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November 10, 2016
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Abstract

Birds time their activities in synchronization with daily and seasonal periodicities in the environment, which is mainly provided by changes in day length (=photoperiod). Photoreceptor cells in an avian brain are localized in three independent neural structures, the retina of eyes, pineal gland and hypothalamus. Deep brain photoreceptors (DBPs) localised particularly in the paraventricular organ (PVO) and lateral septal area (LSO) of hypothalamus are implicated in regulation of photoperiod induced reproductive response. DBPs relay the photoperiodic information to the pars tuberalis thyroid hormone stimulating (TSH) expressing cells. The TSH mediated signalling mediates the photoperiod induced gonadotropins releasing hormone (GnRH) release from the pre optic area (POA). In addition to the GnRH, other neurohormones including the neuropeptides Y (NPY), vasoactive intestinal peptide (VIP), and the neurosteroids, especially the brain derived testosterone contribute to regulation of the overt reproductive response and behaviour in seasonal breeding avian species. Here, we briefly review limited evidence on the roles of photoreceptors, and the local hormone variations of the hypothalamus in the regulation of seasonal physiology, particularly in the long-day breeding species.

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avian breeding photperiodic

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Mishra, I. . (2017). Photoperiodic regulation of reproduction in birds. Environment Conservation Journal, 18(1&2), 1–8. https://doi.org/10.36953/ECJ.2017.181201
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References

  1. Ball, G.F., 1993. The neural integration of environmental information by seasonally breeding birds. Am. Zool. 33, 185–199.
  2. Ball, G.F., Balthazart, J., 2002. Neuroendocrine mechanisms regulating reproductive cycles and reproductive behaviour in birds. In Hormones, Brain and Behavior. Vol. 2. (Pfaff, D.W., ed.). Academic Press; San Diego, CA, pp. 649-798.
  3. Benoit, J., 1935. Le role des yeux dans l’action stimulante de la lumiere sure le developpement testiulaire chez le canard. CR Soc. Biol. (Paris) 118, 669–671.
  4. Bentley, G.E., Perfito, N., Ukena, K., Tsutsui, K., Wingfield, J.C., 2003. Gonadotropininhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone. J. Neuroendocrinol. 15, 794–802.
  5. Brandstäetter, R., Kumar, V., Abraham, U., Gwinner, E., 2000. 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, 12324-12328.
  6. Canoine, V., Fusani, L., Schlinger, B., Hau, M., 2007. Low Sex Steroids, High Steroid Receptors: Increasing the Sensitivity of the Nonreproductive Brain. J. Neurobiol. 67, 57-67.
  7. Cassone, V.M., Menaker, M., 1984. Is the avian circadian system a neuroendocrine loop? J. Exp. Zool. 232, 539–549.
  8. Cassone, V.M., Yoshimura, T., 2015. Circannual cycles and photoperiodism, in: Scanes, C.G. (Eds.), Sturkie’s Avian Physiology. Springer-Verlag, New York, pp. 829-844.
  9. Chandola, A., Pavnaskar, J., Thapliyal, J.P., 1975. Scoto/photoperiodic responses of a subtropical finch (Spotted munia) in relation to seasonal breeding cycle. Biol. Rhythm Res. 6, 189-202.
  10. Chowdhury, V.S., Yamamoto, K., Ubuka, T., Bentley, G.E., Hattori, A., Tsutsui, K., 2010. Melatonin stimulates the release of gonadotropin-inhibitory hormone by the avian hypothalamus. Endocrinology 151, 271–280.
  11. Ciccone, N.A., Dunn, I.C., Boswell, T., Tsutsui, K., Ubuka, T., Ukena, K., Sharp, P.J., 2004. Gonadotropin-inhibitory hormone depresses gonadotropin and follicle stimulating hormone subunit expression in the pituitary of the domestic chicken. J. Neuroendocrinol. 16, 999–1006.
  12. Contijoch, A.M., Malamed, S., McDonald, J.F., Advis, J.P., 1993. Neuropeptide Y regulation of LHRH release in the median eminence: immunocytochemical and physiological evidence in hens. Neuroendocrinol. 57, 135-145.
  13. Dawson, A., 2015. Annual gonadal cycles in birds: modelling the effects of photoperiod on seasonal changes in GnRH-1 secretion. Front Neuroendocrinol. 37, 52-64.
