Ž .Aquaculture 177 1999 47–60

Mechanisms underlying photoperiodic effects onage at sexual maturity in Atlantic salmon, Salmo

salar

Geir Lasse Taranger a,b,), Carl Haux c, Tom Hansen a,Sigurd O. Stefansson a,b, Bjorn Thrandur Bjornsson c,¨ ¨

Bernt Th. Walther d, Harald Kryvi e

a Institute of Marine Research, Matre Aquaculture Research Station, N-5198 Matredal, Norwayb Department of Fisheries and Marine Biology, Bergen High Technology Centre, UniÕersity of Bergen, N-5020

Bergen, Norwayc Department of Zoophysiology, UniÕersity of Goteborg, Medicinaregata 18, S-413 90 Goteborg, Sweden¨ ¨d Marine Molecular Biology Laboratory, UniÕersity of Bergen, Bergen High Technology Centre, N-5020

Bergen, Norwaye Department of Zoology, UniÕersity of Bergen, N-5007 Bergen, Norway

Accepted 1 October 1998

Abstract

Ž . ŽAtlantic salmon Salmo salar L. , reared in sea cages for 18 months age 36 months from. Ž . Ž .hatching , were exposed to natural light NL; control , or continuous light LL from January

Ž . Ž .ALJ or March ALM until July. Oocyte development appeared to be arrested at the oil dropstage during winter and spring in a proportion of the females following exposure to LL. This wasaccompanied by a decrease in plasma oestradiol-17b and testosterone levels following the onset ofLL. Somatic growth was affected by LL during winter and spring. However, the arrested sexualdevelopment in a proportion of the fish in the ALJ and ALM groups did not correlate with lowergrowth rate, body weight or condition factor compared with controls prior to the reduction inplasma sex steroid levels. These results suggest a photoperiodic advancement of the timing of anannual ‘critical period’ during which sexual maturation can be arrested. q 1999 Elsevier ScienceB.V. All rights reserved.

Keywords: Atlantic salmon; Photoperiod; Oocyte development; Oestradiol-17b; Testosterone; Somatic growth

) Corresponding author. Institute of Marine Research, Department of Aquaculture, P.O. Box 1870, N-5024Bergen, Norway. Tel.: q47-55-23- 85-00; Fax: q47-55-23-63-79; E-mail: geir.lasse.taranger@imr.no

0044-8486r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved.Ž .PII: S0044-8486 99 00068-X

( )G.L. Taranger et al.rAquaculture 177 1999 47–6048

1. Introduction

Early sexual maturation is a major problem in Atlantic salmon farming as maturationleads to reduced flesh quality and loss of growth during the spawning season. Sexuallymature fish can also experience high mortality if kept in sea water throughout matura-

Ž .tion. Previous studies indicate that the use of continuous light LL on sea cages duringŽwinter and spring can reduce the proportion of mature Atlantic salmon Hansen et al.,

. Ž .1992; Taranger et al., 1995, 1998 . Hansen et al. 1992 suggest that this effect could bedue to a photoperiodic advancement of a postulated ‘critical period’ during winter and

Ž .early spring. Thorpe 1986, 1989, 1994 hypothesized that if salmonids exceed agenetically determined developmental threshold during this ‘critical period’, maturationwill be completed in the following spawning season, otherwise maturation will bepostponed for a year. A reduction in the proportion of maturing rainbow trout was alsofound following exposure to an accelerated photoperiod regime, and it was hypothesizedthat maturation is only allowed in fish which have exceeded certain thresholds of

Ž .development at a time when an endogenous clock is at a specific phase ‘gate open’ ofŽ .the circannual cycle Duston and Bromage, 1988 .

