Skip to main content

Photoperiodism in Birds and Mammals

  • Chapter
Biological Rhythms

Abstract

Using the annual cycle of changing day length, photoperiodic animals restrict their reproductive efforts to a favorable time of year. Thus, the perception and measurement of day length are vital for maximal reproductive success. A clock mechanism to measure day length is necessary for photoperiodic responses. In one section, this chapter reviews the basic principles of the biological clock for measurement of and entrainment to a 24 h light: dark cycle. Some differences between birds and mammals and the ways in which they measure changing day length are highlighted; most notably, differences in photoreception and in the role for the pineal melatonin signal in the transduction of the light: dark signal. The mammalian clock has received a great deal of attention in recent years because of the identification of several clock genes and greater knowledge of how they interact. The clock in birds is less well understood. Birds measure day length in a circadian manner, but in contrast to mammals, pineal melatonin is not involved in photoperiodic time measurement. Seasonal breeding cycles of birds and the photoperiodic regulation of the hypothalamo-pituitary gonadal axis are discussed, as is a newly-identified role for melatonin in birds. Melatonin acts as an inhibitory hormone on seasonal neuroplasticity within the song control system of songbirds, acting in opposition to the stimulatory effects of gonadal steroids. Thus, there is a complex interaction between the circadian system, photoperiodic time measurement, activation and regulation of the neuroendocrine system regulating reproduction and hormonal actions upon the brain.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Arendt, J. (1997) The pineal gland, circadian rhythms and photoperiodism. In: Redfern, P.H. and Lemmer, B. (eds.) Physiology and Pharmacology of Biological Rhythms Springer-Verlag, Berlin, Heidelberg, pp. 375–414.

    Chapter  Google Scholar 

  • Baines, E., Boswell, T., Dunn, I.C., Sharp, R.T., Talbot, R.T. (1999) The effect of photostimulation on the levels of gonadotrophin hormone releasing hormone (GnRH) mRNA in the hypothalamus of Japanese quail (Coturnix coturnix japonica). J. Reprod. Fert. Abs. Series 24: 59.

    Google Scholar 

  • Ball, G.F., Hahn, T.P. (1997) GnRH neuronal systems in birds and their relation to the control of seasonal reproduction. In: Parhar, I.S., Sakuma, Y. (eds.) GnRH Neurons: Gene to Behavior. Brain Shuppan, Tokyo, pp. 325–342.

    Google Scholar 

  • Bartness, T.J., Powers, J.B., Hastings, M.H., Bittman, E.L., Goldman, B.D. (1993) The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception, and the photoperiodic control of seasonal responses? J. Pineal Res. 15: 161–190.

    Google Scholar 

  • Bentley, G.E., Ball, G.F. (2000) Photoperiod-dependent and-independent regulation of melatonin receptors in the forebrain of songbirds. J. Neuroendocrinol. (in press).

    Google Scholar 

  • Bentley, G.E., Goldsmith, A.R., Juss, T.S., Dawson, A. (1997) The effects of nerve growth factor and anti-nerve growth factor antibody on the neuroendocrine reproductive system in the European starling Sturnus vulgaris. Gen. Comp. Endocrinol. 107: 428–438.

    Article  PubMed  CAS  Google Scholar 

  • Bentley, G.E., Goldsmith, A.R., Dawson, A., Briggs, C., Pemberton, M. (1998a) Decreased light intensity alters the perception of day length by male European starlings (Sturnus vulgaris). J. Biol. Rhythms 13: 148–158.

    Article  PubMed  CAS  Google Scholar 

  • Bentley, G.E., Demas, G.E., Nelson, R.J., Ball, G.F. (1998b) Melatonin, immunity and cost of reproductive state in male European starlings. Proc. R. Soc. B 265: 1191–1195.

    Google Scholar 

  • Bentley, G.E., Van’t Hof, Ti.,. Ball, G.F. (1999) Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. Proc. Natl. Acad. Sci. USA 96: 4674–4679.

    Google Scholar 

  • Bentley, G.E., Spar, B.D., MacDougall-Shackleton, S.A., Hahn, T.P., Ball, G.F. (2000) Photoperiodic regulation of the reproductive axis in male zebra finches, Taeniopygia guttata. Gen. Comp. Endocrinol. (in press).

    Google Scholar 

  • Bernard, D.J., Wilson, F.E., Ball, G.F. (1997) Testis-dependent and-independent effects of photoperiod on volumes of song control nuclei in American tree sparrows (Spizella arborea). Brain Res. 760: 163–169.

    Article  PubMed  CAS  Google Scholar 

  • Bunning, E. (1960) Circadian rhythms and the time measurement in photoperiodism. Cold Spr. Harb. Symp. Quant. Biol. 25: 249–256.

