Advertisement

Fish Physiology and Biochemistry

, Volume 2, Issue 1–4, pp 35–51 | Cite as

Photoperiodic mechanisms and rhythms of reproduction in the female rainbow trout

  • James Duston
  • Niall Bromage
Article

Abstract

The present work investigates the importance of circadian and circannual rhythms in the photoperiodic control of reproduction in the rainbow trout. Maintenance of groups of 20–30 female trout under continuous light (LL), constant long (18L:6D) or short (6L:18D) days and conditions of constant temperature (8.5–9.0°C) and feeding rates (0.5% body weight, day−1), starting in February, produced markedly different spawning periodicities during the first and subsequent years of treatment. At the end of the first year, spawning was advanced by up to 2 months in the fish under LL and 18L:6D and delayed by up to 5 months in those under 6L:18D when compared with the December spawning of control fish under ambient light. Continued exposure of the fish to the same photoperiod regimes produced cycles of spawning and peak levels of testosterone, oestradiol-17β and calcium (as an index of vitellogenin) at intervals of 150–170 days under LL and 18L:6D and 320–420 days under 6L:18D. The functional importance of these spawning cycles and their relationship to circannual rhythms and the control of reproduction is discussed.

Exposure of fish to skeleton (6L:4D:2L:12D, 6L:6D:2L:10D and 6L:8D:2L:8D) and resonance (6L:42D, 6L:48D and 6L:54D) procedures produced ranges of spawning times up to two months in advance of control fish. Results with the resonance regimes, where fish received only a half the light-dark cycles and a quarter of the total daylight hours of those on ambient light cycles show that trout do not measure daylength and time by counting daily cycles or by hour-glass mechanisms. Collectively, these data support the proposition that rhythmic processes of photosensitivity are involved in the modulation of reproductive development in the rainbow trout and that circadian and circannual rhythms cooperate in the timing and entrainment of this cycle.