In general, it is assumed that higher growth rate leads to lower age at maturityŽ .Thorpe, 1986, 1994; Fleming, 1996 , and maturity may depend on exceeding thresholds

Ž . Žof growth rate Thorpe, 1989; Thorpe et al., 1990 , body size McCormick and Naiman,. Ž1984; Skilbrei, 1989 , lipid stores or rate of lipid storage Rowe and Thorpe, 1990;

. ŽRowe et al., 1991; Thorpe, 1994 , stage of gonadal development Sutterlin and MacLean,.1984; Chadwick et al., 1986 , or a combination of such factors. If photoperiodic

Žtreatment advance the timing of the ‘critical period’ e.g., Duston and Bromage, 1988;.Adams and Thorpe, 1989; Duston and Saunders, 1992 , this may prevent some fish from

exceeding potential threshold values of one or more of these factors.Alternatively, the photoperiodic effect on age at maturity may be due to altered rates

of growth andror energy storage during the ‘critical period’, as LL has been shown toŽaffect growth performance of Atlantic salmon in seawater tanks Saunders and Harmon,

. Ž1988; Taranger et al., 1995 and sea cages Endal et al., 1991; Krakenes et al., 1991;˚.Hansen et al., 1992; Taranger et al., 1995 . The reduction in growth rate observed

Žimmediately following the onset of LL in winter Endal et al., 1991; Krakenes et al.,˚.1991; Hansen et al., 1992; Taranger et al., 1995 may coincide with the ‘critical period’,

and may arrest sexual development in some of the fish.To investigate whether the reduced proportion of sexually maturing fish following

exposure to LL may be due to altered growth performance per se, or due to alterations inthe timing of the postulated ‘critical period’, Atlantic salmon were exposed to LL fromJanuary or March, and somatic growth, gonadal development, plasma oestradiol-17b

Ž . Ž .E and testosterone T levels were monitored.2

2. Materials and methods

2.1. Fish stock, rearing conditions and experimental design

Ž . Ž .Atlantic salmon Salmo salar L. were reared under natural light NL in sea cagesŽ .for 18 months at Matre Aquaculture Research Station, Norway 618N . The fish used

( )G.L. Taranger et al.rAquaculture 177 1999 47–60 49

were from a low grilsing strain where most of the fish mature for the first time after 2years in sea water, with a normal spawning time during November and December. On

Ž . Ž .January 16 36 months after hatching , grilse fish maturing after 1.5 years in sea waterwere removed from the population, and 600 of the remaining fish were individually

Ž w .tagged with anchor T-bar tags beneath the dorsal fin Floy Tag, Seattle, WA . The3 Ž 3.tagged fish were randomly distributed into three 125 m sea cages 5=5=5 m , 200

fish in each cage. The sex ratio was 67% females and 33% males due to the removal ofgrilse. Water temperature at 5 m depth ranged from 6.5 to 148C during the period fromJanuary until July. Salinity at 5 m depth ranged from 23 to 33‰ with a mean of 29.5‰in the same period.

Three different photoperiod regimes were used between January 16 and July 13:Ž . Ž . Ž .natural light NL; control , natural lightqcontinuous light LL from March 13 ALM ,

Ž .or natural lightqcontinuous light from January 23 ALJ . The LL was supplied by a1300 W quartz halogen light mounted 1.2 m above the sea level of each cage. The fish

Ž .were fed a commercial dry diet Tess Edel, T. Skretting, Norway in surplus fromautomatic feeders during the hours of natural daylight.

2.2. Data sampling and analyses

Prior to the establishment of the photoperiod regimes, on January 5, 23 fish wereblood sampled, sexed, and gonads were weighed to the nearest 0.1 g. Gonadosomatic

Ž . Ž . y1index GSI was calculated as: GSI % sgonad weight=100= fish weight . Subse-quently, monthly blood samples were taken from randomly selected fish under benzo-

Ž . Ž .caine anaesthesia 20 fish from each group . The samples 6 ml were collected from thecaudal vessels in heparinized syringes between 10:00 and 12:00, and stored on ice for

Ž .30–120 min before centrifugation 5000 rpm, 48C, 10 min . Blood was not sampledfrom the same individual on two subsequent sampling occasions. Plasma was stored aty808C until analysed.

On February 28, April 24 and June 20, 10 fish from each group were killed andsexed. The gonads were excised and GSI determined. Small transverse sections from the

Žmiddle region of the largest gonad were stored in modified Karnofsky fixative 900 mlwbuffer 24.1 g sodium cacodylate, 55 g sucrose and 0.2 g CaCl =2H O in 1000 ml2 2

x .deist. water , added to 20 ml 25% glutaraldehyde and 120 ml 3% formaldehyde . Asmall sample of the ovary was dehydrated and embedded in Historesin. Sections werecut at 1 mm, stained with toluidine blue and examined under light microscopy forhistological development. The oocytes were classified into the following stages belowŽ .cf. Nagahama, 1983; Bromage and Cumaranatunga, 1988 .