    Google Scholar 

  • Dawson, A. (1999) Photoperiodic control of gonadotrophin-releasing hormone secretion in seasonally breeding birds. In: Rao, P., Kluwer, P. (eds.) Neural Regulation in the Vertebrate Endocrine System. Academic/ Plenum Publishers, New York, pp. 141–159.

    Chapter  Google Scholar 

  • Dawson, A., Sharp, P.J. (1998) The role of prolactin in the development of reproductive photorefractoriness and postnuptial molt in the European starling (Sturnus vulgaris). Endocrinol. 139: 485–490.

    Article  CAS  Google Scholar 

  • Deviche, P., Saldanha, C.J., Silver, R. (2000) Changes in brain gonadotropin-releasing hormone-and vasoactive intestinal polypeptide-like immunoreactivity accompanying reestablishment of photosensitivity in male dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 117: 8–19.

    Article  PubMed  CAS  Google Scholar 

  • Dumortier, B., Brunnarius, J. (1989) Diet-dependent switch from circadian to hour-glass-like operation of an insect photoperiodic clock. J. Biol. Rhythms 4: 481–490.

    Article  PubMed  CAS  Google Scholar 

  • Dunn, I.C., Millam, J.R. (1998) Gonadotropin releasing hormone: forms and function in birds. Poultry Avian Biol. Rev. 9: 61–85.

    Google Scholar 

  • Elliot, J.A., Stetson, M.H., Menaker, M. (1972) Regulation of testis function in golden hamsters: a circadian clock measures photoperiodic time. Science 178: 771–773.

    Article  Google Scholar 

  • Farner, D.S., Donham, R.S., Lewis, R.A., Mattocks, P.W., Darden, T.R., Smith, J.P. (1977) The circadian component in the photoperiodic mechanism of the house sparrow, Passer domesticus. Physiol. Zoo. 50: 247268.

    Google Scholar 

  • Follett, B.K., Mattocks, P.W., Farner, D.S. (1974) Circadian function in the photoperiodic induction of gonadotrophin secretion in the white-crowned sparrow. Proc. Natl. Acad. Sci. USA 71: 1666–1669.

    Article  PubMed  CAS  Google Scholar 

  • Follett, B.K., Kumar, V., Juss, T.S. (1992) Circadian nature of the photoperiodic clock in Japanese quail. J. Comp. Physiol. A 171: 533–540.

    Article  PubMed  CAS  Google Scholar 

  • Follett, B.K., King, V.M., Meddle, S.L. (1998) Rhythms and photoperiodism in birds. In: Lumsden, P.J., Millar, A.J. (eds.) Biological Rhythms and photoperiodism in plants. BIOS Scientific Publishers Ltd., Oxford, pp. 231–242.

    Google Scholar 

  • Foster, R.G., Follett, B.K. (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 

  • Goldsmith, A.R., Nicholls, T.J. (1984) Thyroidectomy prevents the development of photorefractoriness and the associated rise in plasma prolactin in starlings. Gen. Comp. Endocrinol. 54: 256–263.

    Article  PubMed  CAS  Google Scholar 

  • Gwinner, E., Schwabl-Benzinger, I., Schwabl, H., Dittami, J. (1993) Twenty-four hour melatonin profiles in a nocturnally migrating bird during and between migratory seasons. Gen. Comp. Endocrinol. 90: 119–124.

    Article  PubMed  CAS  Google Scholar 

  • Gwinner, E., Hau, M., Heigl, S. (1997) Melatonin: generation and modulation of avian circadian rhythms. Brain Res. Bull. 44: 439–444.

    Article  CAS  Google Scholar 

  • Hastings, M.H., Maywood, E.S., Ebling, F.J.P. (1995) The role of the circadian system in photoperiodic time measurement in mammals. In: Fraschini, E, Reiter, R.J. and Stankov, B. (eds.) The Pineal Gland and its Hormones. Plenum Press, New York, pp. 95–105.

    Chapter  Google Scholar 

  • Hamner, W.M. (1963) Diurnal rhythm and photoperiodism in testicular recrudescence of the house finch. Science 142: 1294–1295.

    Article  PubMed  CAS  Google Scholar 

  • Hamner, W.M., Enright, J.T. (1967) Relationships between photoperiodism and circadian rhythms of activity in the house finch. J. Exp. Biol. 46: 211–227.

    Google Scholar 

  • Hau, M., Wikelski, M., Wingfield, J.C. (1998) A neotropical forest bird can measure the slight changes in tropical photoperiod. Proc. R. Soc. Lond. B 265: 89-95.

