|TIMING AND DURATION OF CONSTANT LIGHT AFFECTS RAINBOW TROUT (ONCORHYNCHUS MYKISS) GROWTH DURING AUTUMN-SPRING GROW-OUT IN FRESHWATER
Taylor, J.F.* and Migaud, H.
Institute of Aquaculture, University of Stirling, Stirling, Scotland, FK9 4LA.
*Author Correspondence: Dr. John F. Taylor
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Photoperiod; duration; timing; growth; Oncorhynchus mykiss
Photoperiod enhancement of growth is becoming an area of increasing interest as a means of enhancing rainbow trout production efficiency in commercial practice. This paper examines the possible implications of shortening periods of constant light (LL) exposure on rainbow trout growth during autumn-spring grow out under ambient water temperatures in freshwater to portion size. Triplicate groups of juvenile all-female rainbow trout were permanently exposed to LL in October, November, December or January. Growth was monitored and compared to those maintained under a simulated natural photoperiod (SNP) until the following May. Permanent exposure to LL (all treatments) resulted in significantly greater weight gain of rainbow trout than those under SNP. Furthermore, greatest growth was achieved when fish were left permanently exposed to LL from October. These findings suggest there may be implications for fish farmers if the period of photoperiod exposure is reduced, or timing of application is not considered with regards to ambient water temperatures.
Previous trials have demonstrated that exposure of juvenile rainbow trout (Oncorhynchus mykiss) to periods of constant light (LL) or long-days can significantly improve growth rates relative to those maintained under ambient conditions (Mason, Gallant, & Wood, 1991; Makinen & Ruhonen, 1992; Taylor, North, Porter, Bromage, & Migaud, 2006). However, the duration of LL and the actual timing of exposure to LL has not yet been determined in relation to optimising growth enhancement during autumn-spring grow-out in portion size rainbow trout in freshwater. It has been clearly shown in Atlantic salmon (Salmo salar) that the longer the exposure to LL, the longer the period that higher growth rates will be maintained, suggesting a direct photostimulation of growth (Taranger, Haux, Hansen, Stefansson, Bjornsson, Walther & Kryvi, 1999; Endal, Taranger, Stefansson & Hansen, 2000). However, it was also evident that enhanced growth was maintained after salmon were returned to natural photoperiod following LL application suggesting that photoperiod is adjusting seasonal growth and appetite rhythms, rather than as a consequence of direct photostimulation (Kadri, Metcalfe, Huntingford & Thorpe, 1997; Nordgarden, Oppedal, Hansen & Hemre, 2003; Oppedal, Berg, Olsen, Taranger, & Hansen, 2006). If direct photostimulation of growth does occur then the stimulatory effect would last only as long as additional light was applied (Johnston, Manthri, Smart, Campbell, Nickell & Alderson, 2003). However, more recently it has been demonstrated in Atlantic salmon that muscle fibre recruitment is enhanced following initial LL application in autumn rather than muscle hypertrophy. It was also postulated that the earlier the onset of LL the greater the effect on recruitment there may be. Once recruitment ceases, growth occurred only via hypertrophy of fibres previously formed (Johnston, et al., 2003; Johnston, Manthri, Bickerdike, Dingwall, Luijkx, Campbell, Nickell & Alderson, 2004).
Temperature has been shown to act synergistically with photoperiod in a rate-controlling manner on growth response following photoperiod manipulation in numerous species (Clarke, Shelbourn & Brett, 1978; Solbakken, Hansen & Stefansson, 1994; Hallaraker, Folkvord & Stefansson, 1995; Jonassen, Imsland, Kadowaki & Stefansson, 2000). This is particularly important with regards to the use of photoperiod regimes during the winter period in which temperature may limit the physiological response. In juvenile Atlantic salmon, and both underyearling coho and sockeye salmon the growth response during photoperiod manipulation was greater at higher temperatures in autumn (Clarke et al. 1978; Clarke, Shelbourn & Brett, 1981; Saunders, Specker & Komourdjian, 1989). Thorpe, Adams, Miles & Keay, (1989) suggested a greater opportunity for growth as represented by degree-daylight hours in mid to late summer, in which a greater proportion of juvenile salmon would maintain rather than arrest growth. Similar responses have been observed in Atlantic salmon whereby increasing day-lengths did not enhance growth when temperatures were low, while artificially elevating temperatures during late winter and early spring in association with exposure to LL successfully enhanced growth (Saunders, Henderson & Harmon, 1985; Solbakken et al. 1994). This rate-controlling regulation may relate in part to the modulatory effect of the somatotropic axis hormones (GH-IGF-I) which have been shown to be influenced by temperature (Beckman, Larsen, Moriyama, Lee-Pawlak & Dickhoff, 1998; Larsen, Beckman & Dickhoff, 2001) in addition to feed intake (Pierce, Beckman, Shearer, Larsen & Dickhoff, 2001; Beckman, Shimizu, Gadberry & Cooper, 2004) and photoperiod (McCormick, Moriyama & Bjornsson, 2000; Taylor, Migaud, Porter & Bromage, 2005). Thus the timing of photoperiod application and the subsequent response should be given careful consideration with regards to ambient temperatures.
