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Effects of pre-smolt photoperiod regimes on post-smolt growth rates of different genetic groups of Atlantic salmon (Salmo salar)
Aquaculture 242 (2004) 671 – 688 www.elsevier.com/locate/aqua-online
Effects of pre-smolt photoperiod regimes on post-smolt growth rates of different genetic groups of Atlantic salmon (Salmo salar) Ove Tommy Skilbreia,*, Tom Hansenb a Institute of Marine Research, P.O.B. 1870, N-5024 Bergen-Nordnes, Norway Matre Aquaculture Research Station, Institute of Marine Research, N-5198 Matredal, Norway
b
Received 21 February 2004; received in revised form 9 September 2004; accepted 13 September 2004
Abstract The aim was to study relationships between photoperiod in freshwater and growth rates prior to and following seawater exposures for fish from different stocks. Individually tagged 1+juveniles originating from four different stocks of Atlantic salmon were reared under the constant photoperiods LD10:14, LD12:12, LD14:10 and LD16:8 and under simulated natural increasing photoperiods from early spring starting from LD11:13 (SNP-11; fish from LD10:14 and LD12:12) or from LD15:9 (SNP-15; fish from LD14:10 and LD16:8). The groups were exposed to running seawater during May and June under LD22:2 and transferred to natural light regime in late July to monitor the subsequent growth rates in seawater for the next 6 months. The genetic origin of the fish was the factor of most influence for variation in the proportion and growth rates of the upper modal group fish in freshwater. The Dale stock showed the best growth performance, followed by the Vosso, Hatchery and the Lone stock. During the first 3–6 weeks in seawater, there was an evident and common drop in growth rates for all the stocks. The largest part of the variation in growth could be attributed to pre-smolt photoperiods, as the drop in growth rates was less pronounced for the fish previously held under increasing photoperiod in freshwater. During the next 5 months in seawater, the significance of stock was partly re-established. The Dale, Vosso and Hatchery stocks reached comparable sizes, significantly larger than the Lone stock. In addition, the initially slow growing groups under constant photoperiod in freshwater grew at the highest rate resulting in no differences in final sizes between treatment groups, possibly implying that their
* Corresponding author. Tel.: +47 55236894; fax: +47 55236891. E-mail address: [email protected] (O.T. Skilbrei). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.09.017
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transfer to long daylength in seawater stimulated growth and/or completed the smoltification process. Relationships between photoperiod in freshwater, smoltification and growth rate before and after seawater exposure are discussed. D 2004 Elsevier B.V. All rights reserved. Keywords: Atlantic salmon; Smoltification; Growth; Photoperiod
1. Introduction Atlantic salmon smoltify naturally under increasing photoperiod in spring. Photoperiod influences pituitary cytology (Komourdjian et al., 1989), timing of smoltification and the development of hypoosmoregulatory ability of Atlantic salmon (Sigholt et al., 1995; Duston and Saunders, 1990; Stefansson et al., 1991). The smoltification process is partly under endogenous control and annual rhythms have been observed under constant photoperiod regimes (Eriksson and Lundqvist, 1982). Photoperiod also influences the growth rate by stimulating growth under increasing and long daylengths (Villarreal et al., 1988; Bjo¨rnsson et al., 1989). Short daylengths during the first winter in freshwater may reduce growth rates and decrease the proportion of 1-year smolts (Skilbrei, 1991; Skilbrei et al., 1997). It is generally believed that, in hatchery 0+ and 1+ smolt production, a shortening followed by an increase in daylength stimulate smoltification (Berge et al., 1995). As it is beneficial to maximise growth during the freshwater phase, and also to ensure a proper smoltification process, it is of interest for salmonid culture to study relationships between photoperiod, proportion of the upper modal size group, growth rate and parr–smolt transformation to find the best compromise between freshwater growth and smoltification. Smoltification is characterised by a large number of morphological, biochemical, physiological and behavioural changes (Folmar and Dickhoff, 1980; McCormick and Saunders, 1987; Hoar, 1988). The parr–smolt transformation can be measured at different levels. Measurements of enzymatic and physiological mechanisms involved in hypoosmotic regulation are indicative of the onset and development of seawater tolerance (Hoar, 1988, Duston and Saunders, 1990; Rourke et al., 1991; Lubin et al., 1991). The effects of these mechanisms and the degree of parr–smolt transformation may be evaluated by plasma ion concentrations after exposure to seawater. Such measurements are usually performed shortly after the exposure to a higher salinity. A drawback with these methods is that they do not distinguish between seawater tolerance and preference. A fish may be able to regulate its plasma ions, but it is still a question whether the smolt has reached a level of adaptation that enables it to thrive in the marine environment. The nature of the challenge may depend on the purpose of the smolt production; for cage rearing or sea ranching. After the time of seawater entry, the development of a hypo-osmoregulatory ability is only one of the challenges for a released smolt to survive in the wild. It also has to be able to feed, and it may experience accumulated stress because of osmotic imbalance in addition to the presence of predators (Ja¨rvi, 1990) when organising into migrating schools (Skilbrei et al., 1994a,b). To cope with these problems, a fully smoltified fish must be capable of gaining surplus energy shortly after seawater entry. If fish which have not completed the parr–
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smolt transformation grow slower in seawater than those fish that are fully smoltified, measurements of individual growth rates after exposure to seawater may be a good indicator of relative differences in seawater tolerance between treatment groups (Thrush et al., 1994; Duston and Saunders, 1995; Duncan et al., 1998; Handeland and Stefansson, 2001). The growth rates may be of interest during two stages: shortly after seawater transfer, and also after prolonged stay to see whether the poorly growing fish adapt or not. If growth rate is used as an indirect indicator of smoltification or general welfare, then other causes for variation in growth rates should also be considered. Growth rates in freshwater prior to seawater exposure may differ between treatment groups and may therefore have an impact on subsequent performance (Duncan et al., 1998, 1999). Further, there is a high degree of individual variance in quantitative traits such as growth rates which in part can be explained by genetics (Nævdal, 1983; Hanke et al., 1989). If seawater tolerance and growth rate are linked, will then genetic differences in growth potential influence the response to seawater exposure? Alternatively, there may be genetic components influencing adaptation to seawater regardless of earlier growth rate. The aim of the present work was to compare growth rates of individually tagged smolts of different stocks of Atlantic salmon from the freshwater phase when they were reared under different photoperiods, through smoltification until the post-smolt stage in seawater.
2. Materials and methods 2.1. Experimental fish 0+ family offspring from wild parents originating from the Lone River grilse stock (location of river mouth: N 60852VE 5849V) and the multi-sea-winter stocks of River Dale (N 60858VE 5878V) and Vosso River (N 60864VE 5896V) were first fed in March and reared in separate tanks at Sagen Hatchery under continuous light until September. The wild parents were included in a larger screening of microsatelitte DNA in the three rivers. According to K. Glover (Institute of Marine Research) clear genetic distances between the rivers were observed. 0+ juveniles from a hatchery stock (BP Salar 2lvik) (the third generation held in captivity) were also included. To establish groups of equal size at the start of the experiment, only fish ranging between 70 and 81 mm (mean varied from 74 to 76 mm) were selected for the experiment and transferred to the Institute of Marine Research (N 60840V, E 5831V). This length range was chosen because other studies have shown that fish of this size have responded very clearly to photoperiod adjustments by altering growth rates and proportions of the upper mode sized fish (Skilbrei et al., 1997). In addition, repeated selection at different dates of fish of 70–80 mm from a basic group have shown very similar results (Skilbrei, 1991), indicating that the relative differences in growth prior to the photoperiod adjustments had a minor effect for the further development of bimodality in this length group. Therefore, one intention for using selected length groups was to minimise the possible effects of different selection intensities among the stocks. Prior to the experiment, 38% of the Lone fish in the tanks at Sagen Hatchery were within the 70–81 mm length interval, 24% were larger. The corresponding proportions for the Dale and the Vosso stocks were 38% and 53%, and 22% and 66%, respectively. The
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fish was further divided into two new length groups; one of 70–74 mm (n=771) and one of 75–81 mm fork length (n=821). The initial size groups and stocks were identified by a combination of fin clips and dye marking. 2.2. Experimental design 2.2.1. Part A—indoor rearing at the Institute of Marine Research (Fig. 1) Photoperiods were LD24:0 prior to, and LD10:14, LD12:12, LD14:10 or LD16:8 after the start of the experiment on September 19. The source of illumination was 215 W fluorescent tubes providing 2.1–3.4 W m 2 10 cm below surface and 1.5–2.2 W m 2 at the bottom of the covered rectangular 180 l fibreglass tanks (LI-COR LI1000 Underwater Sensor). One-half of the smallest fish (70–74 mm) were reared in separate tanks (SS groups) under each photoperiod (22–34 individuals per stock per tank), while the rest of the small fish were mixed in the tanks (SM groups) with the large fish (75–81 mm, LA groups). Due to a lower number of Vosso fish (410 vs. 679–839) they were not included in all treatment groups. Statistical comparisons of the differences in the proportions of upper modal group fish in the mixed tanks were done within, but not between, the photoperiods. The reasons are that the density of fish was 30% higher in the mixed LD10:14 tank for the first week of the experiment and that 35% of the fish in the mixed LD16:8 tank died after 8 days due to a temporary reduction in the supply of water. These circumstances may have enlarged the effects of photoperiod.
Fig. 1. Temperature regimes (A) and experimental set-up (B) during part A of the experiment. Arrows show time for change of photoperiods and switches of salinity from fresh- to seawater (SWS1–3). Constant photoperiods are LD10:14 (LightDark10:14), LD12:12, LD14:10, LD16:8, LD22:2 and LD24:0. The simulated natural photoperiods starts at LD11:13 (SND-11) and at LD15:9 (SNP-15). M=date of measurement. T=date of tagging.
