Reduced photoperiod - Wiley Online Library

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concentrations; 11-KT is the major androgen pro- ... ethyl ether (Fisher Scientific, Fair Lawn, NJ, USA) ... and grilse data were analysed using the software's.
Aquaculture Research, 2015, 1–5

doi:10.1111/are.12741

SHORT COMMUNICATION Reduced photoperiod (18 h light vs. 24 h light) during first-year rearing associated with increased early male maturation in Atlantic salmon Salmo salar cultured in a freshwater recirculation aquaculture system Christopher Good1, Gregory M. Weber2, Travis May1, John Davidson1 & Steven Summerfelt1 1

The Conservation Fund’s Freshwater Institute, Shepherdstown, WV, USA

2

National Center for Cool and Cold Water Aquaculture, USDA-ARS, Kearneysville, WV, USA

Correspondence: C Good, The Conservation Fund’s Freshwater Institute, 1098 Turner Road, Shepherdstown, WV 25443, USA. E-mail: [email protected]

The onset of sexual maturation in Atlantic salmon Salmo salar is a flexible process (Fjelldal, Hansen & Huang 2011), the timing of which can be influenced by numerous environmental factors including photoperiod (Taranger, Haux, Stefansson, Bj€ ornsson, Walther & Hansen 1998), water temperature (Vikingstad, Andersson, Norberg, Mayer, Klenke, Zohar, Stefansson & Taranger 2008), feed intake (Kadri 2003), nutrition (Alne, Skinlo Thomassen, Sigholt, Berge & Rørvik 2009), lipid reserves (Rowe & Thorpe 1990), growth rate (Duston & Saunders 1999) and stock genetics (Wolters 2010). Early maturing males are known to occur in wild populations (Skilbrei & Heino 2011), and in the salmon farming industry precocious males (‘jacks’ or ‘grilse’) are highly undesirable (Duston & Saunders 1999) due to relatively poor growth performance and feed conversion efficiency (McClure, Hammell, Moore, Dohoo & Burnley 2007), as well as reduced product quality (Aksnes, Gjerde & Roald 1986). Because grilsing can result in serious economic loss to Atlantic salmon farmers (Johnston, Li, Vieira, Nickell, Dingwall, Alderson, Campbell & Bickerdike 2006), strategies for reducing early maturation have been developed and include photoperiod control (Bromage, Porter & Randall 2001), selective breeding (Gjedrem 2000) and triploidy (Benfey 1999).

The concept of raising Atlantic salmon to market size in land-based, closed-containment water recirculation facilities, versus grow-out in coastal netpens, is gaining considerable attention from aquaculture researchers (Summerfelt & Christianson 2014). As raising salmon to market size in water recirculation aquaculture systems (RAS) is presently a frontier in aquaculture, there have been issues encountered in research grow-out trials, including a high prevalence of precociously maturing male salmon in the water recirculation environment (Good, Davidson, Earley, Lee & Summerfelt 2014). On-site research has demonstrated that, under a 24 h photoperiod, up to 80% of male salmon are sexually mature prior to harvest at 4 kg average final weight (Summerfelt, Waldrop, Good, Davidson, Backover, Vinci & Carr 2013). Published research (Fjelldal et al. 2011) combined with anecdotal evidence provided to us by industry personnel, however, suggested that rearing salmon at a reduced photoperiod (i.e. 18 h light/6 h dark) during their first-year post hatch, followed by a constant photoperiod until harvest, will decrease the level of precocity observed during grow-out. We therefore sought to investigate this novel photoperiod approach and its relationship to male salmon maturation in freshwater RAS, and our findings are presented in this short communication.

© 2015 The Authors. Aquaculture Research Published by John Wiley & Sons Ltd. 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.

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Photoperiod and early salmon maturation C Good et al.

