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Effects of photoperiod and light intensity on growth and activity of juvenile haddock (Melanogrammus aeglefinus)
Aquaculture 217 (2003) 633 – 645 www.elsevier.com/locate/aqua-online
Effects of photoperiod and light intensity on growth and activity of juvenile haddock (Melanogrammus aeglefinus) Edward A. Trippel *, Steven R.E. Neil Fisheries and Oceans Canada, St. Andrews Biological Station, 531 Brandy Cove Road, St. Andrews, New Brunswick, Canada E5B 2L9 Received 11 May 2001; received in revised form 28 March 2002; accepted 14 April 2002
Abstract Enhancement of growth of juvenile haddock (Melanogrammus aeglefinus) was achieved through photomanipulation. After 24 weeks (August – January), hatchery-reared haddock under 24 h light were 53 – 60% heavier than those under natural photoperiod. In a second 24-week experiment, haddock were grown under five photoperiod regimes (natural photoperiod, 12, 16, 20 and 24 h light) with two light intensities (30 and 100 lx) at 24 h. Continuous light (and 20 h light) resulted in the greatest growth response, though other seasonally unchanging photoperiods (12 and 16 h light) also resulted in faster growth than natural photoperiod. Reduced light intensity, from 100 to 30 lx, at 24 h, led to a further 11% improvement in body mass. The effects of photomanipulation declined as temperatures decreased in late autumn and winter. Locomotor activity was the greatest under natural photoperiod (100 lx), less at 24 h (100 lx) and lowest at 24 h (30 lx). Lower swimming activity under continuous dim light may translate into metabolic savings and increased body mass. Integrating these findings with research on larval haddock suggests a period in the ontogeny exists during which bright light should be dimmed to maximize growth and this perhaps coincides with changes in body morphology and behaviour associated with benthic foraging. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Photoperiod; Light intensity; Growth; Activity; Temperature; Juvenile; Haddock
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Corresponding author. Tel.: +1-506-529-8854; fax: +1-506-529-5862. E-mail address: [email protected] (E.A. Trippel).
0044-8486/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 ( 0 2 ) 0 0 1 9 8 - 9
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1. Introduction Photoperiod and light intensity manipulation have been successfully used to improve growth of larval and juvenile stages of a number of fish species. Continuous illumination has enhanced juvenile growth of Atlantic salmon (Salmo salar) (Saunders et al., 1985); Atlantic cod (Gadus morhua) (Folkvord and Ottera˚, 1993), turbot (Scophthalamus maximus) (Imsland et al., 1995, 1997), barramundi (Lates calcarifer) (Barlow et al., 1995), and halibut (Hippoglossus hippoglossus) (Simensen et al., 2000), but for several other species juvenile growth was not influenced by extended daylength (sole (Solea solea), Fuchs, 1978; black porgy (Mylio macrocephalus), Kiyono and Hirano, 1981; yellowtail flounder (Pleuronectes ferrugineus), Purchase et al., 2000). Larval haddock (Melanogrammus aeglefinus) grew faster when reared under continuous bright compared to dim light (Downing and Litvak, 1999a), though wide variability in feeding success and growth in relation to light intensity have been reported in larval fishes (Blaxter, 1986; Huse, 1994) and these variations are believed to be a function of species-specific natural light niches and stock origin (Job and Bellwood, 2000; Puvanendran and Brown, 2000). In the marine environment, as haddock change from larval to juvenile phases, they shift from the pelagic to demersal zone. This occurs at a body length of f2 – 3 cm when juveniles are characterized by a subterminal mouth and a natural diet consisting primarily of benthic invertebrates (Scott and Scott, 1988). The requirement of bright visual feeding conditions associated with planktivory presumably diminishes with this ontogenetic shift. Thus, the effect of light intensity on growth of haddock and other demersal marine fishes may be important and different cultivation strategies may be required for different life history phases. Improved fish growth in relation to photo regime has been attributed to a number of factors including higher food conversion efficiency, lower activity and lower oxygen consumption (Imsland et al., 1995; Appelbaum and Kamler, 2000). The objectives of the present study were to examine the effects of photoperiod and light intensity on growth and locomotor activity of juvenile haddock. In the first experiment, we examined the effects of natural photoperiod and continuous light on juvenile growth under two feeding regimes. In the second experiment, we broadened our study and examined juvenile growth in relation to natural photoperiod, 12, 16, 20, and 24 h illumination (in addition two light intensities were examined at 24 h light). Locomotor activity was evaluated under natural photoperiod and continuous light.
2. Method 2.1. Experiment 1 Haddock used in the first experiment were fish of mixed parental background raised from eggs produced by broodstock maintained at the St. Andrews Biological Station, New Brunswick, Canada. Prior to experimentation, larvae were maintained from May to July, 1998 in 7 m3 conical tanks containing filtered seawater (salinity f30 ppt; 7– 10 jC), fed wild zooplankton ad libitum, and weaned to a formulated dry food diet (Moore-Clark, Perla Marine, 400 – 700 Am) and maintained under continuous light (100 lx (f1.72 AE/s/
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m2) at water’s surface). On July 13, at a weight of 1 – 2 g, fish were transferred to 450-l tanks kept under continuous light (100 lx). On August 12, 360 juveniles of similar size were anaesthetized in MS-222 (60 mg/l) and wet weight (F0.1 g) and fork length (F0.1 cm) recorded (initial mean weight (SD) 4.38 g (F0.05 g)). Sixty fishes were randomly distributed into each of six square 450-l (110.45 m deep (water depth 0.30 m)) grey tanks with two replicates for each of three treatments (i) simulated natural photoperiod (NP), dry food delivered continuously during daylight phase using automatic belt feeder; (ii) 24 h light:0 h dark (LD 24:0), food delivery same as (i); and (iii) 24 h light:0 h dark (LD 24:0), food delivered continuously over 24 h. Fish were fed to satiation at f3% body weight per day (Corey Feed, Haddock Grower, pellet size 1 mm, 3 mm). In all treatments, fish foraged on pellets as they descended to the tank bottom as well as off the bottom. Fork length and body weight were recorded once every 4 weeks until the end of the 24-week experiment on January 27, 1999. Fulton’s condition factor (body weight/fork length3) x 100 was calculated once every 4 weeks. Specific growth rate (SGR) over 4-week periods was calculated based on means of treatment weights as: SGR ¼ 100 ðlnW2 lnW1 Þ=ðt2 t1 Þ where W2 and W1 are body weights (g) at days t2 and t1, respectively. Lights used were two fluorescent 60 cm tubes (Sylvania white 20 W bulbs F 20T12) per tank placed 1 m above the water’s surface. Simulated natural photoperiod was adjusted weekly using timers and changed from 14 h light:10 h dark at the beginning of the experiment to 10 h light:14 h dark at its cessation with the shortest daylength in December of f8 h 15 min (Fig. 1). Tanks were checked daily for mortalities and any dead fish removed. Water temperature was recorded throughout the experiment and changed seasonally (Fig. 1).
Fig. 1. Seasonal changes in water temperature and natural photoperiod at the St. Andrews Biological Station during the experimental periods of 1998 and 1999.
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2.2. Experiment 2 Haddock used in the second experiment were fish of mixed parental background raised from eggs produced by broodstock maintained at the Aquarium and Marine Center, Shippagan, New Brunswick. Prior to experimentation, larvae were maintained on a diet of n3 HUFA enriched rotifers and Artemia and weaned to a dry food diet (Biokiowa, 400– 700 Am). Fish were maintained from May to July, 1999 in 1.2 m3 circular tanks containing filtered seawater (salinity 30 ppt, 10– 12 jC) under continuous light (100 lx). On July 8, they were transferred by truck (6 h trip) in insulated tanks containing oxygenated water (f100% saturation) to the St. Andrews Biological Station where they were placed in a 5m3 tank under continuous light (100 lx) and maintained on a formulated dry food diet. On August 4, 600 juveniles of similar size were anaesthetized in MS-222 (60 mg/l) and wet weight (F0.1 g) and fork length (F0.1 cm) recorded (initial mean weight (SD) 5.38 g (F0.06 g)). Sixty fish were randomly distributed in each of 12 square 450-l tanks with two replicates for each of six treatments (i) simulated natural photoperiod (NP), (ii) 12 h light:12 h dark (LD 12:12), (iii) 16 h light:8 h dark (LD 16:8), (iv) 20 h light:4 h dark (LD 20:4), (v) 24 h light:0 h dark (LD 24:0), (i – v at 100 lx, f1.72 AE/s/m2), and (vi) 24 h light:0 dark (LD 24:0) at 30 lx, f0.20 AE/s/m2. Lower light intensity was achieved by covering the two fluorescent 60-cm tubes with shade cloth. Fish were fed to satiation at f3% body weight per day (Corey Feed, Haddock Grower, pellet size 1 mm, 3 mm) partitioned over three meals with food administered using automatic belt feeders (0800 – 0900 h 45% of ration, 1200 – 1300 h 20%, and 1600 –1700 h 35%). Initial fish size (4– 6 g) corresponded with the size at which juvenile haddock are customarily transferred from hatcheries to marine cage sites. Fork length and body weight were recorded once every 4 weeks until the end of the 24-week experiment on January 19, 2000. Locomotor activity was estimated f1 week after final body measurements and were recorded by counting the number of fish that passed through a fixed station in each of six tanks representing three treatments. Fixed stations were erected by vertically fixing two rods 30 cm apart to the bottom of a tank such that the space between them was centrally located in the tank. The rods were placed into tanks 3 days before counts were conducted. The number of fish that passed through the 3030 cm space between the rods (water depth in tanks was 30 cm) was recorded over a 1-min period. From January 24 – 28, 1 min activity measurements were recorded five times per day: 0830, 0930, 1030, 1530, and 2000 h for three treatments; natural photoperiod (100 lx), 24 h (100 lx), and 24 h (30 lx). A red light source was used to conduct night (2000 h) observations under natural photoperiod (40 W incandescent bulb CSA LR94262 located 1 m above water’s surface, light intensity 15 lx (f0.13 AE/s/m) at water’s surface). Fish showed no signs of being startled when the red light was turned on f1 h before movements were recorded as the vision of marine teleosts occurring in blue-green coastal waters is commonly not red-sensitive (Nicol, 1989). Data were tested for normality (Kolmogorov – Smirnov test) and homogeneity of variance (Levene statistic) (SPSS version 10.0). Single classification analysis of variance was used to determine if significant differences ( P<0.05) in fork length, body weight, condition factor and locomotor activity occurred between treatments. For attributes where significant differences occurred, the Duncan’s multiple range test (a=0.05) was used to
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determine whether treatments differed from one another. Tank effects were examined for each variable on each sampling date using a series of Bonferroni corrected t-tests (Trippel and Hubert, 1990). The tanks effects were minor (in 1998, 95% of the replicate tanks showed no significant difference ( P<0.05), and in 1999, 88% showed no difference). When differences did occur, they were small (f10%). For this reason, we pooled data of replicate tanks to conduct subsequent statistical analyses (e.g., ANOVA).