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Two new photoperiods were started on February 12. Samples of fish from LD10:14 and LD12:12 were distributed in two tanks (replicates) and given simulated natural photoperiod (SNP-11) starting at 11 h day 1 while fish from LD14:10 and all fish from LD16:8 were reared in two tanks (replicates) under simulated photoperiod starting at 15 h day 1 (SNP-15, see experimental set-up, Fig. 1). Number of fish in the seven tanks varied between 75 and 108 individuals (Table 1). On May 1, May 25 and June 16 fish from the seven tanks were mixed randomly in new tanks and exposed to running seawater under LD22:2 by switching the water supply from fresh- to seawater (seawater switch 1, 2 and 3; SWS1, SWS2 and SWS3, see Fig. 1). 2.2.2. Part B—outdoor rearing at Austevoll Aquaculture Research Station On July 25, when all groups had been held in seawater for at least 5 weeks, the fish were transferred to the Austevoll Aquaculture Research Station (N 60809V, E 5826V) to be reared outdoor under natural photoperiod in two 3 m diameter circular tanks supplied with seawater (pumped deep water) until January 10, when the experiment was ended. 2.3. Measurements and tagging of fish All fish were anaesthetized (Metomidate), and weight (F0.01 g) and fork length (F1 mm) were measured at the start of the experiment, to record bimodality in late autumn, at tagging, the day before each seawater exposure, 3–4 weeks after a seawater exposure and Table 1 Numbers of individually tagged fish from the different stocks held under the different photoperiods Stock
Period: H D L V SUM
Photoperiods LD10:14 (n)
LD12:12 (n)
LD14:10 (n)
SNP-11
Feb–May 11 6 6 10 29
2 8 5 7 22
11 13 13
7 8 8 11 34
26 25 20 28 99
May 1 (+re-tagged) H 24 D 20 L 18 V 21 SUM 83
14 25 18 18 75
January H D L V SUM
4 17 7 8 36
10 10 5 6 10 31
37
26 24 25 75
11 16 10 36
17 23 14 26 80
H=Hatchery, D=River Dale, L=River Lone and V=River Vosso. a Replicate tank.
SNP-11a (n)
SNP-15 (n)
SNP-15a (n)
4 8 13 11 36
6 15 10 3 34
7 12 12 4 35
25 30 34 19 108
23 25 24 7 79
23 25 23 6 77
17 34 18 7 76
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at the end of the experiment; September 19, December 4–6, February 6–11, May 1, May 23–24, June 16–17, July 13–14 (see Fig. 1) and January 10. All strains developed bimodality during autumn. From February 6–11 parr assumed not to smolt the following spring (lower modal group; based on bimodal length– frequency distributions) were removed, and remaining pre-smolts were individually tagged with Visible Implant Tags (VIT). Of the 617 individuals tagged with Visible Implant Tags (VIT) in February, 607 were alive in May but 367 had lost their tags (20 to 37 fish in each tank). These fish were re-tagged on May 1 (except 15 individuals with regenerated fins that could not be identified to group). The fish that lost their tags were not significantly different in size compared to the tagged fish on the dates of the first, or second tagging (Multiple analysis of variance including tag loss or not, photoperiod and fish origin as independent variables; PN0.1). Of the remaining 596 tagged fish, 159 had lost their tags until July 14 or their tag codes were impossible to read. In January, at the termination of the experiment, 447 fish were alive, but 182 had lost their tags or were rejected because of error reading of codes. Based on visual observations, one reason for the high tag loss was that the sharp edges of the tags made them work their way out of the skin of the fish. 2.4. Feeding The fish were fed commercial dry pellets (Skretting) in excess by automatic feeders. Feeding was 10 h day 1 with 6-min intervals and coincided with the last 10 h of each photoperiod, in both fresh- and seawater until late July, and during daytime for the rest of the experiment. The dark period started at 18:00 under all light regimes. 2.5. Temperatures The freshwater temperature increased from 6.5 to 12.6 8C during the experiment (Fig. 1). The seawater (salinity: 34–35x) temperature was very stable around 9 8C until
Fig. 2. Proportions of upper modal group fish (UM) in each of the different stocks among initially (A) large (LA groups) and (B) small (SM) size groups mixed in the tanks and (C) small size groups kept in separate tanks (SS). Small letters summarises the results of a set of pairwise 22 G-tests comparing proportions of UM fish.
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late July. After being transferred to Austevoll Aquaculture Research Station the seawater temperature varied between 9 and 12 8C. As the freshwater and sea temperatures were comparable during seawater exposures (Fig. 1), except for a moderate increase in the temperature during the final period in freshwater for the SWS3 fish, the specific growth rates were not adjusted for temperature. 2.6. Statistics Multiple analysis of variance was applied to study (1) the variation in the proportion of upper modal group fish and (2) individual variation in length and (3) growth rate using length as a covariate under (3) and genetic origin, photoperiod, condition factor (during seawater phase) and date for switch to seawater (during the last period of the experiment in seawater) to classify the data (SAS Institute, GLM procedure). Student Newman–Keuls multiple tests were used to compare means of length and specific growth rates of multiple treatment groups (StatSoft, 2003). G-tests were applied to compare proportions of upper modal group fish (Sokal and Rohlf, 1981). Significance level was 0.05.
3. Results 3.1. Proportions of upper modal group fish (UM) The Dale stock generally produced the highest proportions of UM fish (Fig. 2). The Vosso stock performed comparable to Dale, as indicated by significant differences in only two out of seven possible comparisons with the Dale stock (Fig. 2). The proportions of the
Fig. 3. Correlation between the proportions and mean sizes of the upper modal group fish (UM) in the SS groups on December 4–6 (R=0.86, Pb0.001). The single observation from the Vosso stock was not included in the correlation analysis.
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upper modal group fish were clearly lower in the Hatchery stock and the Lone stock. No differences were found between these two stocks except for a lower percentage of UM Lone fish in the LD12:12 mixed tank (Fig. 2). 3.1.1. Small size group reared in separate tanks The proportions of upper modal group fish were clearly correlated to growth rate. The correlation (see Fig. 3) was increased by including stock as a categorical variable (R=0.94, P lengthb0.01, P stockb0.05). Analysis’s of variance in proportion and individual length of the UM fish demonstrated the significance of photoperiod, but also showed that stock belonging was more important (Table 2). The significant relationships between the proportions of UM fish and photoperiod (42 G-test, Pb0.5) that was seen for the Lone and the Hatchery SS groups was not significant for the Dale fish. These results may be partly explained by the good growth performance of the Dale stock, although the relationship between %UM and UM size was also seen within the Hatchery and the Lone stock (Fig. 3).
Table 2 Multiple analysis’s of variance Sal.
Model
Significant variables Date/Period
R2
P
F
(1)
F
(2)
F
(1) Pre-tagging FW %UM FW L-SS
06.12 06.12
0.94 0.36
b0.01 b0.0001
17 19
S S
32 27
P P
8 17
(2) Post-tagging FW L FW L FW SGR FW SGR SWS1 SGR SWS1 SGR SWS1 SGR FW SGR SWS2 SGR SWS2 SGR SWS1–3 SGR SW L
06–11.02 01.05 06.02–01.05 06.02–01.05a 01.05–23.05 24.05–16.06 17.06–13.07 01.05–23.05 24.05–16.06 17.06–13.07 14.07–10.01 10.01
0.28 0.40 0.49 0.55 0.43 0.46 0.29 0.35 0.64 0.40 0.59 0.52
b0.0001 b0.0001 b0.0001 b0.0001 0.06b b0.0001 b0.07b b0.01 b0.0001 b0.001 b0.0001 b0.0001
18 21 5 4 1 4 1 2 2 2 3 5
S S L L P P L S P P S S
66 115 88 91 6 23 5 8 11 10 32 53
SP P S S PC LS P
4 7 14 14 3 3 4
C PL P SWS
5 3 9 6
Var
(3)
F
P P
7 7
CS
5
SWS
8
(1) Pre-tagging: Variation in the proportion of upper modal group fish (%UM) between groups and variation in individual length (L-SS) of the upper modal group. %UM=arcsin transformed proportions of the upper modal group fish among the SS groups of the Lone, Dale and Hatchery stock, and L-SS is the length of these UM fish. (2) Post-tagging: Analysis of individual length (L) and specific growth rates (SGR) in fresh- and seawater (see Fig. 1) using multiple analysis of variance. Squared correlation (R 2), significance level ( P) and F-values for model and for significant variables ranged after their F-value are given. FW=freshwater, SWSn=seawater switch group n, C=condition factor, L=individual length at the start of each period, P=photoperiod, S=stock and SWS=date for seawater switch (only included as a category variable for the last period in seawater). Sal.=salinity and seawater switch group. a Replicates of N1 and N2 are treated separately. b ns.
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The initial size differences between the SM and LA groups (approx. 5 mm) also contributed to the variation. The proportion of UM fish in the LA groups were significantly higher compared with the corresponding SM groups under each of the photoperiods LD10:14, LD12:12 and LD14:10, except for the Dale stock under LD14:10 (pairwise G-tests; Pb0.05). 3.2. Individual growth rates in freshwater Genetic origin and individual length, which were partly linked because all groups overlapped in size at the start of the experiment in September, were of most importance for individual variation in growth rates and overruled the effect of photoperiod in freshwater from February to May. During this period the size difference between the Dale and the Vosso stock became significant, resulting in significant differences between all stocks in May (DaleNVossoNHatcheryNLone; Fig. 4). The genetic background of the fish were more important than photoperiod for individual variation in length on February 6–11 and May 1 (shown by the ranking of
Fig. 4. Mean length of the stocks at tagging on February 6–11, on May 1 and at the end of the experiment on January 10. Standard error of means and numbers of fish are shown. Small letters show results of multiple tests of means of stocks. Equal lettering denotes not significant difference between groups. The stocks are presented because multiple tests comparing means of all treatment groups (all stocks vs. photoperiods and SWS1–3) did not show significance within stocks for photoperiod and date for seawater switch for any of the three dates.