2.2.1. Primary growth phase oocytesCn: Chromatin–nucleolus stage. Apparent nucleolus and chromatin threads.Pn: Perinucleolus stage. Multiple nucleoli located around the periphery of the nucleus.

2.2.2. Secondary growth phase oocytesŽ .Ca: Cortical alveoli stage. Cortical alveoli yolk vesicles appear in the periphery of

the oocyte.

( )G.L. Taranger et al.rAquaculture 177 1999 47–6050

Od: Oil drop stage. Oil droplets appear in the perinuclear area, later also in theperiphery.

2.2.3. True ÕitellogenesisPy: Primary yolk stage. Yolk globules appear in the periphery of the oocyte.Sy: Secondary yolk stage. More yolk globules appear throughout the oocyte.Ty: Tertiary yolk stage. The oocyte is filled with yolk globules.

2.2.4. AtresiaŽ .At: Atretic oocytes were determined according to Saidapur 1978 .

The fish were classified in terms of sex and stage of maturation either on the basis ofovulation or spermiation during autumn, or on the basis of GSI in sacrificed fish from

Ž .April 24 onwards cf. Taranger et al., 1998 for details . As the sex ratio was skewed dueto the removal of previously mature males prior to the start of the experiment, maleobservations were relatively scarce, hence, only female data are presented.

2.3. Growth measurements

On January 17, February 28, April 24, and June 20, all remaining fish wereanaesthetized with benzocaine, measured for fork length to the nearest 0.5 cm, and

Ž .weighed to the nearest 10 g. Individual specific growth rate SGR was calculated as:Ž g . Ž .Ž .y1SGRs e y1 )100, where gs ln W y ln W t y t , where W is body weight2 1 2 1 2

Ž .at t , and W is body weight at t . Condition factor CF was calculated as: CFs2 1 1y3 Ž . Ž .WL )100, where W is body weight g and L is fork length cm .

2.4. Hormone analyses

Plasma samples of 100–400 ml were analysed for E and T by radio-immunoassay2Ž .according to Taranger et al. 1998 .

2.5. Statistics

Ž .Data were analysed by Statistica 5.0A StatSoft, Tulsa, USA . Mean values are givenŽ ."SE standard error of mean . Plasma E and T levels were compared with Kruskal–2

Ž .Wallis test followed by single comparisons with Mann–Whitney U-test Zar, 1996 . Theeffects of photoperiod treatment on SGR, body weight and CF were tested using a

ŽOne-way ANOVA, followed by Student–Newman–Keul multiple comparison Zar,.1996 . Prior to the ANOVA, the data were checked for normal distribution using a

Ž .normal plot, and for homogeneity in variance by Barlett’s test Zar, 1996 . A signifi-Ž .cance level a of 0.05 was applied in all tests except where indicated.

3. Results

3.1. Plasma steroids

Plasma E and T levels were grouped according to photoperiodic treatment, sex and2Ž .maturation Fig. 1 . Only female data and subgroups with sufficient number of observa-

tions are shown.

( )G.L. Taranger et al.rAquaculture 177 1999 47–60 51

Ž . Ž .Fig. 1. Mean plasma oestradiol-17b E ; a and testosterone T; b levels of Atlantic salmon females following2Ž .exposure to NL or ALJ or ALM to July. Control NL females on January 5 l; ns17 , maturing NL females

Ž . Ž . Žv; ns7–11 , maturing ALM females B; ns5–11 , immature ALM females I; ns5–7, ns1 on July. Ž .18 and immature ALJ females ^; ns8–12, ns4 on February 28 . Vertical bars represent SE. Asterisks

Ž U UU .denote groups which are different from maturing NL females Mann–Whitney U-test; pF0.05, pF0.01 .