  14. El Halawani, M.E., Pitts, G.R., Sun, S., Silsby, J.L., Sivanandan, V., 1996. Active immunization against vasoactive intestinal peptide prevents photo-induced prolactin secretion in turkeys. Gen. Comp. Endocrinol. 104, 76-83.
  15. El Halawani, M.E., Silsby, J.L., Rozenboim, I., 1995. Increased egg production by active immunization against vasoactive intestinal peptide in the turkey (Meleagris gallopavo). Biol. Reprod. 52, 179-183.
  16. El Halawani, M.E., Youngren, O.M., Pitts, G.R., 1997. Vasoactive intestinal peptide as the avian prolactin releasing factor, in Perspectives in Avian Endocrinology. (R. Etches and S. Harvey, ed.) The Society of Endocrinology, Bristol, United Kingdom. pp. 403-416.
  17. Follett, B.K., 1984. Reproduction in birds. In Marshall's Physiology of Reproduction, 4th edn. Vol. 1, (Lamming, G.E., ed). Churchill Livingstone, London, pp. 283-350.
  18. Foster, R.G., Plowman, G., Goldsmith, A.R., Follett, B.K., 1987. Immunocytochemical demonstration of marked changes in the luteinizing hormone-releasing hormone system of photosensitive and photorefractory European starlings. J. Endocrinol. 115, 211-220.
  19. Fraley, G.S., Kuenzel, W.J., 1993. Precocious puberty in chicks (Gallus domesticus) induced by central injection of neuropeptide Y. Life Sci. 52, 1649–1656.
  20. Frisch, K.V., 1911. Beitrage zur physiologie der pigmentzellen in der fischhaut. Pfluger’s Arch. Gesamte Phys. Menschen Tiere 138, 319–387.
  21. Goodson, J.L., Saldanha, C.J., Hahn, T.P., Soma, K.K., 2005. Recent advances in behavioural neuroendocrinology: insights from studies on birds. Horm. Behav. 48, 461-473.
  22. Gwinner, E., Brandstätter, R., 2001. Complex bird clocks. Phil. Trans. R. Soc. Lond. B: Biol. Sci. 356, 1801–1810.
  23. Gwinner, E., Hau, H., Heigl, S., 1997. Melatonin: generation and modification of avian circadian rhythms. Brain Res. Bull. 44, 439–444.
  24. Gwinner, E., Turek, F.W., Smith, S.D., 1971. Extraocular light perception in photoperiodic responses of the white-crowned sparrow (Zonotrichia leucophrys) and of the golden-crowned sparrow (Z. atricapilla). Z. Vergl. Physiol. 75, 323–331.
  25. Hahn, T.P., Ball, G.F., 1995. Changes in brain GnRH associated with photorefractoriness in house sparrows. Gen. Comp. Endocrinol. 99, 349-363.
  26. Halford, S., Pires, S.S., Turton, M., Zheng, L., Gonza´lez-Mene´ndez, I., Davies, W.L., Peirson, S.N., Garci´a-Ferna´ ndez, J.M., Hankins, M.W., Foster, R.G., 2009. VA opsin-based photoreceptors in the hypothalamus of birds. Curr. Biol. 19, 1396– 1402.
  27. Harrison, P.C., 1972. Extraretinal photocontrol of reproductive responses of Leghorn hens to photoperiods of different length and spectrum. Poultry Sci. 51, 2060– 2064.
  28. Harrison, P.C., Becker, W.C., 1969. Extraretinal photocontrol of oviposition in pinealectomized domestic fowl. Proc. Soc. Exp. Bid. (NY) 132, 161–164.
  29. Hau, M., Wikelski, M., Soma K.K., Wingfield, J.C., 2000. Testosterone and year-round territorial aggression in a Tropical Bird. Gen. Comp. Endocrinol. 117, 20-33.
  30. Klingerman, C.M., Williams, W.P. 3rd, Simberlund, J., Brahme, N., Prasad, A., Schneider, J.E., Kriegsfeld, L.J., 2011. Food restriction-induced changes in gonadotropin-inhibiting hormone cells are associated with changes in sexual motivation and food hoarding, but not sexual performance and food intake. Front. Endocrinol. 2, 101.