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significant variables in Table 2) and most comparisons between the stocks were significant in February and early May (Fig. 4). The individual fork length in February was the most important factor explaining individual variation in specific growth rates from February to May, followed by stock and photoperiod (Table 2). The SNP-11 treatment group grew significantly slower than three of the four other photoperiods (Fig. 5) due to a lower growth rate of one of the two replicates under SNP-11 (0.54 vs. 0.63% day 1). During the next period in freshwater (May 1–23), no significant differences in growth rates were found between photoperiods (Table 2, Fig. 5B), but genetic origin still contributed to individual differences in growth rates (Table 2). 3.3. Growth rates in seawater 3.3.1. First period in seawater Specific growth rates dropped during the first weeks of seawater rearing, but reached levels of growth comparable to or higher than those of freshwater after more than 3 weeks (Figs. 5 and 6). Fish held under simulated natural photoperiod in freshwater grew better in running seawater than the fish previously reared under constant photoperiods, and the preexposure photoperiod contributed most to the total variation in individual growth rates during the drop, during which stock and length did not seem to influence growth rates (Stock and Length was not significant variables in the analysis of variance the first weeks in seawater; Table 2). For the different exposure dates and rearing periods in seawater, the SNP-15 treatment group grew at a comparable or significantly higher rate than the SNP-11 group (Fig. 5). Within the constant photoperiod groups, the LD12:12 group generally had the highest growth rates in the early seawater phase, especially compared with the LD10:14 group that showed the slowest growth rate in all but one period (Fig. 5). 3.3.2. Prolonged growth in seawater The immediate effect of the photoperiods on growth rate in seawater (as described above) was temporary or changed with time. Photoperiod affected growth rates significantly (Table 2), but the effect was partly reversed compared to the early seawater phase as the shortest constant photoperiod groups had a high growth rate, especially compared to SNP-15 (Figs. 5 and 7), and photoperiod did not significantly affect individual variation in final sizes (Fig. 4, Table 2). Genetic background was the most important parameter influencing growth rates (Table 2). The major reason was significantly lower growth rates (Fig. 7), and also lower final mean size (Fig. 4), of the Lone fish compared to the other stocks. With declining growth rates of the treatment groups of the Lone stock, from three to all except one comparisons with the treatment groups of the other stocks were significant (Fig. 7). There were no significant differences within the stocks, or between the Dale, Vosso and the Hatchery stock. Because of the slower growth of the fish of the Lone stock, and their contribution of these fish to total variation, the Lone post-smolts are excluded from the mean specific growth rates of the treatment groups during the last period of measurement in Fig. 5 to better visualise the effect of photoperiod. For this period the effect of the exposure dates also contributed to the analysis of variance (Table 2), but its effect did not vary systematically as the fish of SWS1 and SWS3 (1.12% day 1 for both) grew faster
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Fig. 5. Specific growth rates of SWS1 (A), SWS2 (B) and SWS3 (C). Salinity is given for each period (FW or SW). Small letters gives significances of multiple tests comparing group means. Standard errors of means are shown. The mean growth rates from February 15 to May 1 are added in (B). Note that the scaling of the X-axis is different for the last period (July 14–January 10), which covers a longer period of time. The Lone stock is not included in the last period, see text for explanation.
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Fig. 6. Percentage change in specific growth rate from freshwater (FW) to seawater (SW) for all treatment groups. The number of weeks (W) is approximated using date for exposure to seawater as zero point. The growth in freshwater from May 1–23 is used as baseline for all calculations except that the May 24–June 16 is used for SWS3.
than SWS2 (1.06% day 1) (SWS1 vs. SWS2, t-tests; Pb0.05, SWS2 vs. SWS3, P=0.06). When comparing the means of the growth rates of all treatment groups during the last period in seawater (multiple test; stocks, photoperiods, SWS1–3) no significant effects of
Fig. 7. Specific post-smolt growth rates in seawater during part B of the experiment. The data are split into stocks and photoperiod treatments. Small letters give results of multiple test comparing means of all groups, while capital letters show result of multiple test within stocks (statistical significances found only within the Dale stock).
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Fig. 8. Condition factor during SWS1 (A), SWS2 (B) and SWS3 (C). Salinity is given for each date of measurement (FW or SW). Small letters gives significance of multiple tests comparing group means. Standard errors of means are shown.
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date for seawater switch were found within the stocks, thereby allowing for the presentation of these data shown in Fig. 7. 3.4. Condition factor The switches to seawater were accompanied by a reduction in condition factor (Fig. 8), and a negative, but weak, correlation between mean condition factor and the subsequent mean growth rate in seawater (SWS1: Regression analysis, Pb0.05, R 2=0.85, F=17.1). This relationship was also valid at the individual level, resulting in a significant interaction between photoperiod and condition factor (Table 2). After 7 to 11 weeks in seawater, this relationship was reversed, and the best of the SWS1 growing groups also generally had the highest mean condition factors at the start of that period (Regression analysis, Pb0.05, R 2=0.83, F=14.3). The main reasons for these significances was the tendency for SWS1, and clearer result for SWS2, that the fish under simulated natural photoperiod had lower condition factor prior to sea water switch, and higher condition factor after 7–10 weeks in seawater compared with fish held at constant photoperiod (Fig. 8).
4. Discussion Photoperiod is known to influence freshwater growth rate and the proportion of upper modal group fish (Knutsson and Grav, 1976; Komourdjian et al., 1989; Stefansson et al., 1989, 1991; Skilbrei et al., 1997), smolting (Bjo¨rnsson et al., 1989; Berge et al., 1995) and subsequent growth rate in seawater (Saunders et al., 1985). In the present study, genetic origin was clearly more important than photoperiod during the freshwater phase, probably because the stocks used were different with respect to life-history parameters as growth rate and smolt size. The Dale stock showed the best performance with respect to the proportion and size of upper modal group fish, while the Lone stock developed more slowly than the other stocks. Despite these differences, there was no reason to assume that the size threshold (Elson, 1957; Kristinsson et al., 1985; Skilbrei, 1991) for responding to the reduction in photoperiod (from LD24:0 to LD10:14–LD16:8) did vary between the stocks. The results can be more easily explained by the observed relationship between growth rate and the probability of entering the upper size mode, which favoured the Dale fish because of their higher growth rate. The Hatchery stock improved its relative performance in seawater. The proportion of upper modal group fish in freshwater was comparable to the Lone stock, but the Lone stock was the only stock deviating significantly in size from the other stocks after 6 months in seawater. The lower growth rate in seawater of the Lone fish probably reflects the characteristics of this small sized grilse stock in the wild. Inherent ecological adaptations may therefore add significant variance to measurements of individual growth rates under experimental conditions in fresh- and seawater. The abrupt drop in growth after seawater exposure, which was common for all stocks, was in accordance with the observation of Stradmeyer et al. (1991) that the appetite of smolts is severely reduced after transfer to seawater and also similar to the results of
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Damsga˚rd and Arnesen (1998) who demonstrated that the drop in feed intake after seawater transfer was not related to weight, feed intake or growth rate in freshwater. The finding that photoperiod showed its most significant influence on growth rates shortly after seawater exposures is probably linked to two mechanisms. Increasing photoperiod may stimulate growth rate directly, or indirectly by stimulating smoltification. The hypoosmoregulatory ability has probably been better developed for fish experiencing natural photoperiod in spring as increasing photoperiod is known to stimulate and synchronise the smoltification process (Saunders and Henderson, 1970; McCormick et al., 1987). Further, condition factor is lowered during smoltification (Hoar, 1988). The condition factors of the smolts raised under natural photoperiods were lower at seawater exposures and higher after 6 weeks in seawater compared with the constant photoperiod groups, which indicate that they had an improved physiological status at that time. In support of this, they also grew faster during this period. Increasing photoperiod stimulates growth (Komourdjian et al., 1989; Stefansson et al., 1991; Saunders et al., 1994) and high growth rates may be beneficial during the challenge to adapt to the marine environment when the smolts are highly responsive to stress (Carey and McCormick, 1989). When comparing growth rates in fresh- and seawater it is important to establish whether smoltification implies that the smolt develops the ability to grow at the same rate in seawater as it did in freshwater, or if smoltification itself is characterised by an increase in growth rate. Growth hormone stimulates hypo-osmoregulatory ability (Sakamoto et al., 1994) and environmental salinity increase stimulates plasma growth hormone levels and triggers the final development of hypo-osmoregulatory ability (Schmitz et al., 1994). However, Bjo¨rnsson et al. (1998) speculates whether this transient increase in circulating growth hormone levels represents a specific short-term hypoosmoregulatory role of GH. In the present study, the constant photoperiod groups reached acceptable growth rates, i.e. comparable to those in freshwater, after more than 3 weeks in seawater. When taken into account that they grew at least as rapidly as the natural photoperiod groups for the next months, it is difficult to conclude that they were less smoltified if we assume that such differences affect post-smolt growth rates. The good performance of the constant photoperiod groups in seawater may be an example of a match between the timing of the exposures and circannual rhythms influencing seawater tolerance (Eriksson and Lundqvist, 1982), but was not expected as an increase in photoperiod is regarded as a prerequisite for normal development through synchronisation of the components of smolting (Duston and Saunders, 1990; Berge et al., 1995; Sigholt et al., 1995; Duncan and Bromage, 1998). The fact that the photoperiod of these groups were changed to LD22:2 when the fish were exposed to full salinity seawater complicates this picture. A change to long day is known to induce an increase in plasma growth hormone levels within 3 weeks (Bjo¨rnsson et al., 1995), a change which is accompanied by an increase in growth rate and hypoosmoregulatory ability (Bjo¨rnsson et al., 1995) and a reduction in condition factor (Bjo¨rnsson et al., 2000). It is therefore probable that the increase to LD22:2 has improved the seawater performance of the short daylength groups by stimulating smoltification and/ or growth rate. The comparable performance of the SNP-11 and SNP-15 groups in seawater raises a question of practical interest. When applying artificial photoperiods in smolt production by using a succession of a short followed by a long daylength, what would be the minimum
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winter daylength that is required for the following photo stimulated smoltification? In agreement with the present results, a daylength of 12 h or lower has been demonstrated to increase the numbers of lower modal group fish (Skilbrei et al., 1997), and therefore seems to be an effective bwinter stimulusQ for the bimodal development. At first, one may assume that the increase in photoperiod should be of the same magnitude to stimulate smoltification. However, the relatively minor effect of photoperiod relative to stock origin was probably due to the fact that all photoperiods provided an adequate stimulus to induce smolting. It would be expected that inclusion of non-stimulatory photoperiods would have had a more pronounced effect on growth after transfer to seawater. Therefore, it does not seem to be necessary to reduce the daylength during winter below 14 h. On the contrary, shorter daylengths may reduce the numbers and size of the upper modal group fish, and the time period available for feeding compared to 14–16 h of daily light will be shorter. Such relationships should, however, be studied in more detail before it is recommended to increase the minimum day length above 12 h, which has been frequently applied in Norwegian hatchery practices. The present study demonstrates the responsiveness of Atlantic salmon to photoperiod by showing alterations in growth patterns that follow from adjustments of endogenous rhythms and timing of smoltification. While the variability in growth between genetic groups was large enough to almost shade the effect of photoperiod under stable salinity, there was no evidence of a stock specific response to seawater exposures. Because of the double effect of photoperiod, to stimulate both smoltification and growth, there are several problems associated with the general interpretation of relationships between photoperiod, timing of smoltification and growth rate in seawater. The following alternatives for relationships between growth rate and seawater entry are therefore proposed. Seawater tolerance may be characterised by: (a) The minimal growth rate shortly after exposure to seawater. (b) The period used to reach pre-exposure growth rates. (c) The period used to exceed pre-exposure growth rates. One may ask whether seawater tolerance (b) and preference (c) should be distinguished from each others, implying that a smolt that tolerates seawater is able to re-establish freshwater growth rate while a fully smoltified fish shows its preference for seawater by speeding up its growth rate. The relative differences in the early seawater growth rates did reflect the photoperiod regimes, but the data also illustrate the need in this type of experiments to study the performance in seawater over several months as photoperiod manipulations may have long-term consequences for the growth pattern of Atlantic salmon.