3. Results 3.1. Experiment 1 Haddock grew faster under continuous light than under simulated natural photoperiod. After 4 weeks, significantly greater body weights occurred under the two 24-h treatments compared to natural photoperiod (significant differences in fork length and condition Table 1 Fork length, body weight, and condition factor of haddock maintained for 24 weeks at three light/feeding regimes (NP=natural photoperiod) Photoperiod Week
NP (100 lx) NP Feed
24 h (100 lx) NP Feed
24 h (100 lx) 24 h Feed
Fork length (cm) 0 12/08/98 4 09/09/98 8 07/10/98 12 05/11/98 16 02/12/98 20 30/12/98 24 27/01/99
Date
7.25aF0.09 10.52bF0.12 12.78bF0.16 14.40bF0.18 15.56bF0.20 16.34bF0.21 17.01bF0.21
7.29aF0.09 10.96aF0.13 13.89aF0.14 16.10aF0.14 17.75aF0.16 18.82aF0.16 19.33aF0.17
7.31aF0.08 10.98aF0.12 13.89aF0.13 16.09aF0.13 17.66aF0.14 18.63aF0.14 19.19aF0.14
Body weight (g) 0 12/08/98 4 09/09/98 8 07/10/98 12 05/11/98 16 02/12/98 20 30/12/98 24 27/01/99
4.32aF0.17 13.71bF0.47 25.13bF0.95 35.62bF1.43 45.77bF1.89 53.79bF2.19 57.34bF2.26
4.38aF0.16 15.78aF0.52 33.50aF0.99 52.42aF1.43 73.02aF1.94 88.63aF2.30 91.47aF2.38
4.43aF0.14 15.79aF0.49 33.48aF0.91 51.76aF1.32 71.05aF1.73 86.06aF2.09 87.72aF2.19
Condition factor 0 12/08/98 4 09/09/98 8 07/10/98 12 05/11/98 16 02/12/98 20 30/12/98 24 27/01/99
1.06aF0.01 1.12aF0.01 1.14bF0.01 1.12bF0.01 1.14bF0.01 1.16bF0.01 1.10bF0.01
1.06aF0.01 1.14aF0.01 1.20aF0.01 1.22aF0.01 1.27aF0.01 1.29aF0.01 1.23aF0.01
1.09aF0.01 1.14aF0.01 1.21aF0.01 1.21aF0.01 1.26aF0.01 1.30aF0.01 1.21aF0.01
MeanFstandard error values are shown. Means sharing the same letter superscript on given dates are not significantly different (Duncan’s multiple range test, a=0.05).
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factor commenced at 8 weeks) (Table 1). After 24 weeks, haddock under 24 h light (natural photoperiod (NP) food delivery) and 24 h light (24 h food delivery) were significantly heavier (60% and 53%, respectively) than those under NP (Table 1). Timing
Fig. 2. Changes in daily specific growth rate (SGR) of haddock exposed to different photo regimes in 1998 and 1999. Unless indicated otherwise, all treatments were conducted at a light intensity of 100 lx. In 1998, two feeding regimes were used at 24 h, one in which food was administered over 24 h and the other during the daylight phase of natural photoperiod (NP). In 1999, a single feeding regime comprised of three meals per day was used for the six treatments.
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of food delivery did not significantly influence body growth at 24 h light (Table 1). Specific growth rate (weights) calculated over 28-day periods declined seasonally as fish became larger and water temperature cooled (Figs. 1 and 2). Weight gain was <7% during the final 4 weeks of the experiment at f2.5 jC. Percent survival over 24 weeks ranged from 82% to 92% among the three treatments. 3.2. Experiment 2 After 16 weeks, significantly greater body weights occurred at 20 and 24 h light than at 12 and 16 h light and natural photoperiod (Table 2). Body weight was significantly lower under natural photoperiod than at other light regimes and this difference was noted early (4 weeks) and maintained through the experiment (24 weeks). Low light intensity resulted in comparatively faster growth. After 24 weeks, significantly greater body weights (11.1%) occurred at 30 lx (24 h) than at 100 lx (24 h). Specific growth rates reflected the trend of faster growth in dim light (Fig. 2). The initial higher specific growth rates in 1998 Table 2 Fork length, body weight, and condition factor of haddock maintained for 24 weeks at six light regimes (NP=natural photoperiod) Photoperiod Week Date
NP (100 lx)
12 h (100 lx)
16 h (100 lx)
20 h (100 lx)
Fork length (cm) 0 04/08/99 4 01/09/99 8 29/09/99 12 27/10/99 16 24/11/99 20 22/12/99 24 19/01/00
7.61aF0.07 7.64aF0.07 10.38aF0.09 10.37aF0.09 12.90aF0.08 13.03aF0.08 14.76cF0.09 15.23abF0.09 16.19dF0.10 16.78bcF0.10 17.52dF0.11 18.13bcF0.11 18.20dF0.13 18.86cF0.12
7.67aF0.07 10.40aF0.09 13.00aF0.08 15.07bF0.08 16.62cF0.09 17.95cF0.10 18.76cF0.11
7.67aF0.07 7.69aF0.07 7.54aF0.08 10.38aF0.09 10.40aF0.10 10.23aF0.11 13.09aF0.09 13.04aF0.09 13.08aF0.10 15.24abF0.09 15.04bF0.10 15.39aF0.11 16.93bF0.11 16.76bcF0.10 17.26aF0.11 18.36bF0.12 18.26bcF0.11 18.50aF0.11 19.26bF0.12 19.20bF0.12 19.79aF0.12
Body 0 4 8 12 16 20 24
5.54aF0.13 5.63aF0.14 a 13.20 F0.33 13.25aF0.34 26.94bF0.55 28.37abF0.59 40.78cF0.86 45.70bF0.96 54.99dF1.17 62.99bcF1.24 64.77dF1.46 72.26cF1.54 74.56dF1.71 82.61cF1.86
5.56aF0.13 13.43aF0.33 28.16abF0.57 44.78bF0.94 59.81cF1.27 71.23cF1.54 82.07cF1.77
5.60aF0.14 5.84aF0.15 5.46aF0.16 a a 12.80 F0.31 13.61 F0.38 13.02aF0.42 28.12abF0.54 28.62abF0.63 29.33aF0.67 46.94abF0.88 44.70bF0.96 49.46aF1.05 65.16bF1.19 64.50bF1.25 69.56aF1.39 78.02bF1.51 77.29bF1.57 85.05aF1.52 91.11bF1.78 92.05bF1.81 102.26aF2.00
weight (g) 04/08/99 01/09/99 29/09/99 27/10/99 24/11/99 22/12/99 19/01/00
Condition factor 0 04/08/99 4 01/09/99 8 29/09/99 12 27/10/99 16 24/11/99 20 22/12/99 24 19/01/00
1.24abF0.01 1.15bF0.01 1.23cF0.01 1.25dF0.01 1.27cF0.01 1.18dF0.01 1.21cF0.01
1.24abF0.01 1.16bF0.01 1.26abF0.01 1.27cdF0.01 1.31bF0.01 1.19cdF0.01 1.21cF0.01
1.21aF0.01 1.16bF0.01 1.26abF0.01 1.29bcF0.01 1.28cF0.01 1.21cF0.01 1.22cF0.01
1.22aF0.01 1.12aF0.01 1.24bcF0.01 1.31abF0.01 1.33abF0.01 1.24bF0.01 1.26bF0.01
24 h (100 lx) 24 h (30 lx)
1.26bF0.01 1.17bF0.01 1.27aF0.01 1.29bcF0.01 1.35aF0.01 1.25bF0.01 1.28abF0.01
1.23abF0.01 1.16bF0.01 1.28aF0.01 1.33aF0.01 1.34abF0.01 1.34aF0.01 1.30aF0.01
MeanFstandard error values are shown. Means sharing the same letter superscript on given dates are not significantly different (Duncan’s multiple range test, a=0.05).