( )G.L. Taranger et al.rAquaculture 177 1999 47–6052

The E and T levels obtained on January 5 were collected from NL females which2Ž .were sacrificed for gonadal samples mean GSIs0.41"0.04%, ns17 . These values

were compared with immature NL, ALM and ALJ females pooled within each group forthe period of February to July using Mann–Whitney U-test. The E levels in the control2

females on January 5 were significantly elevated compared with immature NL femalesŽ . Ž .ns12, ps0.003 , immature ALJ females ns52, ps0.000003 and immature

Ž .ALM females ns21, ps0.0001 during the February to July, whereas the samecomparison gave no significant differences in T levels.

Only a few immature NL females were available for hormonal analysis, but theirŽ y1plasma levels remained stable and low E s0.21"0.05 ng ml , Ts0.30"0.05 ng2

y1 .ml , ns12 from February through July. By contrast, the plasma levels in maturingŽ y1NL females were elevated compared to immature fish E )0.6 ng ml except in two2

y1 .cases, and T)0.5 ng ml and increasing with time during the same period.E and T were significantly lower in immature ALJ females than in maturing NL2

females from February 28 onwards, and stayed low and at the same level as in immatureNL females until July. As a result of a low number of maturing fish in the ALJ group,no comparison could be done between E and T levels in maturing ALJ females and2

other groups.A decrease in plasma E and T levels was observed in immature ALM females after2

onset of LL, as the levels were significantly lower compared with maturing NL femalesŽ .from March 30 and April 24 onwards for E and T, respectively . Subsequently, the E2 2

and T levels in immature ALM females remained low and at the same level as inimmature NL and ALJ females until July. A significant decrease in E also occurred in2

maturing ALM females on March 30 following onset of LL compared with maturing NLfemales. However, the E levels increased again, and both E and T tended to be higher2 2

Žin maturing ALM females than in maturing NL females during April to July significant.in May for E , and in May and July for T .2

3.2. Oocyte deÕelopment

The various stages of oocyte development found in the histological preparations areshown in Fig. 2. The histological preparations generally contained oocytes in bothprimary and secondary growth phases, but one preparation from late spring only

Ž .contained secondary growth phase oocytes due to small sample size Table 1 . OnFebruary 28, the most advanced oocytes within each female ranged from cortical alveoli

Ž .to primary yolk ns6 . By April 24, the most advanced oocytes ranged from oil drop

Ž .Fig. 2. Different stages in the maturation of oocytes: chromatin–nucleolus a; denoted by an arrow , earlyŽ . Ž . Ž .perinucleolus b , a later stage of early perinucleolus c , late perinucleolus d , cortical alveolirearly oil drop

Ž . Ž . Ž . Ž . Ž .e , oil drop f , secondary yolk g , tertiary yolk h , and an atretic oocyte i . Abbreviations: A scorticalalveolus, Osoil drop, Ys yolk globule. Arrow in panel e indicates the zona radiata. Magnification 150=;the bar in panel i is 100 mm and is valid for all panels.

( )G.L. Taranger et al.rAquaculture 177 1999 47–60 53

( )G.L. Taranger et al.rAquaculture 177 1999 47–6054

Table 1Ž .GSI, maturity classification, and distribution of the different oocyte stages % in Atlantic salmon females

Ž .exposed to different photoperiod regimes from January until July; natural light NL , continuous additionalŽ . Ž .light from March ALM , continuous additional light from January ALJ

Ž .Date Group GSI % Maturity n Cn Pn Ca Od Py Sy Ty At

February 28 NL 0.36 56 5 71 21 0 0 0 0 20.45 47 0 62 21 9 0 0 0 90.53 35 0 48 6 46 0 0 0 00.56 37 3 19 30 35 11 0 0 3

ALJ 0.58 65 3 51 0 38 0 0 0 80.58 25 0 92 0 4 0 0 0 4

April 24 NL 0.50 maturing 42 0 26 0 0 57 0 0 170.69 maturing 58 0 45 0 0 9 36 0 100.76 maturing 12 0 50 0 0 0 50 0 00.85 maturing 12 0 25 0 0 33 33 0 80.90 maturing 15 0 20 0 0 0 67 0 130.93 maturing 17 0 59 0 12 0 24 0 6

