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Journal of Ornithology

, Volume 146, Issue 4, pp 355–364 | Cite as

The pineal clock affects behavioral circadian rhythms but not photoperiodic induction in the Indian weaver bird (Ploceus philippinus)

  • Sangeeta Rani
  • Sudhi Singh
  • Vinod KumarEmail author
Original Article

Abstract

We investigated whether pineal is part of the circadian clock system which regulates circadian rhythms of activity and photosensitivity in the Indian weaver bird (Ploceus philippinus). Two experiments were performed. The first experiment examined the induction of testicular growth, and androgen-dependent beak pigmentation and luteinizing hormone (LH)-specific plumage coloration in pinealectomised (pinx) and sham-operated (sham) birds exposed to short day (8 h light: 16 h darkness, 8L:16D) and long day (16L:8D) for 9 months in the late breeding and early regressive phase (October), or the late regressive and preparatory phase (January) of the annual testicular cycle. As expected, short days were non-stimulatory, and long days stimulated testicular growth, beak pigmentation and plumage coloration. There was no difference in the response between pinx and sham birds subjected to short or long days in October, but the response was enhanced in pinx birds that were subjected to long day in January. In the second experiment circadian behavioral rhythms were studied (activity pattern in singly housed birds) in weaver birds first exposed at two different phases of the annual testicular cycle to a stimulatory photoperiod (12L:12D in preparatory phase or 13L:11D in early breeding phase) and then released into dim continuous light (LLdim). All birds showed synchronization to the light period before and after the pinealectomy; there was no difference in the response between pinx and sham birds. When released into LLdim, sham birds exhibited circadian rhythmicity continuously, whereas pinx birds lost circadian rhythmicity after some cycles. Considered together, these results suggest that circadian clock residing within the pineal gland regulates the circadian rhythm in activity, but not the circadian rhythm involved in photoperiodic induction of the Indian weaver bird.

Keywords

Circadian rhythm Melatonin Pineal Pinealectomy Photoperiod Ploceus philippinus 

Notes

Acknowledgments

The experiments included in this paper conform to Indian laws, and were done using the facility exclusively generated from the SERC research grant to VK by the Department of Science and Technology, Government of India.