Keywords

daylength trout reproduction circannual rhythms resonance skeleton photoperiod endocrine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Bailey, N.T.J. 1959. Statistical Methods in Biology. English Univ. Press, London.Google Scholar
  2. Baggerman, B. 1972. Photoperiodic responses in the stickleback and their control by a daily rhythm of photosensitivity. Gen. Comp. Endocrinol. Suppl. 3: 466–476.CrossRefGoogle Scholar
  3. Baggerman, B. 1980. Photoperiodic and endogenous control of the annual reproduction cycle in teleost fishes.In Environmental Physiology of Fishes. pp. 533–567. Edited by M. Ali. Plenum Press, New York.Google Scholar
  4. Benoit, J., Assenmacher, I. and Brard, E. 1956. Apparition et maintien de cycles sexuels non saisonniers chez le canard domestique eleve pendant plus de trois ans à l'obscurité totale. J. Physiol. (Paris). 48: 388–391.Google Scholar
  5. Berthold, P. 1974. Circannual rhythms in birds with different migratory habits.In Circannual Clocks. pp. 55–94. Edited by E.T. Pengelley. Academic Press, London.Google Scholar
  6. Berthold, P., Gwinner, E. and Klein, M. 1972. Circannuale periodik bei grasmucken II. Periodik der gonadengrose beiS. atricapilla andS. borin unter verschiedenen konstanten bedingungen. J. Ornith. 113: 407–417.CrossRefGoogle Scholar
  7. Bromage N. 1982. Fish culture and research into reproduction.In Proceedings of the Institute of Fisheries Management. pp. 165–176. Edited by M. Bulleid. Commercial Trout Farming Symp., Reading.Google Scholar
  8. Bromage, N., Whitehead, C. and Breton, B. 1982a. Relationships between serum levels of gonadotropin, oestradiol 17β and vitellogenin in the control of ovarian development in the rainbow trout. II. Effects of alterations in environmental photoperiod. Gen. Comp. Endocrinol. 47: 366–376.CrossRefPubMedGoogle Scholar
  9. Bromage, N., Whitehead, C., Elliott, J. and Matty, A. 1982b. Investigations into the importance of daylength on the photoperiodic control of reproduction in the female rainbow trout.In Reproductive Physiology of Fish. pp.233–236. Edited by C. Richter and H.Th. Goos. Pudoc Press, Wageningen.Google Scholar
  10. Bromage, N.R., Elliott, J.A., Springate, J.R.C. and Whitehead, C., 1984. The effects of constant photoperiods on the timing of spawning in the rainbow trout. Aquaculture 43: 213–223.CrossRefGoogle Scholar
  11. Bromage, N.R. and Duston, J. 1986. The control of spawning in the rainbow trout (Salmo gairdneri) using photoperiod techniques. Rept. Fres. Res. Drottn. (in press)Google Scholar
  12. Bünning, E. 1936. Die endogene tagesrhythmik alse grundlaye der photoperiodischen reaktion. Ber. Dtsch. Bot. Ges. 54: 590–607.Google Scholar
  13. Bünning, E. 1960. Circadian rhythms and the time measurement in photoperiodism. Cold Spring Harbor Symp. Quant. Biol. 25: 257–260.Google Scholar
  14. Chan, K. 1976. A photosensitive daily rhythm in the female medaka,Oryzias latipes. Can. J Zool. 54: 852–856.PubMedGoogle Scholar
  15. Cuellar, H.S. and Cuellar, O. 1977. Evidence for endogenous rhythmicity in the reproductive cycle of the parthenogenetic lizardCnemidophorous uniparens. Copeia 1977: 554–557.Google Scholar
  16. Danilevsky, A.S. Goryshin, N.I. and Tyshchenko, V.P. 1970. Biological rhythms in terrestrial anthropods. Ann. Rev. Entomol. 15: 201–244.CrossRefGoogle Scholar
  17. Elliott, J.A. 1981. Circadian rhythms, entrainment and photoperiodism in the Syrian hamster.In Biological Clocks in Seasonal Reproductive Cycles. pp. 203–217. Edited by B.K. Follett and D.E. Follett. Scientechnica, Bristol.Google Scholar
  18. Elliott, J., Bromage, N. and Springate, J. 1984. Changes in reproductive function of three strains of rainbow trout exposed to constant and seasonally-changing light cycles. Aquaculture 43: 23–34.CrossRefGoogle Scholar
  19. Eriksson, L. and Lundqvist, H. 1982. Circannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon. Aquaculture 28: 113–121.CrossRefGoogle Scholar
  20. Follett, B.K. 1981. The stimulation of luteinizing hormone and follicle-stimulating hormone secretion in quail with complete and skeleton photoperiods. Gen. Comp. Endocrinol. 45: 306–316.CrossRefPubMedGoogle Scholar
  21. Follett, B.K. 1984. Birds.In Marshall's Physiology of Reproduction. Vol. 1. Reproductive Cycles of Vertebrates. pp. 283–350. Edited by G.E. Lamming. Churchill Livingston, London.Google Scholar
  22. Goss, R.J. 1969. Photoperiodic control of antler cycles in deer. II Alterations in amplitude. J. Exp. Zool. 171: 223–234.CrossRefGoogle Scholar
  23. Gwinner, E. 1973. Circannual rhythms in birds: their interaction with circadian rhythms and environmental photoperiod. J. Reprod. Fert. Supp. 19: 51–65.Google Scholar