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Fig. 3. Number of haddock (meanFstandard error) that moved through a fixed station under three different photo regimes during the period January 24 – 28, 2000. Counts were conducted during five periods: Before Feeding: just prior to loading of belt feeders, Feed Preparation: immediately after belt feeders have been loaded, First Feeding: coincides with first meal, After Feeding: between second and third meals, and Evening: natural photoperiod (NP) represents darkness (red light used to conduct counts). Statistically significant differences in activity occurred between each of the three photo regimes at each time of day evaluated (Duncan’s multiple range test, a=0.05).
compared to 1999 occurred under warmer water temperatures, i.e., natural photoperiod SGRs were 4.2% and 3.2%/day at 14.1 and 12.4 jC, respectively (Figs. 1 and 2). Percent survival over 24 weeks ranged from 94% to 96% among the six treatments. Haddock locomotor activity was the greatest under natural photoperiod (100 lx), less at 24 h (100 lx), and lowest at 24 h (30 lx) (Fig. 3). Fish under natural photoperiod (100 lx) passed through the fixed station approximately twice as often as those at 24 h (30 lx). Under natural photoperiod, activity rates varied through the day with activity being lowest in the mid-afternoon and evening and highest during the loading of belt feeders in the morning. Night activity levels under natural photoperiod remained higher than those at 24 h light.
4. Discussion Extended daylength significantly improved growth of juvenile haddock. Improved appetite, greater ration and higher food conversion efficiency are factors commonly reported to be responsible for faster teleost growth under continuous light (Saunders and Henderson, 1970; Folkvord and Ottera˚, 1993). Changes in endocrine functioning as a
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result of photo regime likely play a key role in this response (Porter et al., 2001). Whether extended daylength continues to have a beneficial effect on haddock growth after the first summer and autumn is uncertain and requires further investigation. Given the cold winter temperatures in the Bay of Fundy (f2– 3 jC) and associated slow growth, any extended gains in growth would presumably occur during the subsequent spring to autumn period. Although the application of continuous light (and 20 h light) resulted in the greatest growth response, it is worth noting that the other seasonally unchanging photoperiods (12 and 16 h light) resulted in faster growth than natural photoperiod; a result similar to that observed in Atlantic salmon (Saunders et al., 1985). Moreover, it is of interest that two discrete growth responses were observed (12 and 16 h compared to 20 and 24 h light) (Table 2). It is unclear why an additional 4 h of light from 16 to 20 h improved growth, but an extra 4 h had no effect between other treatments (i.e., from 12 to 16 h and 20 to 24 h). In juvenile turbot (maintained at natural photoperiod, 16 h light:8 h dark, and 24 h light:0 h dark), continuous light slightly enhanced the growth rate above that of other regimes, after 3 months of exposure at 10 and 16 jC, but not throughout the 6 month experiment (Imsland et al., 1995). However, in a recent paper (Imsland et al., 1997), better long-term growth (18 months) of turbot occurred when exposed to extended daylength during the first winter. In Sebastes diploproa, the positive effects of constant illumination on growth were related to a greater scope for growth and due to their lower standard metabolic rate (Boehlert, 1981). It is often not possible to determine if the light effect on growth depends on food consumption or better food utilization. Similar growth of haddock between the two feeding regimes in Experiment 1 suggests that an extended feeding period does not enhance growth under equivalent daily rations. Thus, haddock may be capable of reaching satiation during a feeding period equivalent to natural daylength, as observed for Atlantic salmon in sea cages (Kra˚kenes et al., 1991). In green sunfish (Lepomis cyanellus) maintained for 6 weeks at four photoperiods (constant 8 h light:16 h dark, 16 h light:8 h dark, increasing 8 – 16 h light and decreasing 16– 8 h light), Gross et al. (1965) demonstrated greater food intake occurred under longer daylength. Fish growth and food conversion efficiency also were closely correlated and were generally highest in the increasing photoperiod. As noted in Boeuf and LeBail’s (1999) review of the subject, Gross et al. (1965) were the first to specify that growth might be influenced by light through a better food conversion efficiency and not just stimulated food intake. Reduced light intensity, from 100 to 30 lx, at 24 h light, led to improved juvenile growth of haddock. Consequently, dim continuous light appears to be the best strategy of those investigated. This low light level is more characteristic of their natural habitat at 60 –120 m on offshore banks in the Northwest Atlantic (Beamish, 1966; Jerlov, 1968; Scott and Scott, 1988; Nicol, 1989; Puvanendran and Brown, 2000). Locomotor activity indicated that juvenile haddock swim less at low light and this may translate into metabolic savings and increased body mass. Swimming activity is a bioenergetic component not frequently related to improved growth efficiency and larger body mass of cultivated fish (Jorgensen and Jobling, 1991). African catfish (Clarias gariepinus) under reduced light, swam less and used less oxygen with more energy channeled into growth (Appelbaum and Kamler, 2000). In another demersal species, Atlantic halibut, Hole and Pittman (1995) observed the best growth at 1 to 10 lx, compared to 500 lx (12 h light at 11 and 14 jC).
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Effects of light intensity on Atlantic salmon postsmolt growth in net pens have shown mixed results, with enhanced summer and autumn growth occurring when light-reducing black polyethylene netting covers were deployed for 1 year (Huse et al., 1990). In another experiment, Atlantic salmon postsmolts exposed to high light intensity in sea pens showed significantly better growth (Oppedal et al., 1997). Swimming activity among individual haddock was less variable (low standard errors) at 24 h light (30 lx) relative to 24 h light (100 lx) and natural photoperiod (100 lx) (Fig. 3). Further observations of haddock following Experiment 2 in February – May, 2000 revealed that by shifting photoperiod and light intensity, their activity patterns could be altered (E.A. Trippel, unpublished data). When measurements of activity were made 3 days after shade cloth was removed from the 24 h light (30 lx) treatment (raising it to 100 lx), the activity rate had increased and was equivalent to the 24 h light (100 lx) treatment (the reverse was also achieved). Thus, the behavioural responses to light appear to be quite flexible. Interestingly, haddock activity was greater during darkness than in light under, either of the two 24 h light regimes (i.e., during the 2000 h observation period, which was initiated f4 h after darkness in natural photoperiod) (Fig. 3). Thus, the dark phase of natural photoperiod did not have a great impact in reducing swimming activity. The greater movement during light and dark phases under natural photoperiod compared to 24 h light presumably resulted in additional oxygen consumption and energy expended, which could have been diverted to growth. Although not specifically measured, haddock at 24 h light (30 lx) relative to other treatments appeared to require lower rations (via visual observations of remaining uneaten food) and this facet of their diet requires further examination. If true, then food conversion efficiency is better under dim constant illumination and would help to reduce food costs for commercial culture. Consequently, haddock photo regime (periodicity and intensity) could have a significant effect on the culture of haddock during the 3 – 100 g phase when seasonal water temperatures support good growth. The seasonal duration that photo regime enhances growth could be further extended in a land-based facility in which water temperature can be controlled. Differences in specific growth rates between 1998 and 1999 may in part be related to differences in seasonal water temperatures between the two years (Figs. 1 and 2). In Experiment 1, the summer temperature was higher and winter temperature lower than in Experiment 2. The growth differences between natural photoperiod and 24 h light were greater in Experiment 1, perhaps initiated by the higher early period temperature. At the completion of Experiment 2, there was much less of a growth difference between natural photoperiod and 24 h light (22% compared to 53 –60% in Experiment 1), but the higher temperature by f2 jC during winter was associated with faster December – January growth compared to Experiment 1. Fish culturists need to recognize that the scope for improving growth through photo manipulation is apparently associated with ambient water temperature. Inspection of the specific growth rates in Fig. 2 suggests that the effect of photoperiod declined as temperatures decreased in late autumn and winter. It would be of interest to further explore the interaction between photoperiod and temperature under controlled temperature conditions. Other contributing factors include diet composition and parental origin. As a preliminary analysis, Iwama and Tautz’s (1981) growth coefficient ( Gc) was calculated for each treatment from each experimental year. This measure is useful in that it allows the comparison of the growth of fish at different sizes, reared at
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different temperatures. Growth coefficients for 1998 (all at 100 lx) were: 36.4 (NP, NP feed), 62.4 (24 h light, NP feed), and 60.0 (24 h light, 24 h feed). Growth coefficients for 1999 (all at 100 lx unless indicated) were: 42.4 (NP), 48.1 (12 h light), 47.2 (16 h light), 53.3 (20 h light), 52.8 (24 h light), and 59.6 (24 h light, 30 lx). These trends reflect the results presented. Note, however, at natural photoperiod, Gc was substantially lower in 1998 (36.4) than in 1999 (42.4) suggesting that other factors in addition to temperature and fish size could have contributed to the growth differences in 1998 and 1999. To maximize production, the present study on juveniles and the results of Downing and Litvak (1999a,b) on larval haddock indicate there is a period in the ontogeny during which bright light which increases forage success of highly visual feeders should be dimmed and this perhaps coincides with changes in body morphology and behaviour adapted for benthic feeding. Continuous light also has been reported to reduce the incidence of sexual maturity in some teleosts (Hansen et al., 1992; Oppedal et al., 1997; Jourdan et al., 2000), and supports the widespread applicability of photoperiod manipulation to finfish aquaculture (Boeuf and LeBail, 1999). Recently, many Atlantic salmon farmers in Norway and Scotland began using continuous lighting during the autumn or winter (October –April) to improve growth, as growth of fish subjected to natural daylight is lowered during the autumn and winter, while, conversely, no such growth depression is observed during winter under a continuous light regime (Forsberg, 1995). In a recent study (Oppedal et al., 1997), when light intensity was sufficient, abrupt changes in exposure of Atlantic salmon from natural short daylength to continuous additional illumination (January – June) promoted growth without initiating maturation. Besides application to aquaculture, the findings on light intensity are also relevant to our understanding of fish behaviour in the natural environment. Aquatic ecosystems, both freshwater and marine, often undergo changes in clarity which affect light transmission. Thus, fish in part may alter their depth distribution in relation to preferred light intensities (Job and Bellwood, 2000). The degree that light intensity and photoperiod affect locomotion and growth is worthy of study for other fishes from both aquaculture and environmental perspectives. Acknowledgements We thank J. Bowers, P. Harmon, K. Madsen, T. Shepherd, and T. Taylor for laboratory assistance and appropriate care of fish. C. Lanteigne of the Aquarium and Marine Center located in Shippagan, NB, kindly provided haddock for experimental use. J. Castell and P. Harmon provided helpful comments on an earlier draft. Two anonymous reviewers also assisted in improving the manuscript for which the authors are grateful. Financial support for the project was provided in part by the Department of Fisheries and Oceans Science Youth Internship Program and Heritage Aquaculture, Blacks Harbour, NB. References Appelbaum, S., Kamler, E., 2000. Survival, growth, metabolism and behaviour of Clarias gariepinus (Burchell 1822) early stages under different light conditions. Aquac. Eng. 22, 269 – 287.
