Menaker, M. (1976) Extraretinal photoreception in lizard. Photochem. Photobiol. 24: 227–243. Underwood, H., Harless, M. (1985) Entrainment of the circadian activity rhythm of a lizard to melatonin injection. Physiol. Behay. 35: 267–270.Google Scholar
  60. Underwood, H., Calaban, M. (1987) Pineal melatonin rhythms in lizards Anolis carolinensis: I. Response to light and temperature cycles. J. Biol. Rhythms. 2: 179–193.Google Scholar
  61. Vivien-Roels, B., Arendt, J., Bradtke, J. (1979) Circaadian and circannual fluctuations of pineal indoleamines (serotonin and melatonin) in Testudo hermanni Gmelin ( Reptilia, Chelonia) I. Under natural conditions of photoperiod and temperature. Gen. Comp. Endocr. 37: 197–210.Google Scholar
  62. Vivien-Roels, B., Pevet, P., Claustrat, B. (1988) Pineal and circulating melatonin rhythms in the box turtle, Terrapene carolina triunguis: effects of photoperiod, light pulse, and environmental temperature. Gen. Comp. Endocr. 69: 163–173.Google Scholar
  63. Yamazaki, S., Goto, M., Menaker, M. (1999) No evidence for extraocular photorecptors in the circadian system of the Syrian hamster J Biol. Rhythms 14: 197–201.PubMedCrossRefGoogle Scholar
  64. Xiong, W.H., Solessio, E.C., Yau, K.W. (1998) An unusual cGMP pathway underlying depolarizing light response of vertebrate parietal-eye photoreceptors. Nature Neurosci. 1: 359–365.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • C. Bertolucci
    • 1
  • A. Foà
    • 1
  • G. Tosini
    • 2
  1. 1.Department of BiologyUniversity of FerraraFerraraItaly
  2. 2.Neuroscience InstituteMorehouse School of MedicineAtlantaUSA

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