Influence of Temperature on Growth and Survival of Juvenile Winter Flounder, Pseudopleuronectes Americanus (Walbaum) Reared Under Continuous Light

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Influence of temperature on growth and survival of juvenile winter flounder, Pseudopleuronectes americanus (Walbaum) reared under continuous light

Casey, Paul; Zadmajid, Vahid; Butts, Ian A. E.; Sørensen, Sune Riis; Litvak, Matthew K.

Published in: Journal of the World Aquaculture Society

Link to article, DOI: 10.1111/jwas.12759

Publication date: 2021

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Citation (APA): Casey, P., Zadmajid, V., Butts, I. A. E., Sørensen, S. R., & Litvak, M. K. (2021). Influence of temperature on growth and survival of juvenile winter flounder, Pseudopleuronectes americanus (Walbaum) reared under continuous light. Journal of the World Aquaculture Society, 52(1), 204-215. https://doi.org/10.1111/jwas.12759

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Received: 8 December 2019 Revised: 3 October 2020 Accepted: 19 November 2020

DOI: 10.1111/jwas.12759

FUNDAMENTAL STUDIES

Influence of temperature on growth and survival of juvenile winter flounder, Pseudopleuronectes americanus (Walbaum) reared under continuous light

Paul Casey1 | Vahid Zadmajid2 | Ian A. E. Butts3 | Sune Riis Sørensen4,5 | Matthew K. Litvak6

1Department of Biology and Centre for Coastal Studies and Aquaculture, University Abstract of New Brunswick, Saint John, New Winter flounder, Pseudopleuronectes americanus, has Brunswick, Canada emerged as a promising candidate flatfish for cold-water 2 Department of Fisheries Science, Faculty of aquaculture and restocking. Here, juveniles were reared for Natural Resources, University of Kurdistan, Sanandaj, Iran 8 weeks at three temperatures: 10, 15, and 20 C under

3School of Fisheries, Aquaculture and Aquatic 24-hr light. All fish were imaged at stocking and at 2-week Sciences, Auburn University, Auburn, Alabama intervals, where growth was measured as changes in stan- 4National Institute of Aquatic Resources, dard length (SL) and body area (BA). By week 2, fish reared Technical University of Denmark, Lyngby, Denmark at 15 and 20 C were larger than those grown at 10 C. At 5Billund Aquaculture, Billund, Denmark weeks 4 to 6, fish at 15 C were larger than fish at 20 C. Lin-

6Department of Biology, Mount Allison ear regressions were used to model growth dynamics over University, Sackville, New Brunswick, Canada time at each temperature. Highly significant linear growth

Correspondence trajectories were detected over time for SL and BA. SL and

Matthew K. Litvak, Mount Allison University, BA regressions also showed a significant difference among 62 York Street, Sackville, New Brunswick, E4L the slopes across temperatures, where comparing slopes 1E2, Canada. Email: [email protected] showed the best temperature to rear the flounder was 15C. Weights of fish held at 15C and 20C were greater than at 10C at the termination of the experiment. Within each temperature, the growth rate of malpigmented fish was not different from that of the normally pigmented fish. Overall, growth of winter flounder was comparable to that of other commercially produced flatfish species, providing

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Journal of the World Aquaculture Society published by Wiley Periodicals LLC on behalf of World Aquaculture Society.

204 wileyonlinelibrary.com/journal/jwas J World Aquac Soc. 2021;52:204–215. CASEY ET AL. 205

strong evidence for this flatfish species as a potential species for aquaculture.

KEYWORDS aquaculture, flatfish, growth dynamic, hatchery management, metamorphosis

