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The entrainment and gating of the endogenous circannual rhythm of reproduction in the female rainbow trout (Salmo gairdneri)

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Summary

The endogenous circannual rhythm of maturation in the female rainbow trout and associated changes in serum oestradiol-17β and vitellogenin (as calcium) can be entrained by abrupt changes in the photoperiod. Groups of virgin fish (which naturally spawn in December) maintained under LD 18∶6 from mid-January (Year 1), and then subjected to a reduction to LD 6∶18 either on 1st March (Group A), 1st April (Group B), 1st May (Group C) or 1st June (Group D), commenced spawning on 31st July, 13th and 30th August, and the 16th September, respectively. Fish maintained on LD 18∶6 throughout the experiment (Group E) commenced spawning on 10th October. These advances in the timing of spawning can be described in the form of a phase-response curve analogous to the entrainment behaviour of circadian oscillators. It is concluded that under natural conditions the annual change in photoperiod serves to continuously entrain the circannual clock thus ensuring that maturation and spawning occur at the optimal season for the survival of the species.

In Groups A, B, C and D, respectively, 74%, 48%, 23% and 8% of the fish failed to mature in Year 1. Maintaining a sample of both maturing and non-maturing trout under constant LD 6∶18 for a further year resulted in all the fish spawning in August of Year 2, approximately one year after the spawning members of this group matured in Year 1. It is proposed that the reduction from LD 18∶6 to LD 6∶18 phase-advanced a circannual timing mechanism in all the fish which then ‘free-ran’; this advance was only overtly expressed by the earlier spawning of a certain percentage of the fish in Year 1, but in all the fish in Year 2. These results indicate that the internal timing mechanism can be dissociated from the neuroendocrine mechanisms controlling maturation and thus it can be considered as an autonomous circannual clock. The relationship between the timing of the reduction in photoperiod and the percentage of virgin fish attaining maturation can be explained by a gating model. It is hypothesized that the energetically demanding process of gonadal maturation is only allowed in virgin fish which have reached a certain threshold stage of development and when the clock is at a specific (‘gate open’) phase of the circannual cycle.

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References

  • Allison LN (1951) Delay of spawning in eastern brook trout by means of artificially prolonged light intervals. Prog Fish Cult 13:111–116

    Google Scholar 

  • Baggerman B (1980) Photoperiodic and endogenous control of the annual reproductive cycle in teleost fishes. In: Ali MA (ed) Environmental physiology of fishes. Plenum Press, New York London, pp 533–568

    Google Scholar 

  • Bailey NTJ (1959) Statistical methods in biology. English University Press, London

    Google Scholar 

  • Berthold P (1979) Über die photoperiodische Synchronisation circannualer Rhythmen bei Grasmücken. Vogelwarte 30:7–10

    Google Scholar 

  • Blake GM (1959) Control of diapause by an ‘internal clock’ inAnthrenus verbasci. Nature 183:126–127

    Google Scholar 

  • Bromage N, Whitehead C, Elliott J, Breton B, Matty A (1982a) Investigations into the importance of daylength on the photoperiodic control of reproduction in the female rainbow trout. In: Richter CJJ, Goos HJTh (eds) Reproductive physiology of fish. Pudoc Press, Wageningen, pp 233–236

    Google Scholar 

  • Bromage N, Whitehead C, Breton B (1982b) 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

    Google Scholar 

  • Bromage NR, Elliott JAK, Springate JRC, Whitehead C (1984) The effects of constant photoperiods on the timing of spawning in the rainbow trout. Aquaculture 43:213–223

    Google Scholar 

  • Combs B, Burrows R, Bige JR (1959) The effect of controlled light on the maturation of adult blueback salmon. Prog Fish Cult 21:63–69

    Google Scholar 

  • Corson BW (1955) The use of artificially controlled light to induce early spawning of brook trout. Prog Fish Cult 21:99–102

    Google Scholar 

  • Daan S (1982) Circadian rhythms in animals and plants. In: Brady J (ed) Biological timekeeping. Soc Exp Biol Seminar Series No. 14. Cambridge University Press, Cambridge, pp 11–31

    Google Scholar 

  • Duston J, Bromage N (1986) Photoperiodic mechanisms and rhythms of reproduction in the female rainbow trout. Fish Physiol Biochem 2:35–51

    Google Scholar 

  • Duston J, Bromage N (1987) Constant photoperiod regimes and the entrainment of the annual cycle of reproduction in the female rainbow trout (Salmo gairdneri). Gen Comp Endocrinol 65:373–384

    Google Scholar 

  • Farner DS (1985) Annual rhythms. Annu Rev Physiol 47:65–82

    Google Scholar 

  • Foster DL, Ryan KD (1981) Endocrine mechanisms governing transition into adulthood in female sheep. J Reprod Fertil [Suppl] 30:75

    Google Scholar 

  • Foster DL, Yellon SM, Olster DH (1985) Internal and external determinants of the timing of puberty in the female sheep. J Reprod Fertil 75:327–344

    Google Scholar 

  • Foster DL, Karsch FJ, Olster DH, Ryan KD, Yellon SM (1986) Determinants of puberty in a seasonal breeder. Recent Prog Horm Res 42:331–384

    Google Scholar 

  • Franke HD (1986) Resetting a circalunar reproduction rhythm with artificial moonlight signals: phase-response curve and ‘moon-off’ effect. J Comp Physiol A 159:569–576

    Google Scholar 

  • Goss RJ, Dinsmore CE, Grimes LN, Rosen RK (1974) Expression and suppression of the circannual antler cycle in deer. In: Pengelley ET (ed) Circannual clocks. Academic Press, New York, pp 393–422