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Barlow, C.G., Pearce, M.G., Rodgers, L.J., Clayton, P., 1995. Effects of photoperiod on growth, survival, and feeding periodicity of larval and juvenile barramundi, Lates calcarifer (Bloch). Aquaculture 138, 159 – 168. Beamish, F.W.H., 1966. Vertical migration by demersal fish in the Northwest Atlantic. J. Fish. Res. Board Can. 23, 109 – 139. Blaxter, J.H.S., 1986. Visual thresholds and spectral sensitivity of flatfish larvae. J. Exp. Biol. 51, 221 – 230. Boehlert, G.W., 1981. The effects of photoperiod and temperature on laboratory growth of juvenile Sebastes diploproa and a comparison with growth in the field. Fish. Bull. 79, 789 – 794. Boeuf, G., LeBail, P.Y., 1999. Does light have an influence on fish growth? Aquaculture 1777, 129 – 152. Downing, G., Litvak, M.K., 1999a. The effect of photoperiod, tank colour and light intensity on growth of larval haddock. Aquac. Int. 7, 369 – 382. Downing, G., Litvak, M.K., 1999b. The influence of light intensity on growth of larval haddock. N. Am. J. Aquac. 61, 135 – 140. Folkvord, A., Ottera˚, H., 1993. Effects of initial size distribution, day length, and feeding frequency on growth, survival, and cannibalism in juvenile Atlantic cod (Gadus morhua L.). Aquaculture 114, 243 – 260. Forsberg, O.I., 1995. Empirical investigations on growth of post-smolt Atlantic salmon (Salmo salar L.) in landbased farms. Evidence of a photoperiodic influence. Aquaculture 133, 235 – 248. Fuchs, J., 1978. Influence de la photoperiode sur la croissance et la survie de la larve et du juvenile de sole (Solea solea) en e´le´vage. Aquaculture 15, 63 – 74. Gross, W.L., Roelofs, E.W., Fromm, P.O., 1965. Influence of photoperiod on growth of green sunfish, Lepomis cyanellus. J. Fish. Res. Board Can. 22, 1379 – 1386. Hansen, T., Stefansson, S., Taranger, G.L., 1992. Growth and sexual maturation in Atlantic salmon, Salmo salar L., reared in sea cages at two different light regimes. Aquac. Fish. Manage. 23, 275 – 280. Hole, G., Pittman, K., 1995. Effects of light and temperature on growth in juvenile halibut (Hippoglossus hippoglossus L.). In: Pittman, K., Batty, R.S., Verreth, J. (Eds.), ICES Marine Science Symposia, Mass Rearing of Juvenile Fish. Bergen, 21 – 23 June 1993, vol. 201, p. 197. Huse, I.J., 1994. Feeding at different illumination levels in larvae of three marine teleost species: cod, Gadus morhua L., plaice, Pleuronectes platessa L., and turbot, Scophthalmus maximus (L.). Aquac. Fish. Manage. 25, 687 – 695. Huse, I., Bjordal, A., Ferno¨, A., Furevik, D., 1990. The effect of shading in pen rearing of Atlantic salmon (Salmo salar). Aquac. Eng. 9, 235 – 244. Imsland, A., Folkvord, A.F., Steffansson, S.O., 1995. Growth, oxygen consumption and activity of juvenile turbot (Scophthalmus maximus L.) reared under different temperatures and photoperiods. Neth. J. Sea Res. 34, 149 – 159. Imsland, A.K., Folkvord, A.F., Jo´nsdo´ttir, O.D.B., Steffansson, S.O., 1997. Effects of exposure of extended photoperiods during the first winter on long-term growth and age at first maturity in turbot (Scophthalmus maximus). Aquaculture 159, 125 – 141. Iwama, G.K., Tautz, A.F., 1981. A simple growth model for salmonids in hatcheries. Can. J. Fish. Aquat. Sci. 38, 649 – 656. Jerlov, N.G., 1968. Optical Oceanography. Elsevier, Amsterdam. Job, S.D., Bellwood, D.R., 2000. Light sensitivity in larval fishes: implications for vertical zonation in the pelagic zone. Limnol. Oceanogr. 45, 362 – 371. Jorgensen, E.H., Jobling, M., 1991. The effects of exercise on growth, food utilization and osmoregulatory capacity of juvenile Atlantic salmon, Salmo salar. Aquaculture 116, 233 – 246. Jourdan, S., Fontaine, P., Boujard, T., Vandeloise, E., Gardeur, J.N., Anthouard, M., Kestemont, P., 2000. Influence of daylength on growth, heterogeneity, gonad development, sexual steroid and thyroid levels, and N and P budgets in Perca fluviatilis. Aquaculture 186, 253 – 265. Kiyono, M., Hirano, R., 1981. Effects of light on the feeding and growth of black porgy, Mylio macrocephalus (Basilewsky), postlarvae and juveniles. Rapp. et proces-verbaux des re´unions. Cons. Inter. Explor. Mer 178, 334 – 336. Kra˚kenes, R., Hansen, T., Stefansson, S.O., Taranger, G.L., 1991. Continuous light increases growth rate of Atlantic salmon (Salmo salar L.) postsmolts in sea cages. Aquaculture 95, 281 – 287. Nicol, J.A.C., 1989. The Eyes of Fishes. Clarendon Press, Oxford, UK. Oppedal, F., Taranger, G.L., Juell, J., Fosseidengen, J.E., Hansen, T., 1997. Light intensity affects growth and
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sexual maturation of Atlantic salmon (Salmo salar L.) postsmolts in sea cages. Aquat. Living Resour. 10, 351 – 357. Porter, M.J.R., Duncan, N., Handeland, S.O., Stefansson, O., Bromage, N.R., 2001. Temperature, light intensity and plasma melatonin levels in juvenile Atlantic salmon. J. Fish Biol. 58, 431 – 438. Purchase, C.F., Boyce, D.L., Brown, J.A., 2000. Growth and survival of juvenile flounder Pleuronectes ferrugineus (Storer) under different photoperiods. Aquac. Res. 31, 547 – 552. Puvanendran, V., Brown, J.J., 2000. Effect of light intensity on the foraging and growth of Atlantic cod larvae: interpopulation difference? Mar. Ecol., Prog. Ser. 167, 207 – 214. 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. 27, 1295 – 1311. 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. Scott, W.B., Scott, M.G., 1988. Atlantic fishes of Canada. Can. Bull. Fish. Aquat. Sci. 219, 274 – 276. Simensen, L.M., Jonassen, T.M., Imsland, A.K., Stefansson, S.O., 2000. Photoperiod regulation of growth of juvenile Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 190, 119 – 128. Trippel, E.A., Hubert, J.J., 1990. Common statistical errors in fishery research. In: Hunter, J. (Ed.), Writing for Fishery Journals. American Fisheries Society, Bethesda, MD, pp. 93 – 102.