Acknowledgement We thank Gunnar Bakke and Viktor Solbakken for practical assistance during the experiment. The Norwegian Research Council and the Institute of Marine Research
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provided financial support. Salar 2lvik provided one group of experimental fish. We are grateful for the helpful pieces of advice from the anonymous referees, which evidently improved the paper.
References Berge, 2.I., Berg, A., Fyhn, H.J., Barnung, T., Hansen, T., Stefansson, S.O., 1995. Development of salinity tolerance in underyearling smolts of Atlantic salmon (Salmo salar) reared under different photoperiods. Can. J. Fish. Aquat. Sci. 52, 243 – 251. Bjo¨rnsson, B.Th., Thorarensen, H., Ogasawara, T., Kristinsson, J.B., 1989. Photoperiod and temperature affect plasma growth hormone levels, growth condition factor and hypoosmoregulatory ability of juvenile Atlantic salmon (Salmo salar) during parr–smolt transformation. Aquaculture 82, 77 – 91. Bjo¨rnsson, B.Th., Stefansson, S.O., Hansen, T., 1995. Photoperiod regulation of plasma growth hormone levels during parr–smolt transformation of Atlantic salmon: implications for hypoosmoregulatory ability and growth. Gen. Comp. Endocrinol. 100, 73 – 82. Bjo¨rnsson, B.Th., Stefansson, G.V., Berge, 2.I., Hansen, T., Stefansson, S.O., 1998. Circulating growth hormone levels in Atlantic salmon smolts following seawater transfer: effects of photoperiod regime, salinity, duration of exposure and season. Aquaculture 168, 121 – 137. Bjo¨rnsson, B.Th., Hemre, G.-I., Bjbrnevik, M., Hansen, T., 2000. Photoperiod regulation of plasma growth hormone levels during induced smoltification of underyearling Atlantic salmon. Gen. Comp. Endocrinol. 119, 17 – 25. Carey, J.B., McCormick, S.D., 1989. Atlantic salmon smolts are more responsive to an acute handling and confinement stress than parr. Aquaculture 168, 237 – 254. Damsg3rd, B., Arnesen, A.M., 1998. Feeding, growth and social interactions during smolting and seawater acclimation in Atlantic salmon, Salmo salar L.. Aquaculture 168, 7 – 16. Duncan, N.J., Bromage, N., 1998. The effect of different periods of constant short days on smoltification in juvenile Atlantic salmon (Salmo salar). Aquaculture 168, 369 – 386. Duncan, N.J., Auchinachie, N., Robertson, D., Murray, R., Bromage, N., 1998. Growth, maturation and survival of out-of-season 0+ and 1+ Atlantic salmon (Salmo salar) smolts. Aquaculture 168, 325 – 339. Duncan, N.N., Mitchell, D., Bromage, N., 1999. Post-smolt growth and maturation of out-of-season 0+ Atlantic salmon (Salmo salar) reared under different photoperiods. Aquaculture 176, 237 – 244. Duston, J., Saunders, R.L., 1990. The entrainment role of photoperiod on hypoosmoregulatory and growth related aspects of smolting in Atlantic salmon (Salmo salar). Can. J. Zool. 68, 707 – 715. Duston, J., Saunders, R.L., 1995. Advancing smolting to autumn in age 0+ Atlantic salmon by photoperiod, and long-term performance in sea water. Aquaculture 135, 295 – 309. Elson, P., 1957. The importance of size in the change from parr to smolt in Atlantic salmon. Can. Fish Cult. 21, 1 – 6. Eriksson, L.-H., Lundqvist, H., 1982. Circannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon (Salmo salar L.). Aquaculture 28, 113 – 121. Folmar, L.C., Dickhoff, W.W., 1980. The parr smolt transformation (smoltification) and seawater transformation in salmonids. A review of selected literature. Aquaculture 21, 1 – 37. Handeland, S.O., Stefansson, S.O., 2001. Photoperiod control and influence of body size on off-season parr– smolt transformation and post-smolt growth. Aquaculture 192, 291 – 307. Hanke, A.R., Friars, G.W., Saunders, R.L., Terhune, J.M., 1989. Family x photoperiod interaction on growth in juvenile Atlantic salmon, Salmo salar. Genome 32, 1105 – 1112. Hoar, W.S., 1988. The physiology of smolting salmonids. In: Hoar, W.S., Randall, D.J. (Eds.), Fish Physiology, vol. XIB. Academic Press, New York, NY, pp. 275 – 343. Ja¨rvi, T., 1990. Cumulative acute physiological stress in Atlantic salmon smolts: the effect of osmotic imbalance and the presence of predators. Aquaculture 89, 337 – 350. Knutsson, S., Grav, T., 1976. Seawater adaptation in Atlantic salmon (Salmo salar L.) at different experimental temperatures and photoperiods. Aquaculture 8, 169 – 187.
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Komourdjian, M.P., Fenwick, J.C., Saunders, R.L., 1989. Endocrine-mediated photostimulation of growth in Atlantic salmon. Can. J. Zool. 67, 1505 – 1509. Kristinsson, J.B., Saunders, R.L., Wiggs, A.J., 1985. Growth dynamics during the development of bimodal length–frequency distribution in Atlantic salmon (Salmo salar L.). Aquaculture 45, 1 – 20. Lubin, R.T., Rourke, A.W., Saunders, R.L., 1991. Influence of photoperiod on the number and ultrastructure of gill chloride cells of the Atlantic salmon (Salmo salar) before and during smoltification. Can. J. Fish. Aquat. Sci. 48, 1302 – 1307. McCormick, S.D., Saunders, R.L., 1987. Preparatory physiological adaptations for marine life of salmonids: osmoregulation, growth and metabolism. Am. Fish. Soc. Symp. 1, 221 – 229. McCormick, S.D., Saunders, R.L., Henderson, E.B., Harmon, P.R., 1987. Photoperiod control of parr–smolt transformation in Atlantic salmon (Salmo salar): changes in salinity tolerance, gill Na+, K+-ATPase activity, and plasma thyroid hormones. Can. J. Fish. Aquat. Sci. 44, 1462 – 1468. N&vdal, G., 1983. Genetic Factors in Connection With Age at Maturation. Rourke, A.W., Saunders, R.L., Harmon, P.R., 1991. Changes in plasma protein patterns in smolting Atlantic salmon, Salmo salar L., are not dependent on changed growth rates. J. Fish Biol. 39, 35 – 43. Sakamoto, T., Hirano, T., McCormick, S.D., Madsen, S.S., Nishioka, R.S., Bern, H.A., 1994. Possible mode of seawater-adapting actions of growth hormone in salmonids. Aquaculture 121, 1 – 3. Saunders, R.L., Henderson, E.B., 1970. Influence of photoperiod on smolt development and growth of Atlantic salmon (Salmo salar). J. Fish. Res. Board Can. 25, 2387 – 2401. Saunders, R.L., Duston, J., Benfey, T.J., 1994. Environmental and biological factors affecting growth dynamics in relation to smolting of Atlantic salmon, Salmo salar L.. Aquac. Fish. Manage. 25, 9 – 20. Saunders, R.L., Henderson, E.B., Harmon, P.R., 1985. Effects of photoperiod on juvenile growth and smolting of Atlantic salmon and subsequent survival and growth in sea cages. Aquaculture 45, 55 – 66. Schmitz, M., Berglund, I., Lundqvist, H., Bjo¨rnsson, B., 1994. Growth hormone response to seawater challenge in Atlantic salmon, Salmo salar, during parr–smolt transformation. Aquaculture 121, 1 – 3. Sigholt, T., Staurnes, M., Jakobsen, H.J., Aasgaard, T., 1995. Effects of continuous light and short-day photoperiod on smolting, seawater survival and growth in Atlantic salmon (Salmo salar). Aquaculture 130, 373 – 388. Skilbrei, O.T., 1991. Importance of threshold length and photoperiod for the development of bimodal length– frequency distribution in Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 48, 2163 – 2172. Skilbrei, O.T., Holm, M., Jbrstad, K., Handeland, S.O., 1994. Migration motivation of cultured Atlantic salmon, Salmo salar L., smolts in relation to size, time of release and acclimatization period. Aquac. Fish. Manage. 25, 65 – 77. Skilbrei, O.T., Jbrstad, K., Holm, M., Farestveit, E., Grimnes, A., Aardal, L., 1994. A new release system for coastal ranching of Atlantic salmon (Salmo salar) and behavioural patterns of released smolts. Nordic J. Freshw. Res. 69, 84 – 94. Skilbrei, O.T., Hansen, T., Stefansson, S.O., 1997. Effects of decreases in photoperiod on growth and bimodality in Atlantic salmon (Salmo salar). Aquacult. Res. 28, 43 – 49. Sokal, R.R., Rohlf, J.F., 1981. Biometry. W.H. Freeman, New York. 859 pp. StatSoft, 2003. STATISTICA (data analysis software system), version 6. www.statsoft.com. Stefansson, S.O., N&vdal, G., Hansen, T., 1989. The influence of three unchanging photoperiods on growth and parr–smolt transformation in Atlantic salmon, Salmo salar L.. J. Fish Biol. 35, 237 – 247. Stefansson, S.O., Bjo¨rnsson, B.T., Hansen, T., Haux, C., Taranger, G.L., Saunders, R.L., 1991. Growth, parr– smolt transformation and changes in growth hormone of Atlantic salmon (Salmo salar) reared under different photoperiods. Can. J. Fish. Aquat. Sci. 48, 2100 – 2108. Stradmeyer, L., DePauw, N., Joyce, J., 1991. The effects of seawater transfer on the feeding and survival of smolts reared in sea cage and tank environments. Spec. Publ. Eur. Aquacult. Soc. 14, 306 – 307. Thrush, M.A., Duncan, N.J., Bromage, N.R., 1994. The use of photoperiod in the production of out-of-season Atlantic salmon (Salmo salar) smolts. Aquaculture 121, 29 – 44. Villarreal, C.A., Thorpe, J.E., Miles, M.S., 1988. Influence of photoperiod on growth changes in juvenile Atlantic salmon (Salmo salar). J. Fish Biol. 33, 15 – 30.