References

  1. Ali S, Ripley SD (1974) Handbook of birds of India and Pakistan, vol 10, 2nd edn. Oxford University Press, Delhi, Bombay, London, New YorkGoogle Scholar
  2. Bailey MJ, Beremand PD, Hammer R, Bell-Pedersen D, Thomas TL, Cassone VM (2003) Transcriptional profiling of the chicken pineal gland, a photoreceptive circadian oscillator and pacemaker. Mol Endocrinol 17:2084–2095CrossRefPubMedGoogle Scholar
  3. Balasubramanian KS, Saxena RN (1973) Effect of pinealectomy and photoperiodism in the reproduction of the Indian weaver birds, Ploceus philippinus. J Exp Zool 185:333–348CrossRefPubMedGoogle Scholar
  4. Binkley S, Kluth E, Menaker M (1971) Pineal function in sparrows: circadian rhythm and body temperature. Science 174:311–314PubMedCrossRefGoogle Scholar
  5. Brandstäetter R, Kumar V, Abraham U, Gwinner E (2000a) Photoperiodic information acquired and stored in vivo is retained in vitro by a circadian oscillator, the avian pineal gland. Proc Natl Acad Sci USA 97:12324–12328CrossRefGoogle Scholar
  6. Brandstäetter R, Kumar V, Van’t Hof TJ, Gwinner E (2000b) Seasonal variations of in vivo and in vitro melatonin production in a passeriform bird, the house sparrow (Passer domesticus). J Pineal Res 31:120–126CrossRefGoogle Scholar
  7. Cassone VM (1992) The pineal gland influences rat circadian activity rhythm in constant light. J Biol Rhythms 7:27–40PubMedCrossRefGoogle Scholar
  8. Cassone VM, Warren WS, Brooks DS, Lu J (1993) Melatonin, the pineal gland, and circadian rhythms. J Biol Rhythms 8(Suppl):573–581Google Scholar
  9. Chandola-Saklani A, Singh R, Thapliyal JP (1976) Evidence for a circadian oscillation in the gonadal response of the tropical weaver bird (Ploceus philippinus) to programmed photoperiods. Chronobiologia 3:219–227PubMedGoogle Scholar
  10. Chandola-Saklani A, Bhatt D, Lakhera P (1988) Effect of pinealectomy on free-running reproductive cycle of tropical spotted munia. J Comp Physiol A 164:117–121CrossRefGoogle Scholar
  11. Elliott JA, Stetson MH, Menaker M (1972) Regulation of testis function in golden hamsters: a circadian clock measures photoperiodic time. Science 178:771–773PubMedCrossRefGoogle Scholar
  12. Gaston S, Menaker M (1968) Pineal function: the biological clock in the sparrow? Science 160:1125–1127PubMedCrossRefGoogle Scholar
  13. Goldman BD (2001) Mammalian photoperiodic systems: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythm 16:283–301CrossRefGoogle Scholar
  14. Gwinner E, Dittami J (1980) Pinealectomy affects the circannual testicular rhythm in European starlings (Sturnus vulgaris). J Comp Physiol A 136:345–348CrossRefGoogle Scholar
  15. Gwinner E, Hau M (2000) The pineal gland, circadian rhythms and photoperiodism. In: Whittow GC (ed) Sturkie’s avian physiology. Academic Press, New York, pp 557–568Google Scholar
  16. Gwinner E, Hau M, Heigl S (1997) Melatonin: generation and modulation of avian circadian rhythms. Brain Res Bull 44:439–444CrossRefPubMedGoogle Scholar
  17. Haldar C (1986) Methods of pinealectomy in vertebrates. Indian J Exp Biol 24:319–322PubMedGoogle Scholar
  18. Haldar C, Ghosh M (1990) Annual pineal and testicular cycle in the Indian jungle bush quail, Perdicula asiatica, with reference to the effect of pinealectomy. Gen Comp Endocrinol 77:150–157CrossRefPubMedGoogle Scholar
  19. Hamner WM, Enright JT (1967) Relationships between photoperiodism and circadian rhythms of activity in the house finch. J Exp Biol 46:43–61PubMedGoogle Scholar
  20. Heigl S, Gwinner E (1994) Periodic melatonin in the drinking water synchronizes circadian rhythms in sparrows. Naturwissenschaften 81:83–85CrossRefGoogle Scholar
  21. Juss TS, King VM, Kumar V, Follett BK (1995) Does an unusual entrainment of the circadian system under T36 h photocycles reduce the critical day length for periodic induction in Japanese quail. J Biol Rhythms 10:17–32PubMedCrossRefGoogle Scholar
  22. Kasahara T, Okano T, Haga T, Fukada Y (2002) Opsin-G11-mediated signaling pathway for photic entrainment of the chicken pineal circadian clock. J Neurosci 22:7321–7325PubMedGoogle Scholar
  23. Kumar V (1996) Effect of melatonin in blocking the response to a skeleton photoperiod in the blackheaded bunting. Physiol Behav 59:617–620CrossRefPubMedGoogle Scholar
  24. Kumar V (1997) Photoperiodism in higher vertebrates—An adaptive strategy in temporal environment. Indian J Exp Biol 35:427–437PubMedGoogle Scholar
  25. Kumar V (2001) Melatonin and circadian rhythmicity in birds. In: Dawson A, Chaturvedi CM (eds) Avian endocrinology. Narosa Publishing House, New Delhi, pp 93–112Google Scholar