At present, the UK trout industry does not employ lighting regimes in portion-size fish. However, there is a growing interest in the potential to use artificial lighting to promote growth during autumn-spring grow out, a period associated with naturally poor performance under ambient conditions (Taylor et al. 2006), and thus use light to increase productivity. Evaluation of such approaches could provide simple and cost effective means which could be applied within the industry, and furthermore, may add to the limited knowledge of the physiological effects of photoperiod manipulation on the mechanisms controlling trout growth. In this respect, this paper examines implications of different timing of exposure and duration of LL application on growth performance of rainbow trout during autumn to spring grow-out.
Materials and methods
On 24th October 2002 groups of 50 all-female rainbow trout (90.0 ± 1.6g, mean ± SEM, Glen Wyllin origin, hatch May 2001) previously reared under natural photoperiod and water temperature (2.3-15°C) were exposed to one of 5 photoperiod treatments in triplicate. One triplicate group was maintained under simulated natural photoperiod (SNP: range 7-17.25 hours daylight) as a control treatment throughout the experiment. The remaining four triplicate groups were exposed to constant light (LL) on 24th October (LL-OCT), 20th November (LL-NOV), 18th December (LL-DEC) and 20th January (LL-JAN) until 26th May 2003 (Figure. 1).
The experiment was conducted at the Niall Bromage Freshwater Research Facility (52°30’N) with freshwater supplied to all tanks by gravity from an upstream reservoir. Fish were reared in 1.38m3 circular flow-through fibreglass tanks (start SD 16kg/m3). Flow rates to all tanks were maintained at 10L sec-1 with DO maintained above 7mg L-1, pH 6.5-6.8, and ambient water temperature (Fig. 1). Light was supplied by two 9 watt equivalent G23 bulbs (RS components Ltd., Northants, UK) housed in one aluminium alloy bulkhead fittings positioned centrally in the lightproof lid creating 0.2 Wm-2 on the tank floor. Simulated natural photoperiod regimes were controlled using a photosensitive switch (RS Components Ltd., Northants, UK), while lighting to LL tanks was permanently switched on. Fish in all treatments were fed a commercial dry diet (Trouw Elips-S 4mm pellet) to satiation (0.5% above recommended feeding tables) via automated feeders during the daylight hours of the SNP treatment with all treatments presented an identical ration, however direct feed intake through waste feed collection was not determined.
All fish from all treatments (n=48-50) were anesthetised with 2-phenoxyethanol (1:10,000 dilution, Sigma, UK), individually measured for weight (W) (± 0.1g) and fork length (L) (± 0.5mm) at monthly intervals, recovered in well aerated water and returned to their respective photoperiod treatment tank. Condition factor (K) was calculated from the measured length and weight of individual fish such that: K = (WL-3)x100. Mortalities were less than 4% during the experiment. Specific growth rates (SGR) were calculated such that: SGR = (eg-1) x 100, where g = (LnX2 – LnX1) / t2 – t1 and X2 and X1 are W or L at times t2 and t1 respectively. A starting SGR in October was based on the fish stock growth prior to experimentation during the previous month while held at the facility.
Differences in growth performance (W, L, K and SGR) were analysed using a nested ANOVA, in which treatment tanks were nested as a random factor within the dependent factor photoperiod at a given sampling point. Data complied with normality and homogeneity of variance tests. No replicate differences were found within photoperiod treatments. For post-hoc multiple comparisons, Tukey’s test was used with a significance level of 5% (p<0.05). All statistical analysis were undertaken using Minitab Statistical Package v14.1.