We procured Atlantic salmon eyed eggs from a commercial supplier; broodstock were spawned in late November, 2011 and eggs were 100% hatched by late February, 2012. The salmon were raised from first feeding up to 12 months post hatch under either constant (i.e. 24 h) or reduced (18 h:6 h) photoperiod. The only break in this treatment regimen was to provide, beginning at approximately 40 g average weight, a 6-week S0 ‘winter’ (i.e. 12 h:12 h) photoperiod, as per industry recommendations, in order to induce smoltification in both groups, after which the two groups were returned to their original photoperiod treatment. From first feeding until the end of the S0 winter, all fish were held in circular 0.5 m3 tanks (six tanks receiving 24 h photoperiod and six tanks receiving 18 h:6 h photoperiod) in a flowthrough system, after which they were transferred to a partial water reuse system and reared in 10 m3 circular dual-drain tanks (one tank per treatment). Throughout the first 12 months of the study, the 24 h photoperiod was achieved by exposing fish to the facility’s constant lighting, while the 18 h:6 h photoperiod was achieved by covering the specific culture tanks with black, opaque plastic tarps and providing 18 h light per day underneath these covers, followed by 6 h of darkness. After the first year of rearing, all fish in the 24 h group were adipose fin-clipped for later identification, and then all fish from both groups were transferred to a semi-commercial scale RAS, containing a single 150 m3 dual-drain culture tank, and raised to 24 months post hatch, at which point they were depurated and harvested as food fish. The only fish removed from the semicommercial scale RAS prior to the final harvest were (1) occasional culls due to external Saprolegnia spp. infections and (2) all visibly mature males (grilse) at 19 months post hatch. During this latter grilse harvest, fin clips were noted to determine the photoperiod treatment regime for each fish removed. Aside from the photoperiod treatment, all other conditions remained the same between the two groups, including feed and feeding rates, water quality and stocking densities. Mean ( SD) water temperatures during each phase of rearing were (i) fry tanks: 13.7C  0.3°C; (ii) partial reuse system: 13.0  0.4°C and (iii) semi-commercial scale RAS: 15.2  0.7°C. Lighting in the fry tank system was provided by full-spectrum, incandescent bulbs, while lighting in the partial reuse and grow-out

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Aquaculture Research, 2015, 1–5

RAS was provided by full-spectrum metal halide bulbs. To assess maturation, samples of 30 males from each treatment group were collected at 12 months (just prior to fish transfer to the grow-out RAS), 16 months, and 19 months (just prior to the grilse harvest) post hatch in fish age, at which times data were collected for (i) gonadosomatic indices (GSI) and (ii) plasma 11-ketotestosterone (11-KT) concentrations; 11-KT is the major androgen produced by the testes in salmonids and is considered an indicator for sexual maturation (Taranger, Carillo, Schulz, Fontaine, Zanuy, Felip, Weltzien, Dufour, Karlsen, Norberg, Andersson & Hansen 2010). An additional final sample was collected at 24 months post hatch, prior to the final harvest, although due to the removal of grilse at 19 months post hatch the majority of fish in the population during the final sampling was female, and hence only 18 males per treatment group were able to be identified and sampled at that point. During each sampling event, fish were selected at random via dip-net collection, euthanised (200 mg L 1) with tricaine methanesulfonate (MS-222; Western Chemicals, Ferndale, WA, USA), and quickly dissected via ventral mid-sagittal incision for gonad examination and sex determination. For all identified males: (i) photoperiod treatment group was noted; (ii) whole blood was collected via caudal venipuncture using 1.5-inch 21.5-gauge needles on 3 mL syringes (blood was immediately transferred to heparinised 1.5 mL centrifuge tubes, and all tubes were kept on ice until centrifugation for 10 min at 8160 g, after which plasma was carefully pipetted from centrifuge tubes and transferred to sterile 2 mL cryovials for long-term storage at 80°C) and (iii) fish were weighed and then testes were removed and weighed separately in order to calculate gonadosomatic indices (GSI = gonad weight/whole fish weight*100). All males were dichotomously classified as either grilse or immature; for the purposes of this study, grilse were defined through a combination of qualitative assessment (darker skin colouration and developing kype) and GSI values greater than 1.000. Finally, plasma 11-KT concentrations were quantified using enzyme-immunoassay (EIA) kits (Cayman Chemicals, Ann Arbor, MI, USA) following EIA kit instructions. Plasma samples were extracted three times with ethyl ether (Fisher Scientific, Fair Lawn, NJ, USA) for 11-KT measurement (Schultz, Perez, Tan, Men-

© 2015 The Authors. Aquaculture Research Published by John Wiley & Sons Ltd., Aquaculture Research, 1–5

Photoperiod and early salmon maturation C Good et al.

Aquaculture Research, 2015, 1–5

dez, Capa, Snodgrass, Prince & Serafy 2005); the intra-assay variability for 11-KT was CV 9.5%, and the inter-assay variability was CV 15.7%. All statistical analyses were performed using STATA v.9 software (StataCorp LP, College Station, TX, USA); 11-KT and GSI data were ln-transformed for normalisation prior to conducting two-sample t-test, and grilse data were analysed using the software’s case-control odds ratio procedure, which in this case measured the strength of statistical association between treatment group (i.e. 18 h:6 h photoperiod vs. 24 h) and the observed outcome (i.e. grilse vs. immature) at each sampling event. Results were considered statistically significant if P < 0.05. The overall finding of this study is that the reduced first-year photoperiod did not impart the

Table 1 Second year (12–24 months post hatch) plasma concentrations (mean  SE) of 11-ketotestosterone (11-KT) in male Atlantic salmon following first-year rearing under either 18 h:6 h or 24 h photoperiod Fish age (mo. post hatch) 12 16 19 24