1 | INTRODUCTION

Aquaculture is the fastest growing food-producing sector in the world, with an estimated annual growth rate of 5.8% during the years of 2000 to 2016 (FAO, 2018). However, in order to meet the demand for food from a growing world population, aquatic plant and animal production need to be accelerated to fill the gap between supply and demand (Ahmed & Thompson, 2019). Winter flounder, Pseudopleuronectes americanus has emerged as a promising candidate flatfish for cold-water aquaculture in Canada and the United States (Fairchild, 2010; Litvak, 1999). The species has displayed a range of attractive characteristics for aquaculture, including being euryhaline (McCraken, 1963), eurythermal (Pearcy, 1961), and freeze-resistant as it is capable of surviving in waters below −1.0C (Duman & DeVries, 1974; Fletcher, 1977). The development of culture techniques suitable for this species has been ongoing for many years (Fairchild, 2010; Litvak, 1999). Larval rearing protocols have already been success- fully developed (Ben Khemis, Audet, Fournier, & De La Noüe, 2003; Ben Khemis, De La Noue, & Audet, 2000; Litvak, 1999; Litvak, Zadmajid, & Butts, 2020; Martinez-Silva, Audet, Winkler, & Tremblay, 2018) and metamorphosed fish can be weaned onto formulated diets (Bélanger et al., 2018; Butts, Ben Khemis, & Litvak, 2015; Fairchild, Rennels, Howell, & Wells, 2007; Lee & Litvak, 1996a, 1996b). However, postmetamorphic mortality rate of winter flounder reared in the hatchery is still high and pigmentation of juveniles can be poorly developed. The success of commercial culture for winter flounder principally requires improving postmetamorphic survival and obtaining a growth rate comparable to that of other commercially important flatfish species. In teleosts, growth varies seasonally, annually, and spatially across species, as a result of differences in their genetic makeup that influences innate capacity for growth under different sets of ecological and environmental conditions (Dutil, Jabouin, Larocque, Desrosiers, & Blier, 2008). Temperature is considered to be the “master ecological factor” in fish (Brett, 1971), as it exerts strong control over processes associated with growth, metabolism, physiological traits, development, and survival (Arnason, Gunnarsson, Steinarsson, Daníelsdóttir, & Björnsson, 2019; Bjornsson, Steinarsson, & Arnason, 2007; Boltaña et al., 2017; De, Ghaffar, Bakar, & Das, 2016; Koenker, Laurel, Copeman, & Ciannelli, 2018; Laurel, Copeman, Spencer, & Iseri, 2018). Although eurythermal fish can live in a broad range of temperatures, they exhibit a range of thermally dependent growth responses as well as lower and upper pejus temperatures. Temperature-dependent growth has been reported for various ecologically and wild-caught fish species, as well as aquaculture species where husbandry protocols are designed in order to maximize growth and performance (Barron et al., 2012; Bjornsson et al., 2007; Cavrois-Rogacki, Davie, Monroig, & Migaud, 2019; Islam, Uddin, Uddin, & Shahjahan, 2019; Koenker et al., 2018; Laurel et al., 2018; Nytrø et al., 2014; Tomiyama et al., 2018). For the majority of species, growth is enhanced as temperature increases, peaking at the optimal temperature for growth (Brett, 1979). Increased growth rates are principally due to greater efficiency, food ingestion, digestion, and nutrient utilization (Bogevik et al., 2010). Ectotherm metabolic theory predicts that temperatures close to critical maxima or minima will adversely impact physiological and behavioral performance (Hofmann & Todgham, 2010; Lyon, Ryan, & Scroggie, 2008). For example, many temperate species may endure very low temperatures for extended periods in a state of low metabolic rate and growth. In contrast, increased temperatures above optima may suddenly reach the upper thermal tolerance range of species and cause metabolic dysfunctions, nitrogenous waste accumulation, heat loss, and low feeding activity as well as higher caloric (energy) needs that reduce 206 CASEY ET AL.

potential growth rates (Bermudes, Glencross, Austen, & Hawkins, 2010; Fu, Fu, Qin, Bai, & Fu, 2018; Kullgren et al., 2013; MacCarthy, Moksness, & Pavlov, 1998; Sun & Chen, 2009). Therefore, under culture conditions, deter- mination of optimal environmental conditions is essential to achieve the greatest growth and performance. Accordingly, optimum temperatures for growth may differ with age and size, such that juveniles of many teleosts prefer warmer temperatures than their older conspecifics (McCauley & Huggins, 1979; Pedersen & Jobling, 1989; Tomiyama et al., 2018). This hypothesis is reinforced by spatial and temporal distributions in nature, where younger fishes are often inhabited in shallower, warmer waters in comparison to adults (McCauley & Huggins, 1979). In addition, shallow estuaries, the nursery grounds for juvenile flatfish, provide good environmental conditions in regard to salinity, prey availability, and optimum temperatures (Able, Neuman, & Wennhage, 2005; Tomiyama et al., 2018). Like other cultured flatfish (Audet & Tremblay, 2011; Fukusho et al., 1987; Heap & Thorpe, 1987; Purchase & Brown, 1997), winter flounder are often malpigmented. The extent of skin malpigmentation varies from small areas without pigmentation to complete lack of pigmentation. This condition is thought to arise from nutritional deficien- cies at the larval stage (Fraboulet, Lambert, Tremblay, & Audet, 2010; Fukusho et al., 1987). However, it is not known if malpigmented and normally pigmented winter flounder grow at similar rates. If malpigmented fish grow slower, it may be beneficial for an aquaculturist to eliminate them early, rather than invest in a fish with a slower growth rate. Therefore, the objectives of this study were to (a) examine the role of temperature on growth and survival of young-of-the-year winter flounder and (b) determine if there is a difference in growth rate between malpigmented and normally pigmented fish. Information about growth dynamics will help in building a bioeconomic model on the feasibility of growing this flatfish species for aquaculture and stock enhancement.