All treatments increased W steadily over the duration of the trial. LL-OCT achieved and maintained a significantly higher mean W than all other treatments by March 2003 (Fig. 2a). LL-NOV, LL-DEC, and LL-JAN treatments reached a significantly heavier weight than SNP by April 2003 that was maintained until the end of the experiment (Fig. 2a), concurrent with a significantly higher SGR during this period with the exception of LL-JAN (Fig. 2b). Overall weight gain advantage relative to SNP final weight in May was 21% for LL-OCT and 11% for LL-NOV, LL-DEC, and LL-JAN treatments respectively.
L increased steadily in all treatments throughout the experiment, with all LL exposures achieving a significantly longer L than SNP during May 2003, with no differences between LL treatments apparent (data not shown).
In general, weight SGR followed a similar pattern in LL and SNP treatments, showing a significant decrease from October to November 2002, concurrent with the rapid fall in temperature, before slowly increasing from November to February 2003 (Fig. 2b). Between March and May 2003 SGR increased steeply in all LL treatments with LL-OCT, LL-NOV, LL-DEC achieving a significantly higher SGR than SNP in April. In May all LL treatments achieved a significantly higher SGR than SNP.
All treatments maintained a steady K between October and November, which was followed by a dramatic decrease in all groups in December 2002 (Fig. 2c). The control SNP then showed a gradual increase in K from December 2002 to March 2003, followed by a decrease in April, only to rise again during May. K in both LL-OCT and LL-NOV increased between December and February achieving a significantly higher K value than SNP, but not in the LL-DEC or LL-JAN groups. K in both treatments then increased through April and May achieving a significantly higher K than SNP. Fish in LL-DEC and LL-JAN groups only displayed a significantly higher K value than SNP in April and May. Significant differences in K were not apparent between any of LL treatments in April or May.
The present study provides clear evidence that abrupt changes from natural photoperiod to LL in October, November, December or January enhances weight gain of portion-size rainbow trout in freshwater. Moreover, maximum growth enhancement was achieved following permanent exposure to LL from October. Furthermore, although conducted at an experimental level SGRs obtained in our study were representative of those observed under full-scale commercial conditions (Taylor et al., 2006) suggesting our findings could provide practical tools directly applicable to industry.
These growth enhancing effects of LL are in accordance with those previously observed in juvenile and adult Atlantic salmon (Saunders et al. 1985; Stefansson, Naevdal & Hansen, 1989; Solbakken et al. 1994; Oppedal, Taranger, Juell, Fosseidengen & Hansen, 1997), Pacific salmonids (Clarke 1990), and provides further support to the limited knowledge of photoperiod effects on growth in rainbow trout (Mason et al. 1991; Makinen & Ruhonen 1992; Taylor et al. 2005). However, care must be taken when drawing comparisons between rainbow trout and other salmonid species, in particular freshwater and post-smolt stages. The use of LL from autumn-winter through to June in Atlantic salmon culture is an industry standard principally used to inhibit early maturation pre-harvest (Hansen, Stefansson & Taranger, 1992; Hansen, Stefansson, Taranger, & Norberg, 2000), the subsequent effect being the reallocation of energy from gonadal development into somatic tissue growth. This however is not an issue in all-female portion-size rainbow trout production (250-300g) which do not typically mature at this size. Although maturity was not assessed in the current experiment, we have extensively used this strain in other studies and observe no maturity before 3years old in females. Equally it is difficult to dissociate growth from smoltification when looking at freshwater stages of salmon (Skilbrei, Hansen & Stefansson, 1997; Duncan & Bromage, 1998).
Nonetheless, our study suggests that the earlier the exposure and the longer the duration of LL in rainbow trout, the greater the degree of enhanced growth, supporting a direct photostimulation of growth theory. Similarly, in Atlantic salmon it was shown that longer exposure maintains a higher growth rate for a longer period (Taranger et al. 1999; Endal et al. 2000). Oppedal, Taranger, Juell & Hansen, (1999) also found no difference in the pattern or rate of growth in underyearling Atlantic salmon exposed to LL for a short period of time, 12 weeks, whereas a previous study only observed an effect 18 weeks post-light exposure (Oppedal, et al. 1997). It has been proposed that fish are unable to synchronise their endogenous rhythms under rapidly increasing and decreasing artificial photoperiod (Clarke et al. 1978; Villarreal, Thorpe & Miles, 1988). Certainly the earlier application in October in conjunction with the greatest growth could suggest a phase shift relative to the other LL treatments, yet no differences in growth were observed between the other LL treatments although they did achieve a larger weight than the SNP treatment. In this respect our data does not support the idea of an endogenous rhythm of growth in rainbow trout although further studies are needed to clarify the situation. Conversely, Nordgarden et al., (2003) reported a clear seasonal profile of growth, condition and feed intake in Atlantic salmon, and that improved growth under LL was associated with improved FCR and increased appetite. As such both FCR and feed intake should be monitored accurately in future trials under the given light treatments in order to draw firm conclusions with regards to rainbow trout. Although waste feed was not monitored in our study, fish were fed to excess and differences in growth due to under-feeding would seem unlikely.