Effects of photoperiod and light intensity on growth and activity of juvenile haddock (Melanogrammus aeglefinus) Edward A. Trippel *, Steven R.E. Neil Fisheries and Oceans Canada, St. Andrews Biological Station, 531 Brandy Cove Road, St. Andrews, New Brunswick, Canada E5B 2L9 Received 11 May 2001; received in revised form 28 March 2002; accepted 14 April 2002
Abstract Enhancement of growth of juvenile haddock (Melanogrammus aeglefinus) was achieved through photomanipulation. After 24 weeks (August – January), hatchery-reared haddock under 24 h light were 53 – 60% heavier than those under natural photoperiod. In a second 24-week experiment, haddock were grown under five photoperiod regimes (natural photoperiod, 12, 16, 20 and 24 h light) with two light intensities (30 and 100 lx) at 24 h. Continuous light (and 20 h light) resulted in the greatest growth response, though other seasonally unchanging photoperiods (12 and 16 h light) also resulted in faster growth than natural photoperiod. Reduced light intensity, from 100 to 30 lx, at 24 h, led to a further 11% improvement in body mass. The effects of photomanipulation declined as temperatures decreased in late autumn and winter. Locomotor activity was the greatest under natural photoperiod (100 lx), less at 24 h (100 lx) and lowest at 24 h (30 lx). Lower swimming activity under continuous dim light may translate into metabolic savings and increased body mass. Integrating these findings with research on larval haddock suggests a period in the ontogeny exists during which bright light should be dimmed to maximize growth and this perhaps coincides with changes in body morphology and behaviour associated with benthic foraging. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Photoperiod; Light intensity; Growth; Activity; Temperature; Juvenile; Haddock
*
Corresponding author. Tel.: +1-506-529-8854; fax: +1-506-529-5862. E-mail address: [email protected] (E.A. Trippel).
0044-8486/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 ( 0 2 ) 0 0 1 9 8 - 9
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1. Introduction Photoperiod and light intensity manipulation have been successfully used to improve growth of larval and juvenile stages of a number of fish species. Continuous illumination has enhanced juvenile growth of Atlantic salmon (Salmo salar) (Saunders et al., 1985); Atlantic cod (Gadus morhua) (Folkvord and Ottera˚, 1993), turbot (Scophthalamus maximus) (Imsland et al., 1995, 1997), barramundi (Lates calcarifer) (Barlow et al., 1995), and halibut (Hippoglossus hippoglossus) (Simensen et al., 2000), but for several other species juvenile growth was not influenced by extended daylength (sole (Solea solea), Fuchs, 1978; black porgy (Mylio macrocephalus), Kiyono and Hirano, 1981; yellowtail flounder (Pleuronectes ferrugineus), Purchase et al., 2000). Larval haddock (Melanogrammus aeglefinus) grew faster when reared under continuous bright compared to dim light (Downing and Litvak, 1999a), though wide variability in feeding success and growth in relation to light intensity have been reported in larval fishes (Blaxter, 1986; Huse, 1994) and these variations are believed to be a function of species-specific natural light niches and stock origin (Job and Bellwood, 2000; Puvanendran and Brown, 2000). In the marine environment, as haddock change from larval to juvenile phases, they shift from the pelagic to demersal zone. This occurs at a body length of f2 – 3 cm when juveniles are characterized by a subterminal mouth and a natural diet consisting primarily of benthic invertebrates (Scott and Scott, 1988). The requirement of bright visual feeding conditions associated with planktivory presumably diminishes with this ontogenetic shift. Thus, the effect of light intensity on growth of haddock and other demersal marine fishes may be important and different cultivation strategies may be required for different life history phases. Improved fish growth in relation to photo regime has been attributed to a number of factors including higher food conversion efficiency, lower activity and lower oxygen consumption (Imsland et al., 1995; Appelbaum and Kamler, 2000). The objectives of the present study were to examine the effects of photoperiod and light intensity on growth and locomotor activity of juvenile haddock. In the first experiment, we examined the effects of natural photoperiod and continuous light on juvenile growth under two feeding regimes. In the second experiment, we broadened our study and examined juvenile growth in relation to natural photoperiod, 12, 16, 20, and 24 h illumination (in addition two light intensities were examined at 24 h light). Locomotor activity was evaluated under natural photoperiod and continuous light.
2. Method 2.1. Experiment 1 Haddock used in the first experiment were fish of mixed parental background raised from eggs produced by broodstock maintained at the St. Andrews Biological Station, New Brunswick, Canada. Prior to experimentation, larvae were maintained from May to July, 1998 in 7 m3 conical tanks containing filtered seawater (salinity f30 ppt; 7– 10 jC), fed wild zooplankton ad libitum, and weaned to a formulated dry food diet (Moore-Clark, Perla Marine, 400 – 700 Am) and maintained under continuous light (100 lx (f1.72 AE/s/
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m2) at water’s surface). On July 13, at a weight of 1 – 2 g, fish were transferred to 450-l tanks kept under continuous light (100 lx). On August 12, 360 juveniles of similar size were anaesthetized in MS-222 (60 mg/l) and wet weight (F0.1 g) and fork length (F0.1 cm) recorded (initial mean weight (SD) 4.38 g (F0.05 g)). Sixty fishes were randomly distributed into each of six square 450-l (110.45 m deep (water depth 0.30 m)) grey tanks with two replicates for each of three treatments (i) simulated natural photoperiod (NP), dry food delivered continuously during daylight phase using automatic belt feeder; (ii) 24 h light:0 h dark (LD 24:0), food delivery same as (i); and (iii) 24 h light:0 h dark (LD 24:0), food delivered continuously over 24 h. Fish were fed to satiation at f3% body weight per day (Corey Feed, Haddock Grower, pellet size 1 mm, 3 mm). In all treatments, fish foraged on pellets as they descended to the tank bottom as well as off the bottom. Fork length and body weight were recorded once every 4 weeks until the end of the 24-week experiment on January 27, 1999. Fulton’s condition factor (body weight/fork length3) x 100 was calculated once every 4 weeks. Specific growth rate (SGR) over 4-week periods was calculated based on means of treatment weights as: SGR ¼ 100 ðlnW2 lnW1 Þ=ðt2 t1 Þ where W2 and W1 are body weights (g) at days t2 and t1, respectively. Lights used were two fluorescent 60 cm tubes (Sylvania white 20 W bulbs F 20T12) per tank placed 1 m above the water’s surface. Simulated natural photoperiod was adjusted weekly using timers and changed from 14 h light:10 h dark at the beginning of the experiment to 10 h light:14 h dark at its cessation with the shortest daylength in December of f8 h 15 min (Fig. 1). Tanks were checked daily for mortalities and any dead fish removed. Water temperature was recorded throughout the experiment and changed seasonally (Fig. 1).
Fig. 1. Seasonal changes in water temperature and natural photoperiod at the St. Andrews Biological Station during the experimental periods of 1998 and 1999.
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2.2. Experiment 2 Haddock used in the second experiment were fish of mixed parental background raised from eggs produced by broodstock maintained at the Aquarium and Marine Center, Shippagan, New Brunswick. Prior to experimentation, larvae were maintained on a diet of n3 HUFA enriched rotifers and Artemia and weaned to a dry food diet (Biokiowa, 400– 700 Am). Fish were maintained from May to July, 1999 in 1.2 m3 circular tanks containing filtered seawater (salinity 30 ppt, 10– 12 jC) under continuous light (100 lx). On July 8, they were transferred by truck (6 h trip) in insulated tanks containing oxygenated water (f100% saturation) to the St. Andrews Biological Station where they were placed in a 5m3 tank under continuous light (100 lx) and maintained on a formulated dry food diet. On August 4, 600 juveniles of similar size were anaesthetized in MS-222 (60 mg/l) and wet weight (F0.1 g) and fork length (F0.1 cm) recorded (initial mean weight (SD) 5.38 g (F0.06 g)). Sixty fish were randomly distributed in each of 12 square 450-l tanks with two replicates for each of six treatments (i) simulated natural photoperiod (NP), (ii) 12 h light:12 h dark (LD 12:12), (iii) 16 h light:8 h dark (LD 16:8), (iv) 20 h light:4 h dark (LD 20:4), (v) 24 h light:0 h dark (LD 24:0), (i – v at 100 lx, f1.72 AE/s/m2), and (vi) 24 h light:0 dark (LD 24:0) at 30 lx, f0.20 AE/s/m2. Lower light intensity was achieved by covering the two fluorescent 60-cm tubes with shade cloth. Fish were fed to satiation at f3% body weight per day (Corey Feed, Haddock Grower, pellet size 1 mm, 3 mm) partitioned over three meals with food administered using automatic belt feeders (0800 – 0900 h 45% of ration, 1200 – 1300 h 20%, and 1600 –1700 h 35%). Initial fish size (4– 6 g) corresponded with the size at which juvenile haddock are customarily transferred from hatcheries to marine cage sites. Fork length and body weight were recorded once every 4 weeks until the end of the 24-week experiment on January 19, 2000. Locomotor activity was estimated f1 week after final body measurements and were recorded by counting the number of fish that passed through a fixed station in each of six tanks representing three treatments. Fixed stations were erected by vertically fixing two rods 30 cm apart to the bottom of a tank such that the space between them was centrally located in the tank. The rods were placed into tanks 3 days before counts were conducted. The number of fish that passed through the 3030 cm space between the rods (water depth in tanks was 30 cm) was recorded over a 1-min period. From January 24 – 28, 1 min activity measurements were recorded five times per day: 0830, 0930, 1030, 1530, and 2000 h for three treatments; natural photoperiod (100 lx), 24 h (100 lx), and 24 h (30 lx). A red light source was used to conduct night (2000 h) observations under natural photoperiod (40 W incandescent bulb CSA LR94262 located 1 m above water’s surface, light intensity 15 lx (f0.13 AE/s/m) at water’s surface). Fish showed no signs of being startled when the red light was turned on f1 h before movements were recorded as the vision of marine teleosts occurring in blue-green coastal waters is commonly not red-sensitive (Nicol, 1989). Data were tested for normality (Kolmogorov – Smirnov test) and homogeneity of variance (Levene statistic) (SPSS version 10.0). Single classification analysis of variance was used to determine if significant differences ( P<0.05) in fork length, body weight, condition factor and locomotor activity occurred between treatments. For attributes where significant differences occurred, the Duncan’s multiple range test (a=0.05) was used to
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determine whether treatments differed from one another. Tank effects were examined for each variable on each sampling date using a series of Bonferroni corrected t-tests (Trippel and Hubert, 1990). The tanks effects were minor (in 1998, 95% of the replicate tanks showed no significant difference ( P<0.05), and in 1999, 88% showed no difference). When differences did occur, they were small (f10%). For this reason, we pooled data of replicate tanks to conduct subsequent statistical analyses (e.g., ANOVA).