2 | MATERIALS AND METHODS

2.1 | Fish husbandry and water quality

Broodstock and larval rearing protocols followed those developed in our lab (Butts et al., 2015; Butts & Litvak, 2007a, 2007b; Litvak, 1999; Litvak et al., 2020). We generated juveniles for this experiment by rearing larvae under 24 hr light (Litvak et al., 2020). Young-of-the-year winter flounder juveniles were reared in the laboratory and exposed to three temperatures (±0.5C): 10, 15, and 20C. A total of 270 fish (mean ± 1 SEM; standard length 2 (SL) = 47.05 ± 0.2 mm; body area (BA) = 652.03 ± 5.97 mm ) were stocked into 18 cages, 15 fish per cage, and 6 cages per treatment. Included in the 270 fish were 17 malpigmented fish. One malpigmented fish was placed in each cage, except for one of the cages in the 20C treatment due to a shortage of malpigmented fish. Sea water for initial startup of recirculation aquaculture system (RAS) systems was pumped from Lorneville, NB, Breakwater wharf and trucked to our lab and held in a 5,400 L holding tank. The tanks for rearing were supplied with water from the 5,400 L holding tank. Each temperature treatment had a separate RAS (Figure 1). Here, each system consisted of a 46 cm diameter × 86.5 cm high cylindrical clear fiberglass header tank, a 104 cm × 104 cm × 25 cm deep square fiberglass gray holding tank, and a 31 cm × 71 cm high conical clear fiberglass biofilter tank. Total water volume in each system was 550 L. For each RAS system, water flowed by gravity from the header tank to the holding tank and then into the square net cages. Keeping the header tank at a set level allowed us to maintain consistent water flow to the cages. Water exited from the fish-holding tanks through a central drain via an external standpipe system and flowed by gravity into the biofilter tanks. Biofilters were downwelling-submerged filters and filled with biobarrel biofilter media. Water exited at the bottom of the biofilters and was then pumped through a pair of parallel cartridge filters (5 μm, Omni) and treated with ultraviolet light (UV16, Aquatic Eco-Systems Inc) before re-entering the header tank. Temperature was controlled in the header tanks. The 20C system was heated using a submerged 1,000-watt heater (QP 10, Aquatic Eco-Systems Inc). The 10 and 15C systems were chilled by pumping cooled CASEY ET AL. 207

FIGURE 1 (a) Schematic illustrating three replicate recirculation aquaculture systems (RASs) used to examine the impact of temperature on growth and survival of winter flounder, Pseudopleuronectes americanus. Each replicate RAS system held 550 L of water. A header tank (clear fiberglass tank) enabled stable head pressure of temperature- controlled water to each temperature treatment. A titanium heater or chiller coil was used to control temperature to ±0.5C. Six net cages were suspended from PVC tubes supported by the experimental tank sides. A center- positioned standpipe collected the return water passing it by gravity into the biofilter (downwelling-submerged filters in fiber glass tanks). In a separate loop from the holding tank, water was passed through a vacuum column for degassing before entering the biofilter. From the lower part of the biofilter, water was pumped into two parallel cartridge filters (5 μm) and after this into a UV lamp (16 W) and back to the top of the header tank. Red tube lines show gravity-aided flow and blue tube lines show pump-based flow. (b) Top view of individual parts of the rearing tanks showing tank dimensions and the six net cages suspended in each of the three replicate holding tanks. PVC tubes held the net cages. Inflow of water into the cages was at 0.9 L/min, while outflow exited through a standpipe. On top of each net cage was a shaker feeder that provided food. Each cage held 15 normally pigmented flounder and one malpigmented fish 208 CASEY ET AL.