Treatment

11-KT (ng/mL)

P

18 24 18 24 18 24 18 24

0.578 0.620 3.649 2.345 12.12 8.876 9.180 3.305

0.069

h:6 h h:6 h h:6 h h:6 h

h h h h

       

0.066 0.108 0.974 1.125 2.369 2.324 2.033 1.291

0.061 0.010 0.003

expected reduction of male sexual precocity in the second year of grow-out; rather, the reduced photoperiod appeared to be associated with a significantly increased level of maturation via the majority of assessments carried out at 16-, 19and 24 months post hatch in fish age. Although mean plasma 11-KT was initially slightly higher at 12 months post hatch in the 24 h photoperiod group, all subsequent assessments indicated higher mean 11-KT concentrations in the 18 h:6 h group, with significantly higher levels at 19- and 24 months post hatch in this group (Table 1; Figure 1). Likewise, mean GSI values were significantly higher in the 18 h:6 h treatment group at 19- and 24 months post hatch (Table 2). Although grilse were observed in both treatment groups during the 16-, 19- and 24 month sampling events, the odds of grilse being from the 18 h:6 h treatment group were significantly higher at 16- and 24 months post hatch. Males sampled at the 19-month event, just prior to the overall population grilse harvest, were 50.0% grilse in the 18 h:6 h group and 33.3% grilse in the 24 h group. Although this difference among sampled fish was not statistically significant, full population data collected subsequently can be compared; these grilse harvest data indicated that among all grilse removed (17.0% of the total salmon population; 34.0% of the entire male population), 60.2% were from the 18 h:6 h treatment group and 39.8% were from the 24 h group. Grilse harvest population data also indicated that, at 19 months post hatch, 40.9% of all males

Figure 1 A comparison of plasma 11-ketotestosterone (11-KT) concentration values (ng/mL) for all male Atlantic salmon sampled at 12-, 16-, 19- and 24 months post hatch. Bars represent 11-KT values for individual fish, with the empirical data ranked from low to high for each treatment group at each sampling point.

© 2015 The Authors. Aquaculture Research Published by John Wiley & Sons Ltd., Aquaculture Research, 1–5

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Photoperiod and early salmon maturation C Good et al.

Aquaculture Research, 2015, 1–5

Table 2 Second year (12–24 months post hatch) gonadosomatic indices (GSI; mean  SE) in male Atlantic salmon following first-year rearing under either 18 h:6 h or 24 h photoperiod. Grilse determination was made through a combination of qualitative assessment (colouration, kype development) and GSI ≥1.000

Age

Treatment

GSI

12 months

18 24 18 24 18 24 18 24

0.038 0.029 1.359 0.632 3.806 2.296 3.510 0.573

16 months 19 months 24 months

h:6 h h:6 h h:6 h h:6 h

h h h h

P        

0.004 0.003 0.429 0.355 0.727 0.618 0.787 0.329

(20.4% of the total population) in 18 h:6 h group were sexually mature, while 27.0% of all males (13.5% of the total population) in the 24 h group were mature. Our results demonstrate that, under the conditions of this study, reducing photoperiod during the first year was associated with increased male maturation during the second year of grow-out. Anecdotal reports from industry stakeholders currently raising Atlantic salmon to market size in land-based closed-containment RAS indicate that, despite attempts to reduce precocious male maturation using various other photoperiod manipulation regimes, there is often a problem of preharvest male grilsing under closed-containment conditions. There remains, therefore, a clear need for further research to identify strategies for reducing or eliminating the problem of precocious maturation in RAS (e.g. the development of an allfemale germplasm), as this phenomenon is currently impacting the closed-containment salmon producers’ ability to maintain economic viability.

Acknowledgments We are grateful to the Gordon and Betty Moore Foundation and the Atlantic Salmon Federation for providing funding for the overall salmon growout trial, as well as the USDA Agricultural Research Service (ARS) that supported this independent study under Agreement No. 59-1930-5510. Appreciation is also extended to Ms Jill Birkett of the USDA-ARS-NCCCWA for conducting the EIA laboratory analyses. The authors do not have any conflicts of interest to declare. Experimental protocols described are in compliance with the

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0.165 0.175 0.040 0.002

Grilse (%) 0.0 0.0 26.7 6.7 50.0 33.3 61.1 11.1

Odds ratio (grilse)