Effects of pre-smolt photoperiod regimes on post-smolt growth rates of different genetic groups of Atlantic salmon (Salmo salar) Ove Tommy Skilbreia,*, Tom Hansenb a Institute of Marine Research, P.O.B. 1870, N-5024 Bergen-Nordnes, Norway Matre Aquaculture Research Station, Institute of Marine Research, N-5198 Matredal, Norway
b
Received 21 February 2004; received in revised form 9 September 2004; accepted 13 September 2004
Abstract The aim was to study relationships between photoperiod in freshwater and growth rates prior to and following seawater exposures for fish from different stocks. Individually tagged 1+juveniles originating from four different stocks of Atlantic salmon were reared under the constant photoperiods LD10:14, LD12:12, LD14:10 and LD16:8 and under simulated natural increasing photoperiods from early spring starting from LD11:13 (SNP-11; fish from LD10:14 and LD12:12) or from LD15:9 (SNP-15; fish from LD14:10 and LD16:8). The groups were exposed to running seawater during May and June under LD22:2 and transferred to natural light regime in late July to monitor the subsequent growth rates in seawater for the next 6 months. The genetic origin of the fish was the factor of most influence for variation in the proportion and growth rates of the upper modal group fish in freshwater. The Dale stock showed the best growth performance, followed by the Vosso, Hatchery and the Lone stock. During the first 3–6 weeks in seawater, there was an evident and common drop in growth rates for all the stocks. The largest part of the variation in growth could be attributed to pre-smolt photoperiods, as the drop in growth rates was less pronounced for the fish previously held under increasing photoperiod in freshwater. During the next 5 months in seawater, the significance of stock was partly re-established. The Dale, Vosso and Hatchery stocks reached comparable sizes, significantly larger than the Lone stock. In addition, the initially slow growing groups under constant photoperiod in freshwater grew at the highest rate resulting in no differences in final sizes between treatment groups, possibly implying that their
* Corresponding author. Tel.: +47 55236894; fax: +47 55236891. E-mail address: [email protected] (O.T. Skilbrei). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.09.017
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transfer to long daylength in seawater stimulated growth and/or completed the smoltification process. Relationships between photoperiod in freshwater, smoltification and growth rate before and after seawater exposure are discussed. D 2004 Elsevier B.V. All rights reserved. Keywords: Atlantic salmon; Smoltification; Growth; Photoperiod
1. Introduction Atlantic salmon smoltify naturally under increasing photoperiod in spring. Photoperiod influences pituitary cytology (Komourdjian et al., 1989), timing of smoltification and the development of hypoosmoregulatory ability of Atlantic salmon (Sigholt et al., 1995; Duston and Saunders, 1990; Stefansson et al., 1991). The smoltification process is partly under endogenous control and annual rhythms have been observed under constant photoperiod regimes (Eriksson and Lundqvist, 1982). Photoperiod also influences the growth rate by stimulating growth under increasing and long daylengths (Villarreal et al., 1988; Bjo¨rnsson et al., 1989). Short daylengths during the first winter in freshwater may reduce growth rates and decrease the proportion of 1-year smolts (Skilbrei, 1991; Skilbrei et al., 1997). It is generally believed that, in hatchery 0+ and 1+ smolt production, a shortening followed by an increase in daylength stimulate smoltification (Berge et al., 1995). As it is beneficial to maximise growth during the freshwater phase, and also to ensure a proper smoltification process, it is of interest for salmonid culture to study relationships between photoperiod, proportion of the upper modal size group, growth rate and parr–smolt transformation to find the best compromise between freshwater growth and smoltification. Smoltification is characterised by a large number of morphological, biochemical, physiological and behavioural changes (Folmar and Dickhoff, 1980; McCormick and Saunders, 1987; Hoar, 1988). The parr–smolt transformation can be measured at different levels. Measurements of enzymatic and physiological mechanisms involved in hypoosmotic regulation are indicative of the onset and development of seawater tolerance (Hoar, 1988, Duston and Saunders, 1990; Rourke et al., 1991; Lubin et al., 1991). The effects of these mechanisms and the degree of parr–smolt transformation may be evaluated by plasma ion concentrations after exposure to seawater. Such measurements are usually performed shortly after the exposure to a higher salinity. A drawback with these methods is that they do not distinguish between seawater tolerance and preference. A fish may be able to regulate its plasma ions, but it is still a question whether the smolt has reached a level of adaptation that enables it to thrive in the marine environment. The nature of the challenge may depend on the purpose of the smolt production; for cage rearing or sea ranching. After the time of seawater entry, the development of a hypo-osmoregulatory ability is only one of the challenges for a released smolt to survive in the wild. It also has to be able to feed, and it may experience accumulated stress because of osmotic imbalance in addition to the presence of predators (Ja¨rvi, 1990) when organising into migrating schools (Skilbrei et al., 1994a,b). To cope with these problems, a fully smoltified fish must be capable of gaining surplus energy shortly after seawater entry. If fish which have not completed the parr–
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smolt transformation grow slower in seawater than those fish that are fully smoltified, measurements of individual growth rates after exposure to seawater may be a good indicator of relative differences in seawater tolerance between treatment groups (Thrush et al., 1994; Duston and Saunders, 1995; Duncan et al., 1998; Handeland and Stefansson, 2001). The growth rates may be of interest during two stages: shortly after seawater transfer, and also after prolonged stay to see whether the poorly growing fish adapt or not. If growth rate is used as an indirect indicator of smoltification or general welfare, then other causes for variation in growth rates should also be considered. Growth rates in freshwater prior to seawater exposure may differ between treatment groups and may therefore have an impact on subsequent performance (Duncan et al., 1998, 1999). Further, there is a high degree of individual variance in quantitative traits such as growth rates which in part can be explained by genetics (Nævdal, 1983; Hanke et al., 1989). If seawater tolerance and growth rate are linked, will then genetic differences in growth potential influence the response to seawater exposure? Alternatively, there may be genetic components influencing adaptation to seawater regardless of earlier growth rate. The aim of the present work was to compare growth rates of individually tagged smolts of different stocks of Atlantic salmon from the freshwater phase when they were reared under different photoperiods, through smoltification until the post-smolt stage in seawater.
2. Materials and methods 2.1. Experimental fish 0+ family offspring from wild parents originating from the Lone River grilse stock (location of river mouth: N 60852VE 5849V) and the multi-sea-winter stocks of River Dale (N 60858VE 5878V) and Vosso River (N 60864VE 5896V) were first fed in March and reared in separate tanks at Sagen Hatchery under continuous light until September. The wild parents were included in a larger screening of microsatelitte DNA in the three rivers. According to K. Glover (Institute of Marine Research) clear genetic distances between the rivers were observed. 0+ juveniles from a hatchery stock (BP Salar 2lvik) (the third generation held in captivity) were also included. To establish groups of equal size at the start of the experiment, only fish ranging between 70 and 81 mm (mean varied from 74 to 76 mm) were selected for the experiment and transferred to the Institute of Marine Research (N 60840V, E 5831V). This length range was chosen because other studies have shown that fish of this size have responded very clearly to photoperiod adjustments by altering growth rates and proportions of the upper mode sized fish (Skilbrei et al., 1997). In addition, repeated selection at different dates of fish of 70–80 mm from a basic group have shown very similar results (Skilbrei, 1991), indicating that the relative differences in growth prior to the photoperiod adjustments had a minor effect for the further development of bimodality in this length group. Therefore, one intention for using selected length groups was to minimise the possible effects of different selection intensities among the stocks. Prior to the experiment, 38% of the Lone fish in the tanks at Sagen Hatchery were within the 70–81 mm length interval, 24% were larger. The corresponding proportions for the Dale and the Vosso stocks were 38% and 53%, and 22% and 66%, respectively. The
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fish was further divided into two new length groups; one of 70–74 mm (n=771) and one of 75–81 mm fork length (n=821). The initial size groups and stocks were identified by a combination of fin clips and dye marking. 2.2. Experimental design 2.2.1. Part A—indoor rearing at the Institute of Marine Research (Fig. 1) Photoperiods were LD24:0 prior to, and LD10:14, LD12:12, LD14:10 or LD16:8 after the start of the experiment on September 19. The source of illumination was 215 W fluorescent tubes providing 2.1–3.4 W m 2 10 cm below surface and 1.5–2.2 W m 2 at the bottom of the covered rectangular 180 l fibreglass tanks (LI-COR LI1000 Underwater Sensor). One-half of the smallest fish (70–74 mm) were reared in separate tanks (SS groups) under each photoperiod (22–34 individuals per stock per tank), while the rest of the small fish were mixed in the tanks (SM groups) with the large fish (75–81 mm, LA groups). Due to a lower number of Vosso fish (410 vs. 679–839) they were not included in all treatment groups. Statistical comparisons of the differences in the proportions of upper modal group fish in the mixed tanks were done within, but not between, the photoperiods. The reasons are that the density of fish was 30% higher in the mixed LD10:14 tank for the first week of the experiment and that 35% of the fish in the mixed LD16:8 tank died after 8 days due to a temporary reduction in the supply of water. These circumstances may have enlarged the effects of photoperiod.
Fig. 1. Temperature regimes (A) and experimental set-up (B) during part A of the experiment. Arrows show time for change of photoperiods and switches of salinity from fresh- to seawater (SWS1–3). Constant photoperiods are LD10:14 (LightDark10:14), LD12:12, LD14:10, LD16:8, LD22:2 and LD24:0. The simulated natural photoperiods starts at LD11:13 (SND-11) and at LD15:9 (SNP-15). M=date of measurement. T=date of tagging.