water at different rates through submerged titanium coils. Degassing was provided by vacuum columns placed above the biofilter tanks on separate loops and small degassing columns on the inflow into the header tanks. Cages were 25 cm square × 21 cm high and made of 0.64 cm black plastic mesh sides with a black chloroplast bottom (Cadillac plastic, NS). The cages were suspended in the tanks from 1.9 cm diameter PVC schedule 80 pipe. Water flow was directed into each cage at a rate of 0.90 L/min. Fish were fed to satiation at 6-hour intervals for a total of four feedings per day. Feed (Nutra #2 starter diet, Moore Clark, NB, particle size range from 1.1 to 1.9 mm) was delivered using automatic shaker feeders (SF 6, Sweeney, Aquatic Eco-Systems Inc.). To concentrate the food into the small cages, 2 L cylindroconical bottles with their bottoms cut off were inverted and attached to the bottom of the feeder to direct the feed into each cage. The average amount of feed per cage per feeding was 1.0 ± 0.06 g. The amount of feed offered to each fish per day was on average 3.3% of their body weight, which was set to be in excess of their demand. The system and tanks and cages were cleaned of leftover food and feces daily by siphoning. Water loss due to cleaning and evaporation was replaced with sea water. Approximately 20% of the water in each system was replaced daily. Feeders were cleaned and refilled with fresh feed once a week. The fish were exposed to a 24-hr photoperiod at light levels of 120 lx.

2.2 | Data collection

Every 2 weeks, all fish were placed on a tray and imaged for SL and BA (Optimas 4.1, BioScan Inc., Edmunds, WA).

The experimental fish were blotted dry and body weight (Wt) was recorded at the termination of the experiment to minimize handling stress possibly incurred by multiple weighings.

2.3 | Statistical analysis

All data were analyzed using the SAS statistical analysis software (v.9.1; SAS Institute Inc., Cary, NC). Levels for sig- nificance were set a priori at α = 0.05. Residuals were evaluated for normality (Shapiro–Wilk test) and homogeneity of variance (plot of residuals vs. predicted values). Data were log10 transformed to remove heterogeneity of variance. Logarithmic transformation removed heterogeneity of variance, but some data remained non-normal. However, analysis of variance is robust for small departures from normality (Zar, 2010). Cage means of the size and growth param- eters [SL, BA, Wt] were used for statistical comparisons.

A two-factor repeated measures analysis of variance with log10 transformed variables, SL and BA, was used to examine the effect of temperature and time. When an interaction (p < .05; Winer, 1971) between time and temperature was detected, separate one factor ANOVA models were performed at each sampling time to evaluate the effect of temperature alone. Multiple comparisons among treatment means in all analyses were compared using Tukey's

HSD (honestly significant difference) test. Next, linear regression was used to model SL and BA growth dynamics over time at each temperature. Thereafter, we used the regression components to calculate homogeneity of slopes following Zar (2010). t-Tests were then run between the slopes using a sequential Bonferroni adjustment to account for experiment-wise error rate.

Final Wt and condition factor (K) were analyzed with respect to temperature using one factor ANOVA models. Condition factor was calculated using the formula: K = W/L3 × 100 (Arndt, Benfey, & Cunjak, 1996; Novotny &

Beeman, 1990). SL and BA of malpigmented fish were compared to those of normally pigmented fish within each temperature using t-tests. Data for normally pigmented fish were averaged to represent a mean per cage. These means were compared to the data for the malpigmented fish in the cages. CASEY ET AL. 209

3 | RESULTS

Due to strong interactions between time and temperature for SL (p < .0001) and BA (p < .0001), the models were sep- arated and temperature groups were examined at each sampling time. At the onset of the experiment, there were no significant differences in SL (p = .518) or BA (p = .690) between any of the temperature treatments (Figure 2). By the second week, a posteriori tests revealed that the fish reared at 15C and 20C were already significantly larger than the fish grown at 10C (Figure 2; p ≤ .002). At week 4 and week 6 the fish at 15C were significantly larger than the fish held at 20C, while responses for 15C and 20C were not significantly different at week 8 (Figure 2). Linear regressions were used to model growth dynamics over time at each temperature. Here, highly significant 2 (r ≥ 0.96, p < .0001) linear growth trajectories were detected over time for SL and BA (Table 1). SL and BA regressions also showed a significant difference among the slopes across temperatures (p < .0001; Table 1, Figure 3).