    Google Scholar 

  • Gwinner E (1971) A comparative study of circannual rhythms in warblers. In: Menaker M (ed) Biochronometry. National Academy of Sciences, pp 405–427

  • Gwinner E (1977) Photoperiodic synchronisation of circannual rhythms in the European starling (Sturnus vulgaris). Naturwissenschaften 64:44–45

    Google Scholar 

  • Gwinner E (1981) Circannual systems. In: Aschoff J (ed) Biological rhythms (Handbook of behavioural neurobiology, vol 4). Plenum Press, New York, pp 391–410

    Google Scholar 

  • Gwinner E (1986) Circannual rhythms (Zoophysiology V18) Springer, Berlin Heidelberg New York, 154 pp

    Google Scholar 

  • Hastings MH, Herbert J, Hutchinson JB, Powers JB, Steel EA, Walker AP (1986) Gonadal response of the Syrian hamster to photoperiod is influenced by photoperiodic history. J Endocrinol 111 [Suppl]: Abstract No 30

  • Hazard TP, Eddy RE (1951) Modification of the sexual cycle in brook trout (S. fontinalis) by control of light. Trans Am Fish Soc 80:158–162

    Google Scholar 

  • Henderson NE (1963) Influence of light and temperature on the reproductive cycle of the eastern brook trout. J Fish Res Bd Can 20:559–597

    Google Scholar 

  • Hoar WS (1976) Smolt transformation: evolution behaviour and physiology. J Fish Res Bd Can 33:1233–1252

    Google Scholar 

  • Hoffmann K (1984) Photoperiodic reaction in the Djungarian hamster is influenced by previous light history. Biol Reprod 39 [Suppl]:55

    Google Scholar 

  • Hoover EE, Hubbard HE (1937) Modification of the sexual cycle in trout by control of light. Copeia 4:206–210

    Google Scholar 

  • Kavaliers M (1982) Seasonal and circannual rhythms in behavioural thermoregulation and their modifications by pinealectomy in the white sucker,Catastomus commersoni. J Comp Physiol 146:235–243

    Google Scholar 

  • MacQuarrie DW, Vanstone WE, Markert J (1979) Photoperiod induced off-season spawning of pink salmon. Aquaculture 18:289–302

    Google Scholar 

  • Nomura M (1962) Studies on reproduction of rainbow trout,Salmo gairdneri, with special reference to egg taking. III. Acceleration of spawning by control of light. Bull Jpn Soc Sci Fish 28:1070–1076

    Google Scholar 

  • Olive PJW (1984) Environmental control of reproduction in Polychaeta. Fortschr Zool 29:17–38

    Google Scholar 

  • Olive PJW, Garwood PR (1983) The importance of long-term endogenous rhythms in the maintenance of reproductive cycles of marine invertebrates: a reappraisal. Int J Invert Reprod 6:339–347

    Google Scholar 

  • Pittendrigh CS (1966) The circadian oscillation inDrosophila pseudoobscura pupae: a model for the photoperiodic clock. Z Pflanzenphysiol 54:275–307

    Google Scholar 

  • Pittendrigh CS (1981) Circadian systems: Entrainment. In: Aschoff J (ed) Biological rhythms (Handbook of behavioral neurobiology, vol 4). Plenum Press, New York, pp 95–124

    Google Scholar 

  • Randall CF, Duston J, Bromage NR (1987) Photoperiodic history and the entrainment of the annual cycle of reproduction in the female rainbow trout,Salmo gairdneri. Proc 3rd Int Symp Reproductive Physiology of Fish. St. Johns, Newfoundland. August 2–7, 1987, p 310

  • Robinson JE, Follett BK (1982) Photoperiodism in Japanese quail: the termination of seasonal breeding and photorefractoriness. Proc R Soc Lond 215B:95–116

    Google Scholar 

  • Robinson JE, Karsch FJ (1987) Photoperiodic history and a changing melatonin pattern can determine the neuroendocrine response of the ewe to daylength. J Reprod Fert 80:159–165

    Google Scholar 

  • Saunders DS (1976) Insect clocks. Pergamon Press, Oxford

    Google Scholar 

  • Shiraishi Y, Fukuda Y (1966) The relation between the daylength and the maturation in four species of salmonid fish. Bull Fresh Fish Res Lab 16:103–111

    Google Scholar 

  • Sundararaj BI, Vasal S, Halberg F (1982) Circannual rhythmic ovarian recrudescence in the catfishHeteropneustes fossilis (Bloch). Adv Biosci 41:319–337

    Google Scholar 

  • Takashima F, Yamada Y (1984) Control of maturation in masu salmon by manipulation of photoperiod. Aquaculture 43:243–257

    Google Scholar 

  • Thorpe JE (1986) Age at first maturity in Atlantic salmon,Salmo salar: Freshwater period influences and conflicts with smolting. Can Spec Publ Fish Aquat Sci 89:7–14

    Google Scholar 

  • Thorpe JE, Talbot C, Villarre C (1982) Bimodality of growth and smolting in Atlantic salmon,Salmo salar. Aquaculture 28:123–132

    Google Scholar 

  • Truman JW (1972) Physiology of insect rhythms I. Circadian organisation of the endocrine events underlying the moulting cycle of larval tobacco hornworms. J Exp Biol 57:805–820

    Google Scholar 

  • Whitehead C, Bromage N, Forster J, 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 

  • Yellon SM, Foster DL (1985) Alternate photoperiods time puberty in the female lamb. Endocrinology 116:2090–2097

    Google Scholar 

Download references

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Duston, J., Bromage, N. The entrainment and gating of the endogenous circannual rhythm of reproduction in the female rainbow trout (Salmo gairdneri). J. Comp. Physiol. 164, 259–268 (1988). https://doi.org/10.1007/BF00603956

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