3. Results 3.1. Experiment 1 Haddock grew faster under continuous light than under simulated natural photoperiod. After 4 weeks, significantly greater body weights occurred under the two 24-h treatments compared to natural photoperiod (significant differences in fork length and condition Table 1 Fork length, body weight, and condition factor of haddock maintained for 24 weeks at three light/feeding regimes (NP=natural photoperiod) Photoperiod Week
NP (100 lx) NP Feed
24 h (100 lx) NP Feed
24 h (100 lx) 24 h Feed
Fork length (cm) 0 12/08/98 4 09/09/98 8 07/10/98 12 05/11/98 16 02/12/98 20 30/12/98 24 27/01/99
Date
7.25aF0.09 10.52bF0.12 12.78bF0.16 14.40bF0.18 15.56bF0.20 16.34bF0.21 17.01bF0.21
7.29aF0.09 10.96aF0.13 13.89aF0.14 16.10aF0.14 17.75aF0.16 18.82aF0.16 19.33aF0.17
7.31aF0.08 10.98aF0.12 13.89aF0.13 16.09aF0.13 17.66aF0.14 18.63aF0.14 19.19aF0.14
Body weight (g) 0 12/08/98 4 09/09/98 8 07/10/98 12 05/11/98 16 02/12/98 20 30/12/98 24 27/01/99
4.32aF0.17 13.71bF0.47 25.13bF0.95 35.62bF1.43 45.77bF1.89 53.79bF2.19 57.34bF2.26
4.38aF0.16 15.78aF0.52 33.50aF0.99 52.42aF1.43 73.02aF1.94 88.63aF2.30 91.47aF2.38
4.43aF0.14 15.79aF0.49 33.48aF0.91 51.76aF1.32 71.05aF1.73 86.06aF2.09 87.72aF2.19
Condition factor 0 12/08/98 4 09/09/98 8 07/10/98 12 05/11/98 16 02/12/98 20 30/12/98 24 27/01/99
1.06aF0.01 1.12aF0.01 1.14bF0.01 1.12bF0.01 1.14bF0.01 1.16bF0.01 1.10bF0.01
1.06aF0.01 1.14aF0.01 1.20aF0.01 1.22aF0.01 1.27aF0.01 1.29aF0.01 1.23aF0.01
1.09aF0.01 1.14aF0.01 1.21aF0.01 1.21aF0.01 1.26aF0.01 1.30aF0.01 1.21aF0.01
MeanFstandard error values are shown. Means sharing the same letter superscript on given dates are not significantly different (Duncan’s multiple range test, a=0.05).
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factor commenced at 8 weeks) (Table 1). After 24 weeks, haddock under 24 h light (natural photoperiod (NP) food delivery) and 24 h light (24 h food delivery) were significantly heavier (60% and 53%, respectively) than those under NP (Table 1). Timing
Fig. 2. Changes in daily specific growth rate (SGR) of haddock exposed to different photo regimes in 1998 and 1999. Unless indicated otherwise, all treatments were conducted at a light intensity of 100 lx. In 1998, two feeding regimes were used at 24 h, one in which food was administered over 24 h and the other during the daylight phase of natural photoperiod (NP). In 1999, a single feeding regime comprised of three meals per day was used for the six treatments.
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of food delivery did not significantly influence body growth at 24 h light (Table 1). Specific growth rate (weights) calculated over 28-day periods declined seasonally as fish became larger and water temperature cooled (Figs. 1 and 2). Weight gain was <7% during the final 4 weeks of the experiment at f2.5 jC. Percent survival over 24 weeks ranged from 82% to 92% among the three treatments. 3.2. Experiment 2 After 16 weeks, significantly greater body weights occurred at 20 and 24 h light than at 12 and 16 h light and natural photoperiod (Table 2). Body weight was significantly lower under natural photoperiod than at other light regimes and this difference was noted early (4 weeks) and maintained through the experiment (24 weeks). Low light intensity resulted in comparatively faster growth. After 24 weeks, significantly greater body weights (11.1%) occurred at 30 lx (24 h) than at 100 lx (24 h). Specific growth rates reflected the trend of faster growth in dim light (Fig. 2). The initial higher specific growth rates in 1998 Table 2 Fork length, body weight, and condition factor of haddock maintained for 24 weeks at six light regimes (NP=natural photoperiod) Photoperiod Week Date
NP (100 lx)
12 h (100 lx)
16 h (100 lx)
20 h (100 lx)
Fork length (cm) 0 04/08/99 4 01/09/99 8 29/09/99 12 27/10/99 16 24/11/99 20 22/12/99 24 19/01/00
7.61aF0.07 7.64aF0.07 10.38aF0.09 10.37aF0.09 12.90aF0.08 13.03aF0.08 14.76cF0.09 15.23abF0.09 16.19dF0.10 16.78bcF0.10 17.52dF0.11 18.13bcF0.11 18.20dF0.13 18.86cF0.12
7.67aF0.07 10.40aF0.09 13.00aF0.08 15.07bF0.08 16.62cF0.09 17.95cF0.10 18.76cF0.11
7.67aF0.07 7.69aF0.07 7.54aF0.08 10.38aF0.09 10.40aF0.10 10.23aF0.11 13.09aF0.09 13.04aF0.09 13.08aF0.10 15.24abF0.09 15.04bF0.10 15.39aF0.11 16.93bF0.11 16.76bcF0.10 17.26aF0.11 18.36bF0.12 18.26bcF0.11 18.50aF0.11 19.26bF0.12 19.20bF0.12 19.79aF0.12
Body 0 4 8 12 16 20 24
5.54aF0.13 5.63aF0.14 a 13.20 F0.33 13.25aF0.34 26.94bF0.55 28.37abF0.59 40.78cF0.86 45.70bF0.96 54.99dF1.17 62.99bcF1.24 64.77dF1.46 72.26cF1.54 74.56dF1.71 82.61cF1.86
5.56aF0.13 13.43aF0.33 28.16abF0.57 44.78bF0.94 59.81cF1.27 71.23cF1.54 82.07cF1.77
5.60aF0.14 5.84aF0.15 5.46aF0.16 a a 12.80 F0.31 13.61 F0.38 13.02aF0.42 28.12abF0.54 28.62abF0.63 29.33aF0.67 46.94abF0.88 44.70bF0.96 49.46aF1.05 65.16bF1.19 64.50bF1.25 69.56aF1.39 78.02bF1.51 77.29bF1.57 85.05aF1.52 91.11bF1.78 92.05bF1.81 102.26aF2.00
weight (g) 04/08/99 01/09/99 29/09/99 27/10/99 24/11/99 22/12/99 19/01/00
Condition factor 0 04/08/99 4 01/09/99 8 29/09/99 12 27/10/99 16 24/11/99 20 22/12/99 24 19/01/00
1.24abF0.01 1.15bF0.01 1.23cF0.01 1.25dF0.01 1.27cF0.01 1.18dF0.01 1.21cF0.01
1.24abF0.01 1.16bF0.01 1.26abF0.01 1.27cdF0.01 1.31bF0.01 1.19cdF0.01 1.21cF0.01
1.21aF0.01 1.16bF0.01 1.26abF0.01 1.29bcF0.01 1.28cF0.01 1.21cF0.01 1.22cF0.01
1.22aF0.01 1.12aF0.01 1.24bcF0.01 1.31abF0.01 1.33abF0.01 1.24bF0.01 1.26bF0.01
24 h (100 lx) 24 h (30 lx)
1.26bF0.01 1.17bF0.01 1.27aF0.01 1.29bcF0.01 1.35aF0.01 1.25bF0.01 1.28abF0.01
1.23abF0.01 1.16bF0.01 1.28aF0.01 1.33aF0.01 1.34abF0.01 1.34aF0.01 1.30aF0.01
MeanFstandard error values are shown. Means sharing the same letter superscript on given dates are not significantly different (Duncan’s multiple range test, a=0.05).