ALM 0.28 immature 46 0 48 15 30 0 0 0 70.30 immature 35 0 68 0 26 0 0 0 60.31 immature 54 0 57 9 20 0 0 0 130.32 immature 49 0 63 0 37 0 0 0 00.61 maturing 16 0 56 6 0 31 0 0 6

ALJ 0.35 immature 90 0 57 6 29 0 0 0 80.40 immature 32 0 44 50 3 0 0 0 30.42 immature 27 0 38 7 56 0 0 0 00.45 immature 54 0 50 4 41 0 0 0 6

June 20 NL 0.75 maturing 48 0 48 0 8 0 33 0 100.83 maturing 27 0 41 0 0 40 0 0 190.99 maturing 21 0 34 0 0 52 0 0 141.00 maturing 5 0 0 0 0 0 100 0 0

ALM 0.47 immature 25 0 0 24 36 0 0 0 400.47 immature 65 0 53 0 37 0 0 0 110.62 maturing 27 0 15 0 22 4 0 0 592.09 maturing 9 0 11 0 0 0 56 33 02.41 maturing 6 0 33 0 0 0 17 50 0

ALJ 0.32 immature 26 0 54 0 38 0 0 0 80.43 immature 47 0 25 0 57 0 0 0 170.64 maturing 51 0 34 0 0 0 33 0 330.76 maturing 28 0 50 0 14 0 21 0 142.09 maturing 9 0 11 0 0 0 33 44 11

Ž . Ž . Ž . Ž .Oocyte stages: chromatin–nucleolus Cn , perinucleolus Pn , cortical alveoli Ca , oil drop Od , primary yolkŽ . Ž . Ž . Ž .Py , secondary yolk Sy , tertiary yolk Ty , and atretic oocytes At .n refers to number of oocytes examined in each female.

to secondary yolk. Females with GSI-0.50 on April 24 and June 20 had no oocytesbeyond the oil drop stage and were classified as immature. All examined females in the

Ž .NL group ns10 had oocytes in primary yolk or more advanced stages on April 24and June 20, whereas four of nine females in the ALJ group, and four of 10 females inthe ALM group had no oocytes beyond the oil drop stage at these dates.

( )G.L. Taranger et al.rAquaculture 177 1999 47–60 55

Table 2Ž y1 .Individual specific growth rate % day of Atlantic salmon exposed to different photoperiods from January

Ž . Ž .until July: natural light NL , continuous additional light from March ALM , or continuous additional lightŽ .from January ALJ

Group Time period

January 17–February 28 February 28–April 24 April 24–June 20

Mean"SE n Mean"SE n Mean"SE na a aNL 0.33"0.01 182 0.54"0.01 158 0.45"0.01 134a b bALM 0.35"0.01 191 0.49"0.01 172 0.41"0.01 153b c aALJ 0.39"0.01 193 0.44"0.01 171 0.47"0.01 147

ŽDifferent superscripts within a time period denote significant differences One-way ANOVA followed by.Student–Newman–Keul multiple comparison .

3.3. Somatic growth

Ž .Mean individual growth rate SGR during January to June was significantly affectedŽ .by photoperiod treatment Table 2 . SGR was significantly higher in the ALJ group than

Ž .in the ALM and NL groups during January–February Table 2 , whereas it wassignificantly lower in both the ALJ and ALM groups compared with the NL groupduring February–April. SGR was significantly lower in the ALM group compared withboth the NL and ALJ groups during April–June. The rapid growth in the NL group fromFebruary until June resulted in significantly higher mean body weight compared with the

Fig. 3. Mean body weight of Atlantic salmon exposed to different photoperiod regimes from January untilŽ . Ž . Ž .July: NL v; ns138–191 , ALM I; ns155–198 and ALJ ^; ns152–200 . Vertical bars represent SE.

Different letters indicate significant differences between groups.

( )G.L. Taranger et al.rAquaculture 177 1999 47–6056

ŽFig. 4. Mean CF of Atlantic salmon exposed to different photoperiod regimes from January until July: NL v;. Ž . Ž .ns138–191 , ALM I; ns155–198 and ALJ ^; ns152–200 . Vertical bars represent SE. Different

letters indicate significant differences between groups.