    Google Scholar 

  • Jacobs, L.F. (1996) Sexual selection and the brain. TREE 11: 82–86.

    PubMed  CAS  Google Scholar 

  • Juss, T.S. Meddle, S.L. Servant, R.S. King, V.M. (1993) Melatonin and photoperiodic time measurement in Japanese quail (Coturnix coturnix japonica). Proc. R. Soc. London B 254: 21-28.

    Google Scholar 

  • Juss, T.S., King, V.M., Kumar, V., Follett, B.K. (1995) Does an unusual entrainment of the circadian system under T36h photocycles reduce the critical day length for photoperiodic induction on Japanese quail ? J. Biol. Rhythms 10: 16–31.

    Article  Google Scholar 

  • King, V.M., Follett, B.K. (1997) c-fos expression in the putative avian suprachiasmatic nucleus. J. Comp. Physiol. A 180: 541–551.

    Google Scholar 

  • King, V.M., Bentley, G.E., Follett, B.K. (1997) A direct comparison of photoperiodic time measurement and the circadian system in European starlings and Japanese quail. J. Biol. Rhythms 12: 421–442.

    Google Scholar 

  • Kumar, V., Follett, B.K. (1993) The circadian nature of melatonin secretion in Japanese quail (Coturnix coturnix japonica). J. Pineal Res. 14: 192–200.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, V., Tewary, P.D. (1982) Photoperiodic regulation of gonadal recrudescence in common Indian rosefinch: Dependence on circadian rhythm. J. Exp. Zool. 223: 37–40.

    Article  Google Scholar 

  • Kumar, B.S., Kumar, V. (1993) Photoperiodic control of annual reproductive cycle in subtropical brahminy myna, Sturnus pagodarum. Gen. Comp. Endocr. 89: 149–160.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, V., Kumar, B.S. (1995) Entrainment of circadian system under variable photocycles (T- photocycles) alters the critical daylength for photoperiodic induction in blackheaded buntings. J. Exp. Zool. 273: 297–302.

    Article  Google Scholar 

  • Kumar, V., Goguen, D., Guido, M.E., Rusak, B. (1997) Melatonin does not influence the expression of c-fos in the suprachiasmatic nucleus of rats and hamster. Mol. Brain Res. 52: 242–248.

    Google Scholar 

  • Kumar, V., Jain, N., Follett, B.K. (1996) The photoperiodic clock in blackheaded buntings (Emberiza melanocephala) is mediated by a self-sustaining circadian system. J. Comp. Physiol. A 179: 59–64.

    Article  PubMed  CAS  Google Scholar 

  • Maywood, E.S., Lindsay, J.O., Karp, J., Powers, J.B., Williams, L.M., Titchener, L., Ebling, F.J.P., Herbert, J., Hastings, M.H. (1991) Occlusion of the melatonin-free interval blocks the short day gonadal response of the male Syrian hamster to programmed melatonin infusions of necessary duration and amplitude. J. Neuroendocrinol. 3: 331–337.

    Article  PubMed  CAS  Google Scholar 

  • Meddle, S.L., Follett, B.K. (1995) Photoperiodic activation of Fos-like immunoreactive protein in neurones within the tuberal hypothalamus of Japanese quail. J. Comp. Physiol. A 176: 79–89.

    Article  PubMed  CAS  Google Scholar 

  • Meddle, S.L., Follett, B.K. (1997) Photoperiodic driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J. Neurosci. 17: 8909–8918.

    PubMed  CAS  Google Scholar 

  • Meddle, S.L., Maney, D.L., Wingfield, J.C. (1999) Effects of N-methyl-D-aspartate on luteinizing hormone release and Fos-like immunreactivity in the male White-crowned sparrow (Zonotrichia leucophrys gambellii). Endocrinol. 140: 5922–5928.

    Google Scholar 

  • Menaker, M., Keats, H. (1968) Extraretinal light perception in the sparrow II. Photoperiodic stimulation of testis growth. Proc. Natl. Acad. Sci. USA 60: 146–151.

    Article  PubMed  CAS  Google Scholar 

  • Messager, S., Ross, A.W., Barrett, P., Morgan, P.J. (1999) Decoding photoperiodic time through Perl and ICER gene amplitude. Proc. Natl. Acad. Sci. USA 96: 9938–9943.

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto, K., Hasegawa, Y., Nomura, M., Igarashi, M., Kanagawa, K., Matsuo, H. (1984) Identification of the second gonadotropin-releasing hormone in the chicken hypothalamus: evidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species. Proc. Natl. Acad. Sci. USA 81: 3874–3878.

    Article  PubMed  CAS  Google Scholar 

  • Morgan, J.I., Curran, T. (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Ann. Rev. Neurosci. 14: 421–451.