  31. Kuenzel, W.J., 2000. Central nervous system regulation of gonadal development in the avian male. Poult. Sci. 79, 1669-1688.
  32. Kumar, V., 1997. Photoperiodism in higher vertebrates: An adaptive strategy in temporal Environment . Indian J Exp Biol. 427-437.
  33. Kumar, V., Follett, B.K., 1993. The circadian nature of melatonin secretion in Japanese quail (Coturnix coturnix japonica). J. Pineal Res. 14, 192-200.
  34. Kumar, V., Rani, S., Malik, S., Trivedi, A.K., Schwabl, I., Helm, B., Gwinner, E., 2007. Daytime light intensity affects seasonal timing via changes in the nocturnal melatonin levels. Naturwissenchaften (Germany) 94, 693-696.
  35. Kumar, V., Singh, B.P., 2006. The timekeeping system in birds. Proc. Indian Natl. Sci. Acad. B71, 259–273.
  36. Kumar, V., Wingfield, J.C., Dawson, A., Ramenofsky, M., Rani, S., Bartell, P., 2010. Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol. Biochem. Zool. 83, 827-835.
  37. Majumdar, G., Yadav, G., Rani, S., Kumar, V., 2014. A photoperiodic molecular response in migratory redheaded bunting exposed to a single long day. Gen. Comp. Endocrinol. 204, 104-13.
  38. Maney, D.L., Richardson, R.D., Wingfield, J.C., 1997. Central administration of chicken gonadotropin-releasing hormone-II enhances courtship behaviour in a female sparrow. Horm. Behav. 32, 11–18.
  39. McGuire, N.L., Bentley, G.E., 2010. A functional neuropeptide system in vertebrate gonads: gonadotropin-inhibitory hormone and its receptor in testes of field caught house sparrow (Passer domesticus). Gen. Comp. Endocrinol. 166, 565– 572.
  40. Meddle, S.L., Bush, S., Sharp, P.J., Millar, R.P., Wingfield, J.C., 2006. Hypothalamic pro-GnRH-GAP, GnRH-I and GnRH-II during the onset of photorefractoriness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). J. Neuroendocrinol. 18, 217-226.
  41. Menaker, M., 1968. Extraretinal light perception in the sparrow. I. Entrainment of the biological clock. Proc. Natl. Acad. Sci. U.S.A. 59, 414–421.
  42. Menaker, M., Keatts, H., 1968. Extraretinal light perception in the sparrow. II. Photoperiodic stimulation of testis growth. Proc. Natl. Acad. Sci. U.S.A. 60, 146–151.
  43. Nakane, Y., Ikegami, K., Ono, H., Yamamoto, N., Yoshida, S., Hirunagi, K., Ebihara, S., Kubo, Y., Yoshimura, T., 2010. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc. Natl. Acad. Sci. U.S.A. 107, 15264– 15268.
  44. Nakane, Y., Yoshimura, T., 2014. Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates. Front. Neurosci. 8, 1-7.
  45. Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., Yasuo, S., Katou, Y., Kageyama, S., Uno, Y., Kasukawa, T., Iigo, M., Sharp, P.J., Iwasaw, A., Suzuki, Y., Sugano, S., Niimi, T., Mizutani, M., Namikawa, T., Ebihara, S., Ueda, H.R., Yoshimura, T., 2008. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452, 317-322.
  46. Oishi, T., Konishi, T., Kato, M., 1966. Investigations on photoreceptor mechanism to control gonadal development in Japanese quail. Environ. Control. Biol. 3, 87–90.
  47. Ookawa, T., 1970a. Effects of bilateral optic enucleation on body growth and gonad in young male chicks. Poultry Sci. 49, 333–334.
  48. Ookawa, T., 1970b. Some observations on behavior and reproductive organs in blinded chickens. Poultry Sci. 49, 1531–1535.
  49. Opel, H., Proudman, J.A., 1989. Plasma prolactin levels in incubating turkey hens during pipping of the eggs and after introduction of poults into the nest. Biol. Reprod. 40, 981-987.
  50. Perfito, N., Zann, R., Ubuka, T., Bentley, G., Hau, M., 2011. Potential roles for GNIH and GNRH-II in reproductive axis regulation of an opportunistically breeding songbird. Gen. Comp. Endocrinol. 173, 20-26.