Ž .ALM and ALJ groups in April, and compared with the ALM group in June Fig. 3 .There were no significant differences in body weight between the ALJ and ALM groups.

Ž .CF increased rapidly in all groups during spring Fig. 4 . The increase was mostpronounced in the NL group, resulting in a significantly higher CF in the NL groupcompared with the ALJ group in April and June, and compared with the ALM group inJune. A transitory lower CF was observed in the ALM group in February, comparedwith both the NL and ALJ groups.

4. Discussion

The proportions of sexually maturing fish in this experiment have been reportedŽ .previously Taranger et al., 1998 , where 91, 67 and 9% of the females in the NL, ALM

and ALJ groups, respectively, were classified as maturing. A similar reduction in theproportion of sexually maturing males from 74% in the NL group, to 57 and 16% wereseen in the ALM and ALJ groups, respectively. The present study indicates that thereduced proportion of maturing females was accompanied by arrested oocyte develop-ment and a decline in plasma E and T levels in a proportion of the females following2

exposure to LL.The blood samples obtained on January 5 were collected from individuals which were

sacrificed for gonadal samples, and it was not possible to determine sexual maturation atthis time of the year. However, as 91% of the females in the NL groups in the present

( )G.L. Taranger et al.rAquaculture 177 1999 47–60 57

Ž .study were maturing cf. Taranger et al., 1998 , it is reasonable to take the mean valueson January 5 as representative for maturing females. The plasma E levels on January 52

were significantly higher compared with immature females in the NL, ALM and ALJgroups during spring, indicating that sexual maturation were in progress in most females

Ž . Ž .by this date. This is in accordance with Hunt et al. 1982 and Youngson et al. 1988who found that maturing two sea-winter salmon had elevated E levels compared with2

immature females during January and February.The decline in E and T levels in immature ALM females following exposure to LL,2

and the low E and T levels in immature ALJ females on February 28, indicate that2

maturation was arrested within 4 to 6 weeks after onset of LL in these fish. Thus, theplasma E and T levels in the present study indicate that maturation had commenced by2

early January in most females, whereas sexual development was arrested within a fewweeks after exposure to LL in a proportion of the females in the ALM and ALJ groups.

All females examined had oocytes in the cortical alveoli stage, or a later stage, onFebruary 28, whereas the most advanced oocytes in the NL females were in the primary

Ž .or secondary yolk stage on April 24 Table 1 . This suggests that the secondary growthphase had commenced in all or most females by late February, and that exogenousvitellogenesis had commenced in most maturing females by late April. By contrast, inthe ALM and ALJ groups, no oocytes were found to proceed beyond the oil drop stageduring April and June in a large proportion of the females, suggesting that oocytedevelopment was arrested at this stage following exposure to LL. Taken together withthe plasma sex steroid profiles in females were maturation appeared to be arrested, theseresults suggest that oocyte development was arrested at the oil drop stage in a proportionof the fish following exposure to LL.

The effects of accelerated photoperiod regimes on the proportion of sexually matur-ing salmon have previously been explained by either an advancement of the timing of a

Ž‘critical period’ during winter and spring Adams and Thorpe, 1989; Hansen et al.,.1992 , or by a direct effect of photoperiod on growth andror energy storage during thisŽ .period Hansen et al., 1992 . To evaluate these possibilities, growth rate, body size, CF

Ž .as a measure of energy stores cf. Herbinger and Friars, 1991 , and oocyte developmentwere correlated with the timing of the arrested sexual development as indicated by thedecline in plasma sex steroid levels.

E levels were low from February 28 onwards in immature ALJ females, and from2

March 30 onwards in immature ALM females, suggesting that maturation was arrestedin a proportion of the females prior to these dates following exposure to LL. Theseresults may be interpreted such that the ‘critical period’ was completed progressivelyearlier in the ALM and ALJ groups than in the NL group. An earlier completion of the‘critical period’ during winterrspring would result in fish having a lower growth rateŽ . Ž . Ž .Table 2 , body weight Fig. 3 and CF Fig. 4 , as these parameters generally increasedfrom January onwards. Thus, if completion of maturation depends on exceedingthreshold values of either body size, growth rate or CF, fewer fish would have exceededany of these thresholds by the end of the ‘critical period’ in the ALJ and ALM groupscompared with the NL group. Correspondingly, the lower proportion of maturing fish inthe ALJ group than in the ALM group may have been due to a larger advancement ofthe ‘critical period’ in the ALJ group.