(a) (b) 80 2000 10 10 15 b 15 b 1800 b 20 20 b b a 1600 b 70 c a c 1400 b a a c b 1200 c 60 a a 1000 b b b b a a 800 a a a 50 Body area (mm2) a a a 600 Standard length (mm) 400

40 200 12468 12468 Week Week

FIGURE 2 Standard length (mm, a) and body area (mm2, b) versus sampling time (weeks) for 270 juvenile winter flounder, Pseudopleuronectes americanus (n = 270) held in 18 cages at three temperatures (10, 15, and 20C). Different letters within sampling times denote significant differences. A posteriori multiple comparison between means within each sampling date was done with the Tukey's HSD (honestly significant difference) test. Different lower-case letters represent a significant statistical difference (p < 0.05). Error bars represent ±1 SEM

TABLE 1 Linear relationships between standard length (mm) and body area (mm2) over time at each temperature

Trait Temperature Slope (+SEM) Intercept (+SEM) R2 p-value Standard length 10C 0.39 (0.009)a 47.1 (0.31) 0.99 <.0001 15C 0.51 (0.011)c 47.8 (0.39) 0.99 <.0001 20C 0.47 (0.019)b 47.4 (0.64) 0.96 <.0001 Body area 10C 14.0 (0.41)a 624 (14.0) 0.98 <.0001 15C 19.5 (0.52)c 637 (18.2) 0.98 <.0001 20C 17.3 (0.87)b 645 (29.9) 0.96 <.0001

Note: Regression components were used to calculate homogeneity of slopes following Zar (2010). t-tests were then run between the slopes using a sequential Bonferroni adjustment to account for experiment-wise error rate. Different lower- case letters represent a significant statistical difference (p = .05). 210 CASEY ET AL.

FIGURE 3 Linear regressions were used to model body area (a) and standard length (b) for juvenile winter flounder, Pseudopleuronectes americanus (n = 270) at 10, 15, and 20C

Experiment-wise sequential Bonferroni corrected t-tests comparisons between the slopes showed the best temperature to rear winter flounder was 15 C for both SL and BA (Table 1, Figure 3).

Wt and condition factor were obtained on the last sampling day. There were significant differences among final

Wt of the fish held at the three temperatures (p = .002; Figure 4). Here, the average Wt of the fish held at 15 and 20 C was significantly greater than at 10 C, while Wt of the fish reared at 15 and 20 C were not significantly different. There were no significant differences in condition factor (p = .357) among any of the treatments (ranged from 2.02 at 10C to 2.09 at 15C).

t-Tests revealed no significant differences for SL and BA within any of the temperatures (all probabilities >.05) between malpigmented and normally pigmented fish. Only one fish died during the course of the experiment. This was in the 15C treatment and was most likely due to handling stress. The temperatures used for this experiment were not observed to affect survival.

4 | DISCUSSION

The aquaculture industry aims to produce target species under controlled conditions as cost-effectively as possible. Growth rate is one of the most important factors influencing economic success in commercial fish farming, and it is CASEY ET AL. 211

FIGURE 4 The effect of temperature on final weight of juvenile winter flounder, Pseudopleuronectes americanus (n = 270). Different lower-case letters represent a significant statistical difference (p < 0.05). Error bars represent ±1 SEM

well known that various environmental variables can impact it (Houde, 2019; Yúfera, 2018). For the present study, we hypothesized that temperature of culture water would influence survival and increase growth rates of winter flounder. Water temperature has also been modified to maximize juvenile growth for other flatfish, such as Atlantic halibut, Hippoglossus hippoglossus (Björnsson & Tryggvadóttir, 1996; Hallaråker, Folkvord, & Stefansson, 1995; Jonassen, Imsland, & Stefansson, 1999; Larsen, Imsland, Lohne, Pittman, & Foss, 2011), turbot, Scophthalmus maximus (Arnason, Björnsson, Steinarsson, & Oddgeirsson, 2009; Imsland, Folkvord, & Stefansson, 1995; Van Ham et al., 2003), summer flounder, Paralichthys dentatus (Gaylord, Schwarz, Cool, Jah-ncke, & Craig, 2004), tongue sole, Cynoglossus semilaevis (Fang, Tian, & Dong, 2010), Dover sole, Solea solea (Schram et al., 2013), and marbled flounder, Pseudopleuronectes yokohamae (Kusakabe, Hata, Shoji, Hori, & Tomiyama, 2017; Tomiyama et al., 2018). However, temperature-dependent growth rates vary between species, and these growth differences further change through ontogeny. For example, in Atlantic halibut, the optimum water temperature for growth decreases with increasing fish size (Brown, 2010). The preferred culture temperature for juvenile southern flounder, Paralichthys lethostigma falls within the range of 23 to 25C (Daniels, Watanabe, Murashige, Losordo, & Dumas, 2010). In Japanese flounder, Par- alicthys olivaceus, growth and feed efficiency increased with increasing temperature from 13 to 21C and decreased at 24C (Morizane, 1984).