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Two new photoperiods were started on February 12. Samples of fish from LD10:14 and LD12:12 were distributed in two tanks (replicates) and given simulated natural photoperiod (SNP-11) starting at 11 h day 1 while fish from LD14:10 and all fish from LD16:8 were reared in two tanks (replicates) under simulated photoperiod starting at 15 h day 1 (SNP-15, see experimental set-up, Fig. 1). Number of fish in the seven tanks varied between 75 and 108 individuals (Table 1). On May 1, May 25 and June 16 fish from the seven tanks were mixed randomly in new tanks and exposed to running seawater under LD22:2 by switching the water supply from fresh- to seawater (seawater switch 1, 2 and 3; SWS1, SWS2 and SWS3, see Fig. 1). 2.2.2. Part B—outdoor rearing at Austevoll Aquaculture Research Station On July 25, when all groups had been held in seawater for at least 5 weeks, the fish were transferred to the Austevoll Aquaculture Research Station (N 60809V, E 5826V) to be reared outdoor under natural photoperiod in two 3 m diameter circular tanks supplied with seawater (pumped deep water) until January 10, when the experiment was ended. 2.3. Measurements and tagging of fish All fish were anaesthetized (Metomidate), and weight (F0.01 g) and fork length (F1 mm) were measured at the start of the experiment, to record bimodality in late autumn, at tagging, the day before each seawater exposure, 3–4 weeks after a seawater exposure and Table 1 Numbers of individually tagged fish from the different stocks held under the different photoperiods Stock
Period: H D L V SUM
Photoperiods LD10:14 (n)
LD12:12 (n)
LD14:10 (n)
SNP-11
Feb–May 11 6 6 10 29
2 8 5 7 22
11 13 13
7 8 8 11 34
26 25 20 28 99
May 1 (+re-tagged) H 24 D 20 L 18 V 21 SUM 83
14 25 18 18 75
January H D L V SUM
4 17 7 8 36
10 10 5 6 10 31
37
26 24 25 75
11 16 10 36
17 23 14 26 80
H=Hatchery, D=River Dale, L=River Lone and V=River Vosso. a Replicate tank.
SNP-11a (n)
SNP-15 (n)
SNP-15a (n)
4 8 13 11 36
6 15 10 3 34
7 12 12 4 35
25 30 34 19 108
23 25 24 7 79
23 25 23 6 77
17 34 18 7 76
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at the end of the experiment; September 19, December 4–6, February 6–11, May 1, May 23–24, June 16–17, July 13–14 (see Fig. 1) and January 10. All strains developed bimodality during autumn. From February 6–11 parr assumed not to smolt the following spring (lower modal group; based on bimodal length– frequency distributions) were removed, and remaining pre-smolts were individually tagged with Visible Implant Tags (VIT). Of the 617 individuals tagged with Visible Implant Tags (VIT) in February, 607 were alive in May but 367 had lost their tags (20 to 37 fish in each tank). These fish were re-tagged on May 1 (except 15 individuals with regenerated fins that could not be identified to group). The fish that lost their tags were not significantly different in size compared to the tagged fish on the dates of the first, or second tagging (Multiple analysis of variance including tag loss or not, photoperiod and fish origin as independent variables; PN0.1). Of the remaining 596 tagged fish, 159 had lost their tags until July 14 or their tag codes were impossible to read. In January, at the termination of the experiment, 447 fish were alive, but 182 had lost their tags or were rejected because of error reading of codes. Based on visual observations, one reason for the high tag loss was that the sharp edges of the tags made them work their way out of the skin of the fish. 2.4. Feeding The fish were fed commercial dry pellets (Skretting) in excess by automatic feeders. Feeding was 10 h day 1 with 6-min intervals and coincided with the last 10 h of each photoperiod, in both fresh- and seawater until late July, and during daytime for the rest of the experiment. The dark period started at 18:00 under all light regimes. 2.5. Temperatures The freshwater temperature increased from 6.5 to 12.6 8C during the experiment (Fig. 1). The seawater (salinity: 34–35x) temperature was very stable around 9 8C until
Fig. 2. Proportions of upper modal group fish (UM) in each of the different stocks among initially (A) large (LA groups) and (B) small (SM) size groups mixed in the tanks and (C) small size groups kept in separate tanks (SS). Small letters summarises the results of a set of pairwise 22 G-tests comparing proportions of UM fish.
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late July. After being transferred to Austevoll Aquaculture Research Station the seawater temperature varied between 9 and 12 8C. As the freshwater and sea temperatures were comparable during seawater exposures (Fig. 1), except for a moderate increase in the temperature during the final period in freshwater for the SWS3 fish, the specific growth rates were not adjusted for temperature. 2.6. Statistics Multiple analysis of variance was applied to study (1) the variation in the proportion of upper modal group fish and (2) individual variation in length and (3) growth rate using length as a covariate under (3) and genetic origin, photoperiod, condition factor (during seawater phase) and date for switch to seawater (during the last period of the experiment in seawater) to classify the data (SAS Institute, GLM procedure). Student Newman–Keuls multiple tests were used to compare means of length and specific growth rates of multiple treatment groups (StatSoft, 2003). G-tests were applied to compare proportions of upper modal group fish (Sokal and Rohlf, 1981). Significance level was 0.05.
3. Results 3.1. Proportions of upper modal group fish (UM) The Dale stock generally produced the highest proportions of UM fish (Fig. 2). The Vosso stock performed comparable to Dale, as indicated by significant differences in only two out of seven possible comparisons with the Dale stock (Fig. 2). The proportions of the
Fig. 3. Correlation between the proportions and mean sizes of the upper modal group fish (UM) in the SS groups on December 4–6 (R=0.86, Pb0.001). The single observation from the Vosso stock was not included in the correlation analysis.
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upper modal group fish were clearly lower in the Hatchery stock and the Lone stock. No differences were found between these two stocks except for a lower percentage of UM Lone fish in the LD12:12 mixed tank (Fig. 2). 3.1.1. Small size group reared in separate tanks The proportions of upper modal group fish were clearly correlated to growth rate. The correlation (see Fig. 3) was increased by including stock as a categorical variable (R=0.94, P lengthb0.01, P stockb0.05). Analysis’s of variance in proportion and individual length of the UM fish demonstrated the significance of photoperiod, but also showed that stock belonging was more important (Table 2). The significant relationships between the proportions of UM fish and photoperiod (42 G-test, Pb0.5) that was seen for the Lone and the Hatchery SS groups was not significant for the Dale fish. These results may be partly explained by the good growth performance of the Dale stock, although the relationship between %UM and UM size was also seen within the Hatchery and the Lone stock (Fig. 3).
Table 2 Multiple analysis’s of variance Sal.
Model
Significant variables Date/Period
R2
P
F
(1)
F
(2)
F
(1) Pre-tagging FW %UM FW L-SS
06.12 06.12
0.94 0.36
b0.01 b0.0001
17 19
S S
32 27
P P
8 17
(2) Post-tagging FW L FW L FW SGR FW SGR SWS1 SGR SWS1 SGR SWS1 SGR FW SGR SWS2 SGR SWS2 SGR SWS1–3 SGR SW L
06–11.02 01.05 06.02–01.05 06.02–01.05a 01.05–23.05 24.05–16.06 17.06–13.07 01.05–23.05 24.05–16.06 17.06–13.07 14.07–10.01 10.01
0.28 0.40 0.49 0.55 0.43 0.46 0.29 0.35 0.64 0.40 0.59 0.52
b0.0001 b0.0001 b0.0001 b0.0001 0.06b b0.0001 b0.07b b0.01 b0.0001 b0.001 b0.0001 b0.0001
18 21 5 4 1 4 1 2 2 2 3 5
S S L L P P L S P P S S
66 115 88 91 6 23 5 8 11 10 32 53
SP P S S PC LS P
4 7 14 14 3 3 4
C PL P SWS
5 3 9 6
Var
(3)
F
P P
7 7
CS
5
SWS
8
(1) Pre-tagging: Variation in the proportion of upper modal group fish (%UM) between groups and variation in individual length (L-SS) of the upper modal group. %UM=arcsin transformed proportions of the upper modal group fish among the SS groups of the Lone, Dale and Hatchery stock, and L-SS is the length of these UM fish. (2) Post-tagging: Analysis of individual length (L) and specific growth rates (SGR) in fresh- and seawater (see Fig. 1) using multiple analysis of variance. Squared correlation (R 2), significance level ( P) and F-values for model and for significant variables ranged after their F-value are given. FW=freshwater, SWSn=seawater switch group n, C=condition factor, L=individual length at the start of each period, P=photoperiod, S=stock and SWS=date for seawater switch (only included as a category variable for the last period in seawater). Sal.=salinity and seawater switch group. a Replicates of N1 and N2 are treated separately. b ns.
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The initial size differences between the SM and LA groups (approx. 5 mm) also contributed to the variation. The proportion of UM fish in the LA groups were significantly higher compared with the corresponding SM groups under each of the photoperiods LD10:14, LD12:12 and LD14:10, except for the Dale stock under LD14:10 (pairwise G-tests; Pb0.05). 3.2. Individual growth rates in freshwater Genetic origin and individual length, which were partly linked because all groups overlapped in size at the start of the experiment in September, were of most importance for individual variation in growth rates and overruled the effect of photoperiod in freshwater from February to May. During this period the size difference between the Dale and the Vosso stock became significant, resulting in significant differences between all stocks in May (DaleNVossoNHatcheryNLone; Fig. 4). The genetic background of the fish were more important than photoperiod for individual variation in length on February 6–11 and May 1 (shown by the ranking of
Fig. 4. Mean length of the stocks at tagging on February 6–11, on May 1 and at the end of the experiment on January 10. Standard error of means and numbers of fish are shown. Small letters show results of multiple tests of means of stocks. Equal lettering denotes not significant difference between groups. The stocks are presented because multiple tests comparing means of all treatment groups (all stocks vs. photoperiods and SWS1–3) did not show significance within stocks for photoperiod and date for seawater switch for any of the three dates.