  24. Gwinner, E. 1981. Circannual systems.In Handbook of Behavioural Neurobiology. Vol. 4. Biological Rhythms. pp. 391–410. Edited by J. Aschoff. Plenum Press, New York.Google Scholar
  25. Hamner, W.M. 1964. Circadian control of photoperiodism in the housefinch demonstrated by interrupted-night experiments. Nature, Lond. 203: 1400–1401.Google Scholar
  26. Hamner, W.M. and Enright, J.T. 1967. Relationships between photoperiodism and circadian rhythms of activity in the house finch. J. Exp. Biol. 46: 43–61.PubMedGoogle Scholar
  27. Henderson, N.E. 1963. Influence of light and temperature on the reproductive cycle of the eastern brook trout,Salvelinus fontinalis (Mitchell). J. Fish. Res. Bd. Can. 20: 859–897.Google Scholar
  28. Herbert, J. 1981. The pineal gland and photoperiodic control of the ferret's reproductive cycle. In Biological Clocks in Seasonal Reproductive Cycles. pp. 261–276. Edited by Follett, B.K. and Follett, D.E. Scientechnica, Bristol.Google Scholar
  29. Howles, C.M., Craigon, J. and Haynes, N.B. 1982. Long-term rhythms of testicular volume and plasma prolactin concentrations in rams reared for 3 years in constant photoperiod. J. Reprod. Fertil. 65: 439–446.PubMedGoogle Scholar
  30. Lees, A.D. 1973. Photoperiodic time measurement in the aphidMegoura viciae. J. Insect Physiol. 19: 2279–2316.Google Scholar
  31. Lou, S.W., Aida, K., Manyu, I., Sakai, K., Nomura, M., Tanaka, M. and Tazaki, S. 1984. Endocrine profiles in females of a twice-annually spawning strain of trout. Aquaculture 43: 13–22.CrossRefGoogle Scholar
  32. Pengelley, E.T. and Asmundson, S.J. 1974. Circannual rhythmicity in hibernating mammals.In Circannual Clocks. pp. 95–146. Edited by E.T. Pengelley. Academic Press, London.Google Scholar
  33. Pittendrigh, C.S. 1972. Circadian surfaces and the diversity of possible roles of circadian organisation in photoperiodic induction. Proc. Nat. Acad. Sci. 69: 2734–2737.PubMedGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. Poston, H.A. and Livingstone, D.L. 1971. The effect of continuous darkness and continuous light on the functional sexual maturity of brook trout during their second reproductive cycle. Fish. Res. Bull. N.Y. 33: 25–29.Google Scholar
  36. Pyle, E.A. 1969. The effect of constant light or constant darkness on the growth and sexual maturity of brook trout. Fish. Res. Bull. N.Y. 31: 13–19.Google Scholar
  37. Robinson, J.E. & Follett, B.K. 1982. Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. Roy. Soc. Lond. Ser. B. 215: 95–116.Google Scholar
  38. Robinson, J.E., Wayne, N. and Karsch, F.J. 1985. Refractoriness to inhibitory daylengths initiates the breeding season of the Suffolk ewe. Biol. Reprod. 32: 1024–1030.CrossRefPubMedGoogle Scholar
  39. Saunders, D.S. 1981. Insect Photoperiodism.In Handbook of Behavioural Rhythms. Vol. 4. Biological Rhythms. pp. 411–447. Edited by J. Aschoff. Plenum Press, London.Google Scholar
  40. Scott, A.P., Baynes, S.M., Skarphedinsson, O. and Bye, V.J. 1984. Control of spawning time in rainbow troutSalmo gairdneri, using constant long daylengths. Aquaculture 43: 225–233.CrossRefGoogle Scholar
  41. Sundararaj, B., Vasal, S. and Halberg, F. 1973. Circannual rhythmic ovarian recrudescence in the catfish.Heteropneustes fossilis. Int. J. Chronobiol. 1: 362–363.Google Scholar
  42. Sundararaj, B. and Vasal, S. 1976. Photoperiod and temperature control in the regulation of reproduction in female catfish. J. Fish. Res. Bd. Can. 33: 959–973.Google Scholar
  43. Takashima, F. and Yamada, Y. 1984. Control of maturation in masu salmon by manipulation of photoperiod. Aquaculture 43: 243–257.CrossRefGoogle Scholar
  44. Underwood, H. 1981. Circadian clocks in lizards: Photoreception physiology and photoperiodic times measurement.In Biological Clocks in Seasonal Reproductive Cycles. pp. 203–217. Edited by B.K. Follett and D.E. Follett. Scientechnica, Bristol.Google Scholar
  45. Whitehead, C., Bromage, N., Forster, J. and Matty, A. 1978. The effects of alterations in photoperiod on ovarian development and spawning time in the rainbow trout. Ann. Biol. Anim. Bioch. Biophys. 18: 1035–1053.Google Scholar
  46. Whitehead, C. and Bromage, N. 1980. Effects of constant long and short day photoperiods on the reproductive physiology and spawning of the rainbow trout. J. Endocrinol. 87: 6–7.Google Scholar

Copyright information

© Kugler Publications bv 1986

Authors and Affiliations

  • James Duston
    • 1
  • Niall Bromage
    • 1
  1. 1.Fish Culture, Department of Molecular SciencesAston UniversityBirminghamUK

Personalised recommendations