SL and BA regressions showed a significant difference among the slopes at three temperatures, where comparing slopes showed the best temperature to rear winter flounder was 15C. In cooler water (10C), the growth rate was markedly depressed. These findings support other observations, which have found juvenile winter flounder grow faster at higher temperatures. For example, Hoornbeek, Sawyer, and Sawyer (1982) examined the effect of water temperature on growth in winter flounder juveniles collected from the wild, and in this study they found that fish in heated water (15C) grew faster than fish grown in unheated water (1C). In another study, Meise, Johnson, Stehlik, Manderson, and Shaheen (2003) collected winter flounder juveniles from Navesink River (New Jersey) with average daily temperatures ranging from 10 to 21C. They found that the highest growth rate occurred at temperatures around 18C, while the colder waters and poorer diets experienced by juveniles corresponded to slower somatic growth rates. In addition, mean growth coefficients for winter flounder (size: 0.32–2.34 g) were similar at temperatures of 11.9 and 16.9C, but showed an increase at 21.3C (Mercaldo-Allen, Kuropat, & Caldarone, 2008). Low temperatures probably depressed appetite and feeding behavior in winter flounder juveniles (Fraboulet, 212 CASEY ET AL.

Lambert, Tremblay, & Audet, 2011), thereby resulting in lower somatic growth and/or protein synthesis for growth as reported for non-flatfishes like Atlantic wolfish, Anarhichas lupus (McCarthy, Moksness, Pavlov, & Houlihan, 1999). In other juvenile flatfish, lower temperatures also proved to decrease feeding activity (7–16C: Hallaråker et al., 1995; 10 vs. 16C: Imsland et al., 1995). Condition factor is often used as an indicator of fish health (Berge & Storebakken, 1996). In this experiment, juveniles in all treatments were in good condition at the end of the experiment since there were no significant differences in the condition factor between any of the treatments. The fish in the different temperatures were therefore equally healthy but growing at different rates. The lack of any differences in responses between malpigmented and normally pigmented juveniles is supported by other studies conducted with flatfish (Heap & Thorpe, 1987; Purchase & Brown, 1997). Therefore, no reason exists for an aquaculturist to cull malpigmented fish based only on their growth. There may however be other reasons to cull malpigmented fish such as: poor marketability (Heap & Thorpe, 1987; Stickney & White, 1975) and/or increased likelihood of getting sunburnt in cage culture (Raymond D., St. Andrews, N.B., personal communication). In conclusion, this study contributes to a growing database on winter flounder culture and will help bring this species closer to commercialization. Aquaculture is capital intensive where culture of a fast growing species is more profitable. The time that a fish requires to reach market size is dependent on growth rate, and the economic viability of a commercial operation is largely dependent on that rate. Heating water requires energy and the return from accelerated growth must appropriately exceed the cost of energy to heat the water. Although winter flounder is a slow-growing species reaching market size in 2–3 years (Fairchild, 2010), production time can be decreased by rearing the fish at warmer temperatures and under continues light (Casey, Butts, Zadmajid, Sørensen, & Litvak, 2020). This study shows that the optimum temperature range for growth of 0 group winter flounder lies between 15 and 20C. Every change in temperature will have an associated change in growth rate and an associated change in the cost to maintain that temperature. The temperature that maximizes growth while minimizing costs has yet to be determined. Future research will be required to find the bioeconomic optimum temperature profile for raising these fish from egg to market.

ACKNOWLEDGMENTS This research was funded by the New Brunswick and Nova Scotia Canada Cooperative Agreement on Aquaculture and NSERC research and equipment grants to M.K. Litvak. IAEB was supported by the USDA National Institute of Food and Agriculture (Hatch project 1013854).

CONFLICT OF INTEREST The authors declare no conflict of interest.

ORCID Vahid Zadmajid https://orcid.org/0000-0002-8034-9557

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How to cite this article: Casey P, Zadmajid V, Butts IAE, Sørensen SR, Litvak MK. Influence of temperature on growth and survival of juvenile winter flounder, Pseudopleuronectes americanus (Walbaum) reared under continuous light. J World Aquac Soc. 2021;52:204–215. https://doi.org/10.1111/jwas.12759