  26. Kumar V, Tewary PD (1984) Circadian rhythmicity and the termination of refractoriness in the blackheaded bunting (Emberiza melanocephala). Condor 86:27–29CrossRefGoogle Scholar
  27. Kumar V, Follett BK (1993a) The nature of photoperiodic clock in vertebrates. Proc Zool Soc Calcutta; JBS Haldane Com-. memoration Vol. pp 217–227Google Scholar
  28. Kumar V, Follett BK (1993b) The circadian nature of melatonin secretion in Japanese quail (Coturnix coturnix japonica). J Pineal Res 14:192–200PubMedCrossRefGoogle Scholar
  29. Kumar V, Juss TS, Follett BK (1993) Melatonin secretion in quail provides a seasonal calendar but not one used for photoperiodic time measurement. In: Touitou Y, Arendt J, Pevet P (eds) Melatonin and the pineal gland from basic sciences to clinical applications. Elsevier Science Publications, Amsterdam, pp 163–168Google Scholar
  30. Kumar V, Jain N, Follett BK (1996a) The photoperiodic clock in blackheaded buntings (Emberiza melanocephala) is mediated by self-sustaining circadian system. J Comp Physiol A 179:59–64CrossRefPubMedGoogle Scholar
  31. Kumar V, Kumar BS, Jain N (1996b) Effect of late afternoon administration of melatonin on the photoperiod-induced responses in buntings. Indian J Exp Biol 34:20–225Google Scholar
  32. Kumar V, Singh S, Misra M, Malik S (2001) Effects of duration and time of food availability on photoperiodic responses in the migratory male blackheaded bunting (Emberiza melanocephala). J Exp Biol 204:2843–2848PubMedGoogle Scholar
  33. Kumar V, Singh S, Misra M, Malik S, Rani S (2002) Role of melatonin in photoperiodic time measurement in the migratory redheaded bunting (Emberiza bruniceps) and the non-migratory Indian weaver bird (Ploceus philippinus). J Exp Zool 292:277–286CrossRefPubMedGoogle Scholar
  34. Kumar V, Singh BP, Rani S (2004) The bird clock: a complex multi-oscillatory and highly diversified system. Biol Rhythm Res 35:121–144CrossRefGoogle Scholar
  35. Maitra SK, Dey M (1992) Testicular responsiveness to exogenous melatonin during different phases of the annual testicular cycle in roseringed parakeet, Psittacula krameri. Eur Arch Biol 103:157–164Google Scholar
  36. Malik S, Rani S, Kumar V (2004) Wavelength dependency of light-induced effects on photoperiodic clock in the migratory blackheaded bunting (Emberiza melanocephala). Chronobiol Int 21:367–384CrossRefPubMedGoogle Scholar
  37. Okano T, Yoshizawa T, Fukada Y (1994) Pinopsin is a chicken pineal photoreceptive molecule. Nature 372:94–97CrossRefPubMedGoogle Scholar
  38. Saldanha CJ, Siverman AJ, Silver R (2001) Direct innervation of GnRH neurons by encephalic photoreceptors in birds. J Biol Rhythms 16:39–49PubMedCrossRefGoogle Scholar
  39. Saxena RN (1964) Sexual cycle and secondary sex characters of Indian weaver bird (Ploceus philippinus). PhD Thesis, Banaras Hindu University, Varanasi, IndiaGoogle Scholar
  40. Saxena RN, Thapliyal JP (1962) Male hormone and bill pigmentation in baya, Ploceus philippinus (Linn.). Sec Cong Zool (Abstr 29)Google Scholar
  41. Sumova A, Sladek M, Jac M, Illnerova H (2002) The circadian rhythm of Per1 gene product in the rat suprachiasmatic nucleus and its modulation by seasonal changes in day length. Brain Res 947:260–270CrossRefPubMedGoogle Scholar
  42. Takahashi JS, Menaker M (1982) Role of suprachiasmatic nuclei in the circadian system of the house sparrow, Passer domesticus. J Neurosci 2:815–828PubMedGoogle Scholar
  43. Thapliyal JP, Saxena RN (1961) Plumage control in Indian weaver bird (Ploceus philippinus). Naturwissenschaften 24:741–742CrossRefGoogle Scholar
  44. Thapliyal JP, Tewary PD (1964) Effect of light on the pituitary, gonad and plumage pigmentation in the avadavat, Estrilda amandava, and Baya weaver, Ploceus philippinus. Proc Zool Soc Lond 142:67–71Google Scholar
  45. Trivedi AK (2004) Seasonal responses of house sparrow (Passer domesticus) Linnaeus at 27°N. PhD Thesis, University of Lucknow, Lucknow, IndiaGoogle Scholar
  46. Underwood H (1994) The circadian rhythm of thermoregulation in Japanese quail. I. Role of the eyes and pineal. J Comp Physiol A 175:639–653CrossRefPubMedGoogle Scholar
  47. Wilson FE (1991) Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows. J Exp Zool 259:117–127CrossRefGoogle Scholar
  48. Zimmerman NH, Menaker M (1979) The pineal gland: a pacemaker within the circadian system of the house sparrow. Proc Natl Acad Sci USA 76:999–1003PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2005

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of LucknowLucknowIndia

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