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Fig. 3. Number of haddock (meanFstandard error) that moved through a fixed station under three different photo regimes during the period January 24 – 28, 2000. Counts were conducted during five periods: Before Feeding: just prior to loading of belt feeders, Feed Preparation: immediately after belt feeders have been loaded, First Feeding: coincides with first meal, After Feeding: between second and third meals, and Evening: natural photoperiod (NP) represents darkness (red light used to conduct counts). Statistically significant differences in activity occurred between each of the three photo regimes at each time of day evaluated (Duncan’s multiple range test, a=0.05).
compared to 1999 occurred under warmer water temperatures, i.e., natural photoperiod SGRs were 4.2% and 3.2%/day at 14.1 and 12.4 jC, respectively (Figs. 1 and 2). Percent survival over 24 weeks ranged from 94% to 96% among the six treatments. Haddock locomotor activity was the greatest under natural photoperiod (100 lx), less at 24 h (100 lx), and lowest at 24 h (30 lx) (Fig. 3). Fish under natural photoperiod (100 lx) passed through the fixed station approximately twice as often as those at 24 h (30 lx). Under natural photoperiod, activity rates varied through the day with activity being lowest in the mid-afternoon and evening and highest during the loading of belt feeders in the morning. Night activity levels under natural photoperiod remained higher than those at 24 h light.
4. Discussion Extended daylength significantly improved growth of juvenile haddock. Improved appetite, greater ration and higher food conversion efficiency are factors commonly reported to be responsible for faster teleost growth under continuous light (Saunders and Henderson, 1970; Folkvord and Ottera˚, 1993). Changes in endocrine functioning as a
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result of photo regime likely play a key role in this response (Porter et al., 2001). Whether extended daylength continues to have a beneficial effect on haddock growth after the first summer and autumn is uncertain and requires further investigation. Given the cold winter temperatures in the Bay of Fundy (f2– 3 jC) and associated slow growth, any extended gains in growth would presumably occur during the subsequent spring to autumn period. Although the application of continuous light (and 20 h light) resulted in the greatest growth response, it is worth noting that the other seasonally unchanging photoperiods (12 and 16 h light) resulted in faster growth than natural photoperiod; a result similar to that observed in Atlantic salmon (Saunders et al., 1985). Moreover, it is of interest that two discrete growth responses were observed (12 and 16 h compared to 20 and 24 h light) (Table 2). It is unclear why an additional 4 h of light from 16 to 20 h improved growth, but an extra 4 h had no effect between other treatments (i.e., from 12 to 16 h and 20 to 24 h). In juvenile turbot (maintained at natural photoperiod, 16 h light:8 h dark, and 24 h light:0 h dark), continuous light slightly enhanced the growth rate above that of other regimes, after 3 months of exposure at 10 and 16 jC, but not throughout the 6 month experiment (Imsland et al., 1995). However, in a recent paper (Imsland et al., 1997), better long-term growth (18 months) of turbot occurred when exposed to extended daylength during the first winter. In Sebastes diploproa, the positive effects of constant illumination on growth were related to a greater scope for growth and due to their lower standard metabolic rate (Boehlert, 1981). It is often not possible to determine if the light effect on growth depends on food consumption or better food utilization. Similar growth of haddock between the two feeding regimes in Experiment 1 suggests that an extended feeding period does not enhance growth under equivalent daily rations. Thus, haddock may be capable of reaching satiation during a feeding period equivalent to natural daylength, as observed for Atlantic salmon in sea cages (Kra˚kenes et al., 1991). In green sunfish (Lepomis cyanellus) maintained for 6 weeks at four photoperiods (constant 8 h light:16 h dark, 16 h light:8 h dark, increasing 8 – 16 h light and decreasing 16– 8 h light), Gross et al. (1965) demonstrated greater food intake occurred under longer daylength. Fish growth and food conversion efficiency also were closely correlated and were generally highest in the increasing photoperiod. As noted in Boeuf and LeBail’s (1999) review of the subject, Gross et al. (1965) were the first to specify that growth might be influenced by light through a better food conversion efficiency and not just stimulated food intake. Reduced light intensity, from 100 to 30 lx, at 24 h light, led to improved juvenile growth of haddock. Consequently, dim continuous light appears to be the best strategy of those investigated. This low light level is more characteristic of their natural habitat at 60 –120 m on offshore banks in the Northwest Atlantic (Beamish, 1966; Jerlov, 1968; Scott and Scott, 1988; Nicol, 1989; Puvanendran and Brown, 2000). Locomotor activity indicated that juvenile haddock swim less at low light and this may translate into metabolic savings and increased body mass. Swimming activity is a bioenergetic component not frequently related to improved growth efficiency and larger body mass of cultivated fish (Jorgensen and Jobling, 1991). African catfish (Clarias gariepinus) under reduced light, swam less and used less oxygen with more energy channeled into growth (Appelbaum and Kamler, 2000). In another demersal species, Atlantic halibut, Hole and Pittman (1995) observed the best growth at 1 to 10 lx, compared to 500 lx (12 h light at 11 and 14 jC).
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Effects of light intensity on Atlantic salmon postsmolt growth in net pens have shown mixed results, with enhanced summer and autumn growth occurring when light-reducing black polyethylene netting covers were deployed for 1 year (Huse et al., 1990). In another experiment, Atlantic salmon postsmolts exposed to high light intensity in sea pens showed significantly better growth (Oppedal et al., 1997). Swimming activity among individual haddock was less variable (low standard errors) at 24 h light (30 lx) relative to 24 h light (100 lx) and natural photoperiod (100 lx) (Fig. 3). Further observations of haddock following Experiment 2 in February – May, 2000 revealed that by shifting photoperiod and light intensity, their activity patterns could be altered (E.A. Trippel, unpublished data). When measurements of activity were made 3 days after shade cloth was removed from the 24 h light (30 lx) treatment (raising it to 100 lx), the activity rate had increased and was equivalent to the 24 h light (100 lx) treatment (the reverse was also achieved). Thus, the behavioural responses to light appear to be quite flexible. Interestingly, haddock activity was greater during darkness than in light under, either of the two 24 h light regimes (i.e., during the 2000 h observation period, which was initiated f4 h after darkness in natural photoperiod) (Fig. 3). Thus, the dark phase of natural photoperiod did not have a great impact in reducing swimming activity. The greater movement during light and dark phases under natural photoperiod compared to 24 h light presumably resulted in additional oxygen consumption and energy expended, which could have been diverted to growth. Although not specifically measured, haddock at 24 h light (30 lx) relative to other treatments appeared to require lower rations (via visual observations of remaining uneaten food) and this facet of their diet requires further examination. If true, then food conversion efficiency is better under dim constant illumination and would help to reduce food costs for commercial culture. Consequently, haddock photo regime (periodicity and intensity) could have a significant effect on the culture of haddock during the 3 – 100 g phase when seasonal water temperatures support good growth. The seasonal duration that photo regime enhances growth could be further extended in a land-based facility in which water temperature can be controlled. Differences in specific growth rates between 1998 and 1999 may in part be related to differences in seasonal water temperatures between the two years (Figs. 1 and 2). In Experiment 1, the summer temperature was higher and winter temperature lower than in Experiment 2. The growth differences between natural photoperiod and 24 h light were greater in Experiment 1, perhaps initiated by the higher early period temperature. At the completion of Experiment 2, there was much less of a growth difference between natural photoperiod and 24 h light (22% compared to 53 –60% in Experiment 1), but the higher temperature by f2 jC during winter was associated with faster December – January growth compared to Experiment 1. Fish culturists need to recognize that the scope for improving growth through photo manipulation is apparently associated with ambient water temperature. Inspection of the specific growth rates in Fig. 2 suggests that the effect of photoperiod declined as temperatures decreased in late autumn and winter. It would be of interest to further explore the interaction between photoperiod and temperature under controlled temperature conditions. Other contributing factors include diet composition and parental origin. As a preliminary analysis, Iwama and Tautz’s (1981) growth coefficient ( Gc) was calculated for each treatment from each experimental year. This measure is useful in that it allows the comparison of the growth of fish at different sizes, reared at
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different temperatures. Growth coefficients for 1998 (all at 100 lx) were: 36.4 (NP, NP feed), 62.4 (24 h light, NP feed), and 60.0 (24 h light, 24 h feed). Growth coefficients for 1999 (all at 100 lx unless indicated) were: 42.4 (NP), 48.1 (12 h light), 47.2 (16 h light), 53.3 (20 h light), 52.8 (24 h light), and 59.6 (24 h light, 30 lx). These trends reflect the results presented. Note, however, at natural photoperiod, Gc was substantially lower in 1998 (36.4) than in 1999 (42.4) suggesting that other factors in addition to temperature and fish size could have contributed to the growth differences in 1998 and 1999. To maximize production, the present study on juveniles and the results of Downing and Litvak (1999a,b) on larval haddock indicate there is a period in the ontogeny during which bright light which increases forage success of highly visual feeders should be dimmed and this perhaps coincides with changes in body morphology and behaviour adapted for benthic feeding. Continuous light also has been reported to reduce the incidence of sexual maturity in some teleosts (Hansen et al., 1992; Oppedal et al., 1997; Jourdan et al., 2000), and supports the widespread applicability of photoperiod manipulation to finfish aquaculture (Boeuf and LeBail, 1999). Recently, many Atlantic salmon farmers in Norway and Scotland began using continuous lighting during the autumn or winter (October –April) to improve growth, as growth of fish subjected to natural daylight is lowered during the autumn and winter, while, conversely, no such growth depression is observed during winter under a continuous light regime (Forsberg, 1995). In a recent study (Oppedal et al., 1997), when light intensity was sufficient, abrupt changes in exposure of Atlantic salmon from natural short daylength to continuous additional illumination (January – June) promoted growth without initiating maturation. Besides application to aquaculture, the findings on light intensity are also relevant to our understanding of fish behaviour in the natural environment. Aquatic ecosystems, both freshwater and marine, often undergo changes in clarity which affect light transmission. Thus, fish in part may alter their depth distribution in relation to preferred light intensities (Job and Bellwood, 2000). The degree that light intensity and photoperiod affect locomotion and growth is worthy of study for other fishes from both aquaculture and environmental perspectives. Acknowledgements We thank J. Bowers, P. Harmon, K. Madsen, T. Shepherd, and T. Taylor for laboratory assistance and appropriate care of fish. C. Lanteigne of the Aquarium and Marine Center located in Shippagan, NB, kindly provided haddock for experimental use. J. Castell and P. Harmon provided helpful comments on an earlier draft. Two anonymous reviewers also assisted in improving the manuscript for which the authors are grateful. Financial support for the project was provided in part by the Department of Fisheries and Oceans Science Youth Internship Program and Heritage Aquaculture, Blacks Harbour, NB. References Appelbaum, S., Kamler, E., 2000. Survival, growth, metabolism and behaviour of Clarias gariepinus (Burchell 1822) early stages under different light conditions. Aquac. Eng. 22, 269 – 287.