  51. Ramenofsky, M., 2011. Hormones in migration and reproductive cycles of birds, in Hormones and Reproduction of Vertebrates, vol. 4. (Norris, D., Lopez, K., eds.). Elsevier; Amsterdam, pp. 205-236.
  52. Rani, S., Singh S., Kumar V., 2007. Photoperiodism, pineal clock and seasonal reproduction in the Indian weaver bird (Ploceus philippinus). J. Ornithol. 148, 601-610.
  53. Reinert, B.D., Wilson, F.E., 1996. The thyroid and the hypothalamus-pituitary-ovarian axis in American tree sparrows. Gen. Comp. Endocrinol. 103, 60-70.
  54. Richardson, R.D., Boswell, T., Raffety, B.D., Seeley, R.J., Wingfield, J.C., Woods, S.C., 1995. NPY increases food intake in white-crowned sparrows: effect in short and long photoperiods. Am. J. Physiol. 268, R1418-R1422.
  55. Sharp, P.J., Dawson, A., Lea, R.W., 1998. Control of luteinizing hormone and prolactin secretion in birds. Comp. Biochem. Physiol. C Pz
  56. Silver, R., Witkovsky, P., Horvath, P., Alones, V., Barnstable, C.J., Lehman, M.N., 1988. Coexpression of opsin- and VIP-like immunoreactivity in CSF-contacting neurones of the avian brain. Cell Tissue Res. 253, 189-198.
  57. Soma, K.K., Tramontin, A.D., Wingfield, J.C., 2000. Oestrogen regulates male aggression in the non-breeding season. Proc. Biol. Sci. 267, 1089-1096.
  58. Stevenson, T.J., MacDougall-Shackleton, S.A., 2005. Season- and age-related variation in neural cGnRH-I and cGnRH-II immunoreactivity in house sparrows (Passer domesticus). Gen. Comp. Endocrinol. 143, 33-39.
  59. Surbhi, Rastogi, A., Malik, S., Rani, S., Kumar, V., 2016. Changes in brain peptides associated with reproduction and energy homeostasis in photosensitive and photorefractory migratory redheaded buntings. Gen. Comp. Endocrinol. 230- 231, 67-75
  60. Surbhi, Rastogi, A., Rani, S., Kumar, V., 2015. Seasonal plasticity in the peptide neuronal systems: potential roles of gonadotrophin-releasing hormone, gonadotrophin-inhibiting hormone, neuropeptide Y and vasoactive intestinal peptide in the regulation of the reproductive axis in subtropical Indian weaver birds. J. Neuroendocrinol. 27, 357-369.
  61. Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., Ishii, S., Sharp, P.J., 2000. A novel avian hypothalamic peptide inhibiting gonadotropins release. Biochem. Biophys. Res. Commun. 275, 661–667.
  62. Ubuka, T., Kim, S., Huang, Y.C., Reid, J., Jiang, J., Osugi, T., et al., 2008. Gonadotropin inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and-II neurons in European starling brain. Endocrinology 149, 268–278.
  63. Ubuka, T., Ukena, K., Sharp, P.J., Bentley, G.E., Tsutsui, K., 2006. Gonadotropininhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology 147, 1187–1194.
  64. Wald, G., 1968. Molecular basis of visual excitation. Science 162, 230–239.
  65. Wingfield, J.C., Farner, D.S., 1993. Endocrinology of reproduction in wild species. In: Farner, D.S., King, J.R., Parkes, K.C. (Eds.), Avian Biology IX. Academic Press, New York, pp. 163–327.
  66. Yamamura, T., Hirunagi, K., Ebihara, S., Yoshimura, T., 2004. Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology 145, 4264–4267.
  67. Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K., Ebihara, S., 2003. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426, 178–181.
  68. Youngren, O., Chaiseha, Y., Phillips, R., El Halawani, M., 1996. Vasoactive intestinal peptide concentrations in turkey hypophysial portal blood differ across the reproductive cycle. Gen. Comp. Endocrinol. 103, 323-330.
  69. Zadworny, D., Shimada, K., Ishida, H., Sumi, C., Sato, K., 1988. Changes in plasma levels of prolactin and estradiol, nutrient intake, and time spent nesting during the incubation phase of broodiness in the Chabo hen (Japanese bantam). Gen. Comp. Endocrinol. 71, 406-412.