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significant variables in Table 2) and most comparisons between the stocks were significant in February and early May (Fig. 4). The individual fork length in February was the most important factor explaining individual variation in specific growth rates from February to May, followed by stock and photoperiod (Table 2). The SNP-11 treatment group grew significantly slower than three of the four other photoperiods (Fig. 5) due to a lower growth rate of one of the two replicates under SNP-11 (0.54 vs. 0.63% day 1). During the next period in freshwater (May 1–23), no significant differences in growth rates were found between photoperiods (Table 2, Fig. 5B), but genetic origin still contributed to individual differences in growth rates (Table 2). 3.3. Growth rates in seawater 3.3.1. First period in seawater Specific growth rates dropped during the first weeks of seawater rearing, but reached levels of growth comparable to or higher than those of freshwater after more than 3 weeks (Figs. 5 and 6). Fish held under simulated natural photoperiod in freshwater grew better in running seawater than the fish previously reared under constant photoperiods, and the preexposure photoperiod contributed most to the total variation in individual growth rates during the drop, during which stock and length did not seem to influence growth rates (Stock and Length was not significant variables in the analysis of variance the first weeks in seawater; Table 2). For the different exposure dates and rearing periods in seawater, the SNP-15 treatment group grew at a comparable or significantly higher rate than the SNP-11 group (Fig. 5). Within the constant photoperiod groups, the LD12:12 group generally had the highest growth rates in the early seawater phase, especially compared with the LD10:14 group that showed the slowest growth rate in all but one period (Fig. 5). 3.3.2. Prolonged growth in seawater The immediate effect of the photoperiods on growth rate in seawater (as described above) was temporary or changed with time. Photoperiod affected growth rates significantly (Table 2), but the effect was partly reversed compared to the early seawater phase as the shortest constant photoperiod groups had a high growth rate, especially compared to SNP-15 (Figs. 5 and 7), and photoperiod did not significantly affect individual variation in final sizes (Fig. 4, Table 2). Genetic background was the most important parameter influencing growth rates (Table 2). The major reason was significantly lower growth rates (Fig. 7), and also lower final mean size (Fig. 4), of the Lone fish compared to the other stocks. With declining growth rates of the treatment groups of the Lone stock, from three to all except one comparisons with the treatment groups of the other stocks were significant (Fig. 7). There were no significant differences within the stocks, or between the Dale, Vosso and the Hatchery stock. Because of the slower growth of the fish of the Lone stock, and their contribution of these fish to total variation, the Lone post-smolts are excluded from the mean specific growth rates of the treatment groups during the last period of measurement in Fig. 5 to better visualise the effect of photoperiod. For this period the effect of the exposure dates also contributed to the analysis of variance (Table 2), but its effect did not vary systematically as the fish of SWS1 and SWS3 (1.12% day 1 for both) grew faster
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Fig. 5. Specific growth rates of SWS1 (A), SWS2 (B) and SWS3 (C). Salinity is given for each period (FW or SW). Small letters gives significances of multiple tests comparing group means. Standard errors of means are shown. The mean growth rates from February 15 to May 1 are added in (B). Note that the scaling of the X-axis is different for the last period (July 14–January 10), which covers a longer period of time. The Lone stock is not included in the last period, see text for explanation.
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Fig. 6. Percentage change in specific growth rate from freshwater (FW) to seawater (SW) for all treatment groups. The number of weeks (W) is approximated using date for exposure to seawater as zero point. The growth in freshwater from May 1–23 is used as baseline for all calculations except that the May 24–June 16 is used for SWS3.
than SWS2 (1.06% day 1) (SWS1 vs. SWS2, t-tests; Pb0.05, SWS2 vs. SWS3, P=0.06). When comparing the means of the growth rates of all treatment groups during the last period in seawater (multiple test; stocks, photoperiods, SWS1–3) no significant effects of
Fig. 7. Specific post-smolt growth rates in seawater during part B of the experiment. The data are split into stocks and photoperiod treatments. Small letters give results of multiple test comparing means of all groups, while capital letters show result of multiple test within stocks (statistical significances found only within the Dale stock).
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Fig. 8. Condition factor during SWS1 (A), SWS2 (B) and SWS3 (C). Salinity is given for each date of measurement (FW or SW). Small letters gives significance of multiple tests comparing group means. Standard errors of means are shown.
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date for seawater switch were found within the stocks, thereby allowing for the presentation of these data shown in Fig. 7. 3.4. Condition factor The switches to seawater were accompanied by a reduction in condition factor (Fig. 8), and a negative, but weak, correlation between mean condition factor and the subsequent mean growth rate in seawater (SWS1: Regression analysis, Pb0.05, R 2=0.85, F=17.1). This relationship was also valid at the individual level, resulting in a significant interaction between photoperiod and condition factor (Table 2). After 7 to 11 weeks in seawater, this relationship was reversed, and the best of the SWS1 growing groups also generally had the highest mean condition factors at the start of that period (Regression analysis, Pb0.05, R 2=0.83, F=14.3). The main reasons for these significances was the tendency for SWS1, and clearer result for SWS2, that the fish under simulated natural photoperiod had lower condition factor prior to sea water switch, and higher condition factor after 7–10 weeks in seawater compared with fish held at constant photoperiod (Fig. 8).
4. Discussion Photoperiod is known to influence freshwater growth rate and the proportion of upper modal group fish (Knutsson and Grav, 1976; Komourdjian et al., 1989; Stefansson et al., 1989, 1991; Skilbrei et al., 1997), smolting (Bjo¨rnsson et al., 1989; Berge et al., 1995) and subsequent growth rate in seawater (Saunders et al., 1985). In the present study, genetic origin was clearly more important than photoperiod during the freshwater phase, probably because the stocks used were different with respect to life-history parameters as growth rate and smolt size. The Dale stock showed the best performance with respect to the proportion and size of upper modal group fish, while the Lone stock developed more slowly than the other stocks. Despite these differences, there was no reason to assume that the size threshold (Elson, 1957; Kristinsson et al., 1985; Skilbrei, 1991) for responding to the reduction in photoperiod (from LD24:0 to LD10:14–LD16:8) did vary between the stocks. The results can be more easily explained by the observed relationship between growth rate and the probability of entering the upper size mode, which favoured the Dale fish because of their higher growth rate. The Hatchery stock improved its relative performance in seawater. The proportion of upper modal group fish in freshwater was comparable to the Lone stock, but the Lone stock was the only stock deviating significantly in size from the other stocks after 6 months in seawater. The lower growth rate in seawater of the Lone fish probably reflects the characteristics of this small sized grilse stock in the wild. Inherent ecological adaptations may therefore add significant variance to measurements of individual growth rates under experimental conditions in fresh- and seawater. The abrupt drop in growth after seawater exposure, which was common for all stocks, was in accordance with the observation of Stradmeyer et al. (1991) that the appetite of smolts is severely reduced after transfer to seawater and also similar to the results of
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Damsga˚rd and Arnesen (1998) who demonstrated that the drop in feed intake after seawater transfer was not related to weight, feed intake or growth rate in freshwater. The finding that photoperiod showed its most significant influence on growth rates shortly after seawater exposures is probably linked to two mechanisms. Increasing photoperiod may stimulate growth rate directly, or indirectly by stimulating smoltification. The hypoosmoregulatory ability has probably been better developed for fish experiencing natural photoperiod in spring as increasing photoperiod is known to stimulate and synchronise the smoltification process (Saunders and Henderson, 1970; McCormick et al., 1987). Further, condition factor is lowered during smoltification (Hoar, 1988). The condition factors of the smolts raised under natural photoperiods were lower at seawater exposures and higher after 6 weeks in seawater compared with the constant photoperiod groups, which indicate that they had an improved physiological status at that time. In support of this, they also grew faster during this period. Increasing photoperiod stimulates growth (Komourdjian et al., 1989; Stefansson et al., 1991; Saunders et al., 1994) and high growth rates may be beneficial during the challenge to adapt to the marine environment when the smolts are highly responsive to stress (Carey and McCormick, 1989). When comparing growth rates in fresh- and seawater it is important to establish whether smoltification implies that the smolt develops the ability to grow at the same rate in seawater as it did in freshwater, or if smoltification itself is characterised by an increase in growth rate. Growth hormone stimulates hypo-osmoregulatory ability (Sakamoto et al., 1994) and environmental salinity increase stimulates plasma growth hormone levels and triggers the final development of hypo-osmoregulatory ability (Schmitz et al., 1994). However, Bjo¨rnsson et al. (1998) speculates whether this transient increase in circulating growth hormone levels represents a specific short-term hypoosmoregulatory role of GH. In the present study, the constant photoperiod groups reached acceptable growth rates, i.e. comparable to those in freshwater, after more than 3 weeks in seawater. When taken into account that they grew at least as rapidly as the natural photoperiod groups for the next months, it is difficult to conclude that they were less smoltified if we assume that such differences affect post-smolt growth rates. The good performance of the constant photoperiod groups in seawater may be an example of a match between the timing of the exposures and circannual rhythms influencing seawater tolerance (Eriksson and Lundqvist, 1982), but was not expected as an increase in photoperiod is regarded as a prerequisite for normal development through synchronisation of the components of smolting (Duston and Saunders, 1990; Berge et al., 1995; Sigholt et al., 1995; Duncan and Bromage, 1998). The fact that the photoperiod of these groups were changed to LD22:2 when the fish were exposed to full salinity seawater complicates this picture. A change to long day is known to induce an increase in plasma growth hormone levels within 3 weeks (Bjo¨rnsson et al., 1995), a change which is accompanied by an increase in growth rate and hypoosmoregulatory ability (Bjo¨rnsson et al., 1995) and a reduction in condition factor (Bjo¨rnsson et al., 2000). It is therefore probable that the increase to LD22:2 has improved the seawater performance of the short daylength groups by stimulating smoltification and/ or growth rate. The comparable performance of the SNP-11 and SNP-15 groups in seawater raises a question of practical interest. When applying artificial photoperiods in smolt production by using a succession of a short followed by a long daylength, what would be the minimum
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winter daylength that is required for the following photo stimulated smoltification? In agreement with the present results, a daylength of 12 h or lower has been demonstrated to increase the numbers of lower modal group fish (Skilbrei et al., 1997), and therefore seems to be an effective bwinter stimulusQ for the bimodal development. At first, one may assume that the increase in photoperiod should be of the same magnitude to stimulate smoltification. However, the relatively minor effect of photoperiod relative to stock origin was probably due to the fact that all photoperiods provided an adequate stimulus to induce smolting. It would be expected that inclusion of non-stimulatory photoperiods would have had a more pronounced effect on growth after transfer to seawater. Therefore, it does not seem to be necessary to reduce the daylength during winter below 14 h. On the contrary, shorter daylengths may reduce the numbers and size of the upper modal group fish, and the time period available for feeding compared to 14–16 h of daily light will be shorter. Such relationships should, however, be studied in more detail before it is recommended to increase the minimum day length above 12 h, which has been frequently applied in Norwegian hatchery practices. The present study demonstrates the responsiveness of Atlantic salmon to photoperiod by showing alterations in growth patterns that follow from adjustments of endogenous rhythms and timing of smoltification. While the variability in growth between genetic groups was large enough to almost shade the effect of photoperiod under stable salinity, there was no evidence of a stock specific response to seawater exposures. Because of the double effect of photoperiod, to stimulate both smoltification and growth, there are several problems associated with the general interpretation of relationships between photoperiod, timing of smoltification and growth rate in seawater. The following alternatives for relationships between growth rate and seawater entry are therefore proposed. Seawater tolerance may be characterised by: (a) The minimal growth rate shortly after exposure to seawater. (b) The period used to reach pre-exposure growth rates. (c) The period used to exceed pre-exposure growth rates. One may ask whether seawater tolerance (b) and preference (c) should be distinguished from each others, implying that a smolt that tolerates seawater is able to re-establish freshwater growth rate while a fully smoltified fish shows its preference for seawater by speeding up its growth rate. The relative differences in the early seawater growth rates did reflect the photoperiod regimes, but the data also illustrate the need in this type of experiments to study the performance in seawater over several months as photoperiod manipulations may have long-term consequences for the growth pattern of Atlantic salmon.