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Barlow, C.G., Pearce, M.G., Rodgers, L.J., Clayton, P., 1995. Effects of photoperiod on growth, survival, and feeding periodicity of larval and juvenile barramundi, Lates calcarifer (Bloch). Aquaculture 138, 159 – 168. Beamish, F.W.H., 1966. Vertical migration by demersal fish in the Northwest Atlantic. J. Fish. Res. Board Can. 23, 109 – 139. Blaxter, J.H.S., 1986. Visual thresholds and spectral sensitivity of flatfish larvae. J. Exp. Biol. 51, 221 – 230. Boehlert, G.W., 1981. The effects of photoperiod and temperature on laboratory growth of juvenile Sebastes diploproa and a comparison with growth in the field. Fish. Bull. 79, 789 – 794. Boeuf, G., LeBail, P.Y., 1999. Does light have an influence on fish growth? Aquaculture 1777, 129 – 152. Downing, G., Litvak, M.K., 1999a. The effect of photoperiod, tank colour and light intensity on growth of larval haddock. Aquac. Int. 7, 369 – 382. Downing, G., Litvak, M.K., 1999b. The influence of light intensity on growth of larval haddock. N. Am. J. Aquac. 61, 135 – 140. Folkvord, A., Ottera˚, H., 1993. Effects of initial size distribution, day length, and feeding frequency on growth, survival, and cannibalism in juvenile Atlantic cod (Gadus morhua L.). Aquaculture 114, 243 – 260. Forsberg, O.I., 1995. Empirical investigations on growth of post-smolt Atlantic salmon (Salmo salar L.) in landbased farms. Evidence of a photoperiodic influence. Aquaculture 133, 235 – 248. Fuchs, J., 1978. Influence de la photoperiode sur la croissance et la survie de la larve et du juvenile de sole (Solea solea) en e´le´vage. Aquaculture 15, 63 – 74. Gross, W.L., Roelofs, E.W., Fromm, P.O., 1965. Influence of photoperiod on growth of green sunfish, Lepomis cyanellus. J. Fish. Res. Board Can. 22, 1379 – 1386. Hansen, T., Stefansson, S., Taranger, G.L., 1992. Growth and sexual maturation in Atlantic salmon, Salmo salar L., reared in sea cages at two different light regimes. Aquac. Fish. Manage. 23, 275 – 280. Hole, G., Pittman, K., 1995. Effects of light and temperature on growth in juvenile halibut (Hippoglossus hippoglossus L.). In: Pittman, K., Batty, R.S., Verreth, J. (Eds.), ICES Marine Science Symposia, Mass Rearing of Juvenile Fish. Bergen, 21 – 23 June 1993, vol. 201, p. 197. Huse, I.J., 1994. Feeding at different illumination levels in larvae of three marine teleost species: cod, Gadus morhua L., plaice, Pleuronectes platessa L., and turbot, Scophthalmus maximus (L.). Aquac. Fish. Manage. 25, 687 – 695. Huse, I., Bjordal, A., Ferno¨, A., Furevik, D., 1990. The effect of shading in pen rearing of Atlantic salmon (Salmo salar). Aquac. Eng. 9, 235 – 244. Imsland, A., Folkvord, A.F., Steffansson, S.O., 1995. Growth, oxygen consumption and activity of juvenile turbot (Scophthalmus maximus L.) reared under different temperatures and photoperiods. Neth. J. Sea Res. 34, 149 – 159. Imsland, A.K., Folkvord, A.F., Jo´nsdo´ttir, O.D.B., Steffansson, S.O., 1997. Effects of exposure of extended photoperiods during the first winter on long-term growth and age at first maturity in turbot (Scophthalmus maximus). Aquaculture 159, 125 – 141. Iwama, G.K., Tautz, A.F., 1981. A simple growth model for salmonids in hatcheries. Can. J. Fish. Aquat. Sci. 38, 649 – 656. Jerlov, N.G., 1968. Optical Oceanography. Elsevier, Amsterdam. Job, S.D., Bellwood, D.R., 2000. Light sensitivity in larval fishes: implications for vertical zonation in the pelagic zone. Limnol. Oceanogr. 45, 362 – 371. Jorgensen, E.H., Jobling, M., 1991. The effects of exercise on growth, food utilization and osmoregulatory capacity of juvenile Atlantic salmon, Salmo salar. Aquaculture 116, 233 – 246. Jourdan, S., Fontaine, P., Boujard, T., Vandeloise, E., Gardeur, J.N., Anthouard, M., Kestemont, P., 2000. Influence of daylength on growth, heterogeneity, gonad development, sexual steroid and thyroid levels, and N and P budgets in Perca fluviatilis. Aquaculture 186, 253 – 265. Kiyono, M., Hirano, R., 1981. Effects of light on the feeding and growth of black porgy, Mylio macrocephalus (Basilewsky), postlarvae and juveniles. Rapp. et proces-verbaux des re´unions. Cons. Inter. Explor. Mer 178, 334 – 336. Kra˚kenes, R., Hansen, T., Stefansson, S.O., Taranger, G.L., 1991. Continuous light increases growth rate of Atlantic salmon (Salmo salar L.) postsmolts in sea cages. Aquaculture 95, 281 – 287. Nicol, J.A.C., 1989. The Eyes of Fishes. Clarendon Press, Oxford, UK. Oppedal, F., Taranger, G.L., Juell, J., Fosseidengen, J.E., Hansen, T., 1997. Light intensity affects growth and
E.A. Trippel, S.R.E. Neil / Aquaculture 217 (2003) 633–645
645
sexual maturation of Atlantic salmon (Salmo salar L.) postsmolts in sea cages. Aquat. Living Resour. 10, 351 – 357. Porter, M.J.R., Duncan, N., Handeland, S.O., Stefansson, O., Bromage, N.R., 2001. Temperature, light intensity and plasma melatonin levels in juvenile Atlantic salmon. J. Fish Biol. 58, 431 – 438. Purchase, C.F., Boyce, D.L., Brown, J.A., 2000. Growth and survival of juvenile flounder Pleuronectes ferrugineus (Storer) under different photoperiods. Aquac. Res. 31, 547 – 552. Puvanendran, V., Brown, J.J., 2000. Effect of light intensity on the foraging and growth of Atlantic cod larvae: interpopulation difference? Mar. Ecol., Prog. Ser. 167, 207 – 214. 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. 27, 1295 – 1311. 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. Scott, W.B., Scott, M.G., 1988. Atlantic fishes of Canada. Can. Bull. Fish. Aquat. Sci. 219, 274 – 276. Simensen, L.M., Jonassen, T.M., Imsland, A.K., Stefansson, S.O., 2000. Photoperiod regulation of growth of juvenile Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 190, 119 – 128. Trippel, E.A., Hubert, J.J., 1990. Common statistical errors in fishery research. In: Hunter, J. (Ed.), Writing for Fishery Journals. American Fisheries Society, Bethesda, MD, pp. 93 – 102.