( )G.L. Taranger et al.rAquaculture 177 1999 47–6058

An advancement of the ‘critical period’ may have been due to a phase shift of anŽendogenous circannual rhythm controlling the timing of sexual development cf. Duston

.and Bromage, 1988 . Such a phase shift was indicated in the present study by anadvancement of ovulation and plasma sex steroid profiles in maturing females in theALM group compared with the NL group, whereas the low number of maturing fish in

Ž .the ALJ group prevented such an examination cf. Taranger et al., 1998 .Maturation may also depend on the acquisition of a certain stage of gonadal

development prior to a critical time in winterrspring, as well as the need to exceed somegrowth related threshold. Hence, if the timing of the ‘critical period’ differed among thegroups as suggested above, gonadal development would have been at different stages at

Ž .the end of the ‘critical period’ in each group cf. Table 1 . Fish that did not reach thisstage prior to the end of the ‘critical period’ may have failed to mature.

A transient reduction of growth rate has been observed following onset of LL inŽwinter in previous studies on Atlantic salmon Endal et al., 1991; Krakenes et al., 1991;˚

.Hansen et al., 1992; Taranger et al., 1995 , and it has been suggested that this reductionin growth may have caused the reduced proportion of sexually maturing fish reported in

Ž .some of the experiments e.g., Hansen et al., 1992; Taranger et al., 1995 . Such an initialgrowth depression was indicated in the ALM group following onset of LL in March, but

Ž .not following onset of LL in the ALJ group in January Table 2 . No negative effects ofLL on growth rate, body weight or CF were observed prior to February 28 in the ALJgroup, at the time when the plasma sex steroids had reached immature levels. In theALM group, the CF on February 28 and the growth rate during February–April werelower than in the NL group, prior to andror concomitant with the decrease in plasmasex steroid levels in immature ALM females. However, CF increased rapidly in theALM group between February 28 and April 24, indicating increasing energy stores atthe same time as maturation appeared to be arrested in some of the individuals in theALM group. Taken together, these results do not suggest that maturation was arrested byreduced growth performance in either the ALM or ALJ group.

The reduced proportions of mature fish in the ALJ and ALM groups may also be dueto direct effects of LL on the neuroendocrine regulation of maturation independent ofany time shifts of a ‘critical period’ or differences in growth performance. The abruptchange from natural photoperiod to LL in January or March, could lead to a breakdownof circadian rhythms in neurohormonal signals to the hypothalamus andror pituitary

Žwhich potentially could affect the synthesis andror release of gonadotropins cf.. Ž . Ž .Sumpter, 1990 . On the other hand, Endal et al. 1991 and Krakenes et al. 1991˚

observed higher proportions of fish maturing as grilse following exposure of Atlanticsalmon post-smolts to LL from November, December or February until the summersolstice, which seems to contradict a direct negative interference between LL andmaturation. This may imply that differences in physiological state such as age, size,growth rate, energy stores and stage of gonadal development determine the response toLL.

In conclusion, the present results suggest that the effects of LL on age at firstmaturity are not due to effects of photoperiod on growth performance per se, but aremore fully explained by a model involving a photoperiodic alteration of the timing of a‘critical period’.

( )G.L. Taranger et al.rAquaculture 177 1999 47–60 59

Acknowledgements

The authors are grateful to Prof. Snorre Tilseth, Prof. Dag Møller, and Dr. Hjalti ı́Jakupsstovu for essential support in carrying out this research. Special thanks to Tone´Knapskog and the staff at the Matre Aquaculture Research Station for excellenttechnical assistance during the study. This study was financed by the Nordic Fund for

Ž .Technology and Industrial Development 88.107 and the Norwegian Fisheries ResearchŽ .Council V.701.236 and V.701.211 .

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