Acknowledgement We thank Gunnar Bakke and Viktor Solbakken for practical assistance during the experiment. The Norwegian Research Council and the Institute of Marine Research
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provided financial support. Salar 2lvik provided one group of experimental fish. We are grateful for the helpful pieces of advice from the anonymous referees, which evidently improved the paper.
References Berge, 2.I., Berg, A., Fyhn, H.J., Barnung, T., Hansen, T., Stefansson, S.O., 1995. Development of salinity tolerance in underyearling smolts of Atlantic salmon (Salmo salar) reared under different photoperiods. Can. J. Fish. Aquat. Sci. 52, 243 – 251. Bjo¨rnsson, B.Th., Thorarensen, H., Ogasawara, T., Kristinsson, J.B., 1989. Photoperiod and temperature affect plasma growth hormone levels, growth condition factor and hypoosmoregulatory ability of juvenile Atlantic salmon (Salmo salar) during parr–smolt transformation. Aquaculture 82, 77 – 91. Bjo¨rnsson, B.Th., Stefansson, S.O., Hansen, T., 1995. Photoperiod regulation of plasma growth hormone levels during parr–smolt transformation of Atlantic salmon: implications for hypoosmoregulatory ability and growth. Gen. Comp. Endocrinol. 100, 73 – 82. Bjo¨rnsson, B.Th., Stefansson, G.V., Berge, 2.I., Hansen, T., Stefansson, S.O., 1998. Circulating growth hormone levels in Atlantic salmon smolts following seawater transfer: effects of photoperiod regime, salinity, duration of exposure and season. Aquaculture 168, 121 – 137. Bjo¨rnsson, B.Th., Hemre, G.-I., Bjbrnevik, M., Hansen, T., 2000. Photoperiod regulation of plasma growth hormone levels during induced smoltification of underyearling Atlantic salmon. Gen. Comp. Endocrinol. 119, 17 – 25. Carey, J.B., McCormick, S.D., 1989. Atlantic salmon smolts are more responsive to an acute handling and confinement stress than parr. Aquaculture 168, 237 – 254. Damsg3rd, B., Arnesen, A.M., 1998. Feeding, growth and social interactions during smolting and seawater acclimation in Atlantic salmon, Salmo salar L.. Aquaculture 168, 7 – 16. Duncan, N.J., Bromage, N., 1998. The effect of different periods of constant short days on smoltification in juvenile Atlantic salmon (Salmo salar). Aquaculture 168, 369 – 386. Duncan, N.J., Auchinachie, N., Robertson, D., Murray, R., Bromage, N., 1998. Growth, maturation and survival of out-of-season 0+ and 1+ Atlantic salmon (Salmo salar) smolts. Aquaculture 168, 325 – 339. Duncan, N.N., Mitchell, D., Bromage, N., 1999. Post-smolt growth and maturation of out-of-season 0+ Atlantic salmon (Salmo salar) reared under different photoperiods. Aquaculture 176, 237 – 244. Duston, J., Saunders, R.L., 1990. The entrainment role of photoperiod on hypoosmoregulatory and growth related aspects of smolting in Atlantic salmon (Salmo salar). Can. J. Zool. 68, 707 – 715. Duston, J., Saunders, R.L., 1995. Advancing smolting to autumn in age 0+ Atlantic salmon by photoperiod, and long-term performance in sea water. Aquaculture 135, 295 – 309. Elson, P., 1957. The importance of size in the change from parr to smolt in Atlantic salmon. Can. Fish Cult. 21, 1 – 6. Eriksson, L.-H., Lundqvist, H., 1982. Circannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon (Salmo salar L.). Aquaculture 28, 113 – 121. Folmar, L.C., Dickhoff, W.W., 1980. The parr smolt transformation (smoltification) and seawater transformation in salmonids. A review of selected literature. Aquaculture 21, 1 – 37. Handeland, S.O., Stefansson, S.O., 2001. Photoperiod control and influence of body size on off-season parr– smolt transformation and post-smolt growth. Aquaculture 192, 291 – 307. Hanke, A.R., Friars, G.W., Saunders, R.L., Terhune, J.M., 1989. Family x photoperiod interaction on growth in juvenile Atlantic salmon, Salmo salar. Genome 32, 1105 – 1112. Hoar, W.S., 1988. The physiology of smolting salmonids. In: Hoar, W.S., Randall, D.J. (Eds.), Fish Physiology, vol. XIB. Academic Press, New York, NY, pp. 275 – 343. Ja¨rvi, T., 1990. Cumulative acute physiological stress in Atlantic salmon smolts: the effect of osmotic imbalance and the presence of predators. Aquaculture 89, 337 – 350. Knutsson, S., Grav, T., 1976. Seawater adaptation in Atlantic salmon (Salmo salar L.) at different experimental temperatures and photoperiods. Aquaculture 8, 169 – 187.
688
O.T. Skilbrei, T. Hansen / Aquaculture 242 (2004) 671–688
Komourdjian, M.P., Fenwick, J.C., Saunders, R.L., 1989. Endocrine-mediated photostimulation of growth in Atlantic salmon. Can. J. Zool. 67, 1505 – 1509. Kristinsson, J.B., Saunders, R.L., Wiggs, A.J., 1985. Growth dynamics during the development of bimodal length–frequency distribution in Atlantic salmon (Salmo salar L.). Aquaculture 45, 1 – 20. Lubin, R.T., Rourke, A.W., Saunders, R.L., 1991. Influence of photoperiod on the number and ultrastructure of gill chloride cells of the Atlantic salmon (Salmo salar) before and during smoltification. Can. J. Fish. Aquat. Sci. 48, 1302 – 1307. McCormick, S.D., Saunders, R.L., 1987. Preparatory physiological adaptations for marine life of salmonids: osmoregulation, growth and metabolism. Am. Fish. Soc. Symp. 1, 221 – 229. McCormick, S.D., Saunders, R.L., Henderson, E.B., Harmon, P.R., 1987. Photoperiod control of parr–smolt transformation in Atlantic salmon (Salmo salar): changes in salinity tolerance, gill Na+, K+-ATPase activity, and plasma thyroid hormones. Can. J. Fish. Aquat. Sci. 44, 1462 – 1468. N&vdal, G., 1983. Genetic Factors in Connection With Age at Maturation. Rourke, A.W., Saunders, R.L., Harmon, P.R., 1991. Changes in plasma protein patterns in smolting Atlantic salmon, Salmo salar L., are not dependent on changed growth rates. J. Fish Biol. 39, 35 – 43. Sakamoto, T., Hirano, T., McCormick, S.D., Madsen, S.S., Nishioka, R.S., Bern, H.A., 1994. Possible mode of seawater-adapting actions of growth hormone in salmonids. Aquaculture 121, 1 – 3. Saunders, R.L., Henderson, E.B., 1970. Influence of photoperiod on smolt development and growth of Atlantic salmon (Salmo salar). J. Fish. Res. Board Can. 25, 2387 – 2401. Saunders, R.L., Duston, J., Benfey, T.J., 1994. Environmental and biological factors affecting growth dynamics in relation to smolting of Atlantic salmon, Salmo salar L.. Aquac. Fish. Manage. 25, 9 – 20. Saunders, R.L., Henderson, E.B., Harmon, P.R., 1985. Effects of photoperiod on juvenile growth and smolting of Atlantic salmon and subsequent survival and growth in sea cages. Aquaculture 45, 55 – 66. Schmitz, M., Berglund, I., Lundqvist, H., Bjo¨rnsson, B., 1994. Growth hormone response to seawater challenge in Atlantic salmon, Salmo salar, during parr–smolt transformation. Aquaculture 121, 1 – 3. Sigholt, T., Staurnes, M., Jakobsen, H.J., Aasgaard, T., 1995. Effects of continuous light and short-day photoperiod on smolting, seawater survival and growth in Atlantic salmon (Salmo salar). Aquaculture 130, 373 – 388. Skilbrei, O.T., 1991. Importance of threshold length and photoperiod for the development of bimodal length– frequency distribution in Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 48, 2163 – 2172. Skilbrei, O.T., Holm, M., Jbrstad, K., Handeland, S.O., 1994. Migration motivation of cultured Atlantic salmon, Salmo salar L., smolts in relation to size, time of release and acclimatization period. Aquac. Fish. Manage. 25, 65 – 77. Skilbrei, O.T., Jbrstad, K., Holm, M., Farestveit, E., Grimnes, A., Aardal, L., 1994. A new release system for coastal ranching of Atlantic salmon (Salmo salar) and behavioural patterns of released smolts. Nordic J. Freshw. Res. 69, 84 – 94. Skilbrei, O.T., Hansen, T., Stefansson, S.O., 1997. Effects of decreases in photoperiod on growth and bimodality in Atlantic salmon (Salmo salar). Aquacult. Res. 28, 43 – 49. Sokal, R.R., Rohlf, J.F., 1981. Biometry. W.H. Freeman, New York. 859 pp. StatSoft, 2003. STATISTICA (data analysis software system), version 6. www.statsoft.com. Stefansson, S.O., N&vdal, G., Hansen, T., 1989. The influence of three unchanging photoperiods on growth and parr–smolt transformation in Atlantic salmon, Salmo salar L.. J. Fish Biol. 35, 237 – 247. Stefansson, S.O., Bjo¨rnsson, B.T., Hansen, T., Haux, C., Taranger, G.L., Saunders, R.L., 1991. Growth, parr– smolt transformation and changes in growth hormone of Atlantic salmon (Salmo salar) reared under different photoperiods. Can. J. Fish. Aquat. Sci. 48, 2100 – 2108. Stradmeyer, L., DePauw, N., Joyce, J., 1991. The effects of seawater transfer on the feeding and survival of smolts reared in sea cage and tank environments. Spec. Publ. Eur. Aquacult. Soc. 14, 306 – 307. Thrush, M.A., Duncan, N.J., Bromage, N.R., 1994. The use of photoperiod in the production of out-of-season Atlantic salmon (Salmo salar) smolts. Aquaculture 121, 29 – 44. Villarreal, C.A., Thorpe, J.E., Miles, M.S., 1988. Influence of photoperiod on growth changes in juvenile Atlantic salmon (Salmo salar). J. Fish Biol. 33, 15 – 30.