Regarding changes in length no significant differences were observed between LL treatments and SNP despite the former treatments achieving significantly greater weights. Only during the May did LL groups achieve a greater length than SNP. As a result, LL treated fish achieved significantly higher K factors than SNP in spring. Seasonal growth patterns under endogenous control which can be manipulated by light treatment have been demonstrated in Atlantic salmon (Nordgarden et al. 2003; Oppedal, et al., 2006). Typical patterns have shown a tendency towards greater skeletal growth during the winter months, providing the frame for muscle gain in spring (Björnsson et al., 2000). In this respect, Johnston et al. (2003) reported significantly enhanced weight gain of Atlantic salmon 18 weeks post LL exposure. A shift towards greater muscle fibre recruitment was observed during the first 40 days of LL exposure, subsequently followed by muscle hypertrophy. Interestingly within our study, LL-OCT and LL-NOV achieved a significantly higher K before LL-DEC and LL-JAN treatments, suggesting greater muscle gain given that treatments were of the same length during this period. This difference could relate to a longer period of muscle fibre recruitment following the earlier application of light. A future study examining muscle fibre dynamics may reveal the underlying mechanism in rainbow trout.
Finally, in the present study, greatest weight gain was observed in LL applied as of October relative to all other LL treatments. Together with the possible involvement of a phase advancement of a seasonal growth pattern, the greater growth may also be explained by the higher water temperatures at which the light regime was initially applied (12ºC in Oct versus 2-4ºC Nov-Jan). Since fish are ectothermic, then many of their physiological processes are regulated by the thermal regime, with optimum ranges for a variety of freshwater and marine species (Saunders et al. 1985; Solbakken et al. 1994; Hallaraker, et al. 1995; Jonassen, et al. 1999). Numerous studies have shown that changes in growth rate caused by photoperiod treatment in other salmonids were apparent sooner at higher temperatures than at lower ones (Clarke et al. 1978; Clarke et al. 1981; Saunders et al. 1985; Solbakken et al. 1994). Thus, temperature is considered as a rate-controlling factor, whereas light would be classified as a directive factor that stimulates the endocrine system (Bromage, Randall, Duston, Thrush & Jones, 1994). More rapid increases in circulating GH and IGF-I have been found in relation to higher temperatures (Beckman et al. 1998; Larsen et al. 2001) and increasing or long-day photoperiods (Björnsson 1997; McCormick et al. 2000; Taylor et al. 2005). Therefore, since GH and IGF-I in particular, are known potent stimulators of muscle growth (McCormick, Kelley, Young, Nishioka & Bern, 1992), then the greater weight gain we observed following earlier application of photoperiod in October in conjunction with higher water temperatures may simply relate to greater muscle recruitment and growth as previously postulated by Johnston et al. (2003). This would certainly conform with the greater K factors achieved in spring. Unfortunately, no muscle fibre or GH/IGF analysis was performed in the current experiment and should certainly be included in future studies in this field to determine the physiological mechanisms that are contributing to growth. Similarly, in future a trial but under constant temperature conditions may also be able to differentiate the effects of temperature from photoperiod on seasonal patterns of growth.
In summary, these results provide useful information for the rainbow trout industry to capitalise on in order to enhance production efficiency, and indicate avenues by which knowledge of the physiological mechanisms underlying rainbow trout growth could be expanded.
We wish to thank NERC ROPA (GR3/R9827) and the British Trout Association for funding support. A special thanks goes to members of the Genetics & Reproduction Department for help with sampling in the field, and to Alastair McPhee and John Gardener for there assistance with the care and maintenance of experimental animals at the Niall Bromage Freshwater Research Facility.
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Figure 1. The timing of experimental LL regimes in relation to ambient water temperature (Grey line) and photoperiod.
Figure 2. (a) Weight gain (g) and (b) weight specific growth rate (% day-1) (c) condition factor (K) of rainbow trout exposed to LL from October, November, December or January relative to those maintained under SNP. Data are presented as tank mean ± SEM (n=3, 50 fish/tank). Superscripts denote significant differences between treatments (p<0.05). The grey line represents ambient water temperatures (ºC).