P





5.091

0.038

2.143

0.153

12.57

0.002

Animal Welfare Act (9CFR), and were approved by our Institutional Animal Care and Use Committee (IACUC). Use of trade names does not imply endorsement by the US Government. References Aksnes A., Gjerde B. & Roald S.O. (1986) Biological, chemical and organoleptic changes during maturation of farmed Atlantic salmon, Salmo salar. Aquaculture 53, 7–20. Alne H., Skinlo Thomassen M., Sigholt T., Berge R.K. & Rørvik K.A. (2009) Reduced sexual maturation in male post-smolt 1 + Atlantic salmon (Salmo salar L.) by dietary tetradecylthioacetic acid. Aquaculture Research 40, 533–541. Benfey T.J. (1999) The physiology and behaviour of triploid fishes. Reviews in Fisheries Science 7, 39–67. Bromage N., Porter M. & Randall C. (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197, 63–98. Duston J. & Saunders R.L. (1999) Effect of winter food deprivation on growth and sexual maturity of Atlantic salmon (Salmo salar) in sea water. Canadian Journal of Fisheries and Aquatic Science 56, 201–207. Fjelldal P.G., Hansen T. & Huang T.-S. (2011) Continuous light and elevated temperature can trigger maturation both during and immediately after smoltification in male Atlantic salmon (Salmo salar). Aquaculture 321, 93–100. Gjedrem T. (2000) Genetic improvement of cold-water fish species. Aquaculture Research 31, 25–33. Good C., Davidson J., Earley R.L., Lee E. & Summerfelt S. (2014) The impact of water exchange rate and biofiltration on water-borne hormones in recirculation aquaculture systems containing sexually maturing Atlantic salmon Salmo salar. Aquaculture Research and Development 5, 7.

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Aquaculture Research, 2015, 1–5

Johnston I.A., Li X., Vieira V.L.A., Nickell D., Dingwall A., Alderson R., Campbell P. & Bickerdike R. (2006) Muscle and flesh quality traits in wild and farmed Atlantic salmon. Aquaculture 256, 323–336. Kadri S. (2003) Grilse reduction and beyond: growth benefits of photoperiod manipulation in cages. Proceedings of the 2nd St. Andrews Biological Station Aquaculture Workshop: Early Maturation of Atlantic salmon: St. Andrews, NB, 6 March 2003. Bulletin of the Aquaculture Association of Canada 103, 5–9. McClure C.A., Hammell K.L., Moore M., Dohoo I.R. & Burnley H. (2007) Risk factors for early sexual maturation in Atlantic salmon in seawater farms in New Brunswick and Nova Scotia, Canada. Aquaculture 272, 370–379. Rowe D.K. & Thorpe J.E. (1990) Suppression of maturation in male Atlantic salmon (Salmo salar L.) parr by reduction in feeding and growth during spring months. Aquaculture 86, 291–313. Schultz D.R., Perez N., Tan C.-K., Mendez A.J., Capa T.R., Snodgrass D., Prince E.D. & Serafy J.E. (2005) Concurrent levels of 11-ketotestosterone in fish surface mucus, muscle tissue and blood. Journal of Applied Ichthyology 21, 394–398. Skilbrei O.T. & Heino M. (2011) Reduced daylength stimulates size-dependent precocious maturity in 0 + male Atlantic salmon parr. Aquaculture 311, 168– 174. Summerfelt S. & Christianson L. (2014) Fish farming in land-based closed containment systems. World Aquaculture Magazine March 2014, 18–21.

Photoperiod and early salmon maturation C Good et al.

Summerfelt S., Waldrop T., Good C., Davidson J., Backover P., Vinci B. & Carr J. (2013) Freshwater Growout Trial of St. John River Strain Atlantic Salmon in a Commercial-Scale, Land-Based, Closed-Containment System. Report to the Atlantic Salmon Federation, Chamcook, New Brunswick, Canada 52pp. Taranger G.L., Haux C., Stefansson S.O., Bj€ ornsson B.T., Walther B.T. & Hansen T. (1998) Abrupt changes in photoperiod affect age at maturity, timing of ovulation and plasma testosterone and oestradiol-17b profiles in Atlantic salmon, Salmo salar. Aquaculture 162, 85–98. Taranger G.L., Carillo M., Schulz R.W., Fontaine P., Zanuy S., Felip A., Weltzien F.-A., Dufour S., Karlsen O., Norberg B., Andersson E. & Hansen T. (2010) Control of puberty in farmed fish. General and Comparative Endocrinology 165, 483–515. Vikingstad E., Andersson E., Norberg B., Mayer I., Klenke U., Zohar Y., Stefansson S.O. & Taranger G.L. (2008) The combined effects of temperature and GnRHa treatment on the final stages of sexual maturation in Atlantic salmon (Salmo salar L.) females. Fish Physiology and Biochemistry 34, 289–298. Wolters W.R. (2010) Sources of phenotypic and genetic variation for seawater growth in five North American Atlantic salmon stocks. Journal of the World Aquaculture Society 41, 421–429.

Keywords: Atlantic salmon, early male maturation, water recirculation aquaculture, 11-ketotestosterone

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