    Google Scholar 

  • Nanda, K.K., Hamner, K.C. (1958) Studies on the nature of the endogenous rhythm affecting photoperiodic response of Biloxi soybean. Botanical Gazette (Chicago) 120: 121–126.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nottebohm, F., Nottebohm, M.E., Crane, L.A., Wingfield, J.C. (1987) Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behay. Neural Biol. 47: 197–211.

    Article  CAS  Google Scholar 

  • Oliver, J., Bayle, J.D. (1982) Brain photoreceptors for the photoinduced testicular responses in birds. Experientia 28: 1021–1029.

    Article  Google Scholar 

  • Parry, D.M., Goldsmith, A.R. (1993) Ultrastructural evidence for changes in synaptic input to the hypothalamic luteinizing hormone-releasing hormone neurons in photosensitive and photorefractory starlings. J. Neuroendocrinol. 5: 387–395.

    Article  PubMed  CAS  Google Scholar 

  • Parry, D.M., Goldsmith, A.R., Millar, R.P., Glennie, L.M. (1997) Immunocytochemical localization of GnRH precursor in the hypothalamus of European Starlings during sexual maturation and photorefractoriness. J. Neuroendocrinol. 9: 235–243.

    Article  PubMed  CAS  Google Scholar 

  • Perera, A.D., Follett, B.K. (1992) Photoperiodic induction in vitro: the dynamics of gonadotropin-releasing hormone release from hypothalamic explants of the Japanese quail. Endocrinol. 131: 2898–2908.

    Article  CAS  Google Scholar 

  • Pittendrigh, C.S. (1972) Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proc. Natl. Acad. Sci. USA 69: 2734–2737.

    Article  PubMed  CAS  Google Scholar 

  • Pittendrigh, C.S., Minis, D.H. (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am. Nat. 98: 261–294.

    Article  Google Scholar 

  • Saldanha, C.J., Deviche, P.J., Silver, R. (1994) Increased VIP and decreased GnRH expression in photorefractory dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 93: 128–136.

    Article  PubMed  CAS  Google Scholar 

  • Sicard, V., Oliver, J., Bayle, J.D. (1983) Gonadotrophic and photosensitive abilities of the lobus paraolfactorius: electrophysiological study in quail. Neuroendocrinol. 36: 81–87.

    Google Scholar 

  • Silver, R., Witkovsky, P., Horvath, P., Alones, V., Barnstable, C.J., Lehman, M.N. (1988) Coexpression of opsin and VIP-like immunoreactivity in CSF-containing neurons of the avian brain. Cell Tiss. Res. 253: 189–198.

    Google Scholar 

  • Simpson, S.M., Follett, B.K. (1981) Pineal and hypothalamic pacemakers: their role in regulating circadian rhythmicity in Japanese quail. J. Comp. Physiol. A 145: 391–398.

    Article  Google Scholar 

  • Tewary, P.D., Kumar, V. (1981) Circadian periodicity and the initiation of gonadal growth in blackheaded buntings (Emberiza melanocephala). J. Comp. Physiol. B. 144: 210–203.

    Google Scholar 

  • Turek, F.W., Wolfson, A. (1978) Lack of an effect of melatonin treatment via silastic capsules on photic-induced gonadal growth and the photorefractory condition in white-throated sparrows. Gen. Comp. Endocrinol. 34: 471–474.

    Article  PubMed  CAS  Google Scholar 

  • Vanecek, J. (1998) Cellular mechanisms of melatonin action. Physiol. Rev. 78: 687–721.

    PubMed  CAS  Google Scholar 

  • Wallman, J., Saldanha, C.J., Silver, R. (1994) A putative suprachiasmatic nucleus of birds responds to visual motion. J. Comp. Physiol. A 174: 297–304.

    Google Scholar 

  • Wilson, F.E. (1991) Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). J. Exp. Zool. 259: 117-127.

    Google Scholar 

  • Yokoyama, K., Oksche, A., Darden, T.R., Earner, D.S. (1978) The sites of encephalic photoreception in photoperiodic induction of the growth of the testes in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Cell Tiss. Res. 189: 441–467.

    CAS  Google Scholar 

  • Zivkovic, B.D., Underwood, G., Steele, C.T., Edmonds, K. (1999) Formal properties of the circadian and photoperiodic systems of Japanese quail: phase response curve and effects of T-cycles. J. Biol. Rhythms 14: 378–390.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Meddle, S.L., Bentley, G.E., King, V.M. (2002). Photoperiodism in Birds and Mammals. In: Kumar, V. (eds) Biological Rhythms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-06085-8_16

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-06085-8_16

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-06087-2

  • Online ISBN: 978-3-662-06085-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics