Abstract
This study provides new and practical information to implement the use of photoperiodic manipulation for the control of the sexual maturation of Canadian 6+ Atlantic wolffish (Anarhichas lupus) and 3+ first-time spawners spotted wolffish (Anarhichas minor) from Canadian and Norwegian populations. Wolffish reproductive cycle (gametogenesis and oocyte maturation and spermiation) was monitored for 23 consecutive months. Control groups were held under a 12-month simulated natural photoperiod and treatment groups under an 8-month compressed photoperiod. Plasma sex steroid concentrations (estradiol-17β and 11-ketotestosterone), oocyte diameter growth, and milt production were assessed monthly. For all groups under study, fish subjected to the compressed photoperiod spawned 2–6 months earlier than the controls. Complete out-of-shift cycle was not achieved based on the completion of two reproduction cycles, and this is briefly discussed. Photoperiod treatment induced temporal shifts in sex steroid profiles, which are the likely mediators of altered timing of ovulation/final maturation. Photoperiod has a strong influence on the timing of wolffish maturation and could be used as an efficient and inexpensive tool to secure wolffish reproduction operations (year-round supply of egg and milt and/or timing with optimal temperature regimes).
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Notes
According to data from Department of Fisheries and Oceans, Maurice Lamontagne Institute, Mont-Joli, QC, Canada located on the south coast of the Saint-Lawrence Estuary 48° 35′ 0″ N/68° 11′ 0″ W.
According to data from Mérinov Inc., Grande-Rivière, QC, Canada located on the North coast of Baie-des-Chaleurs 48° 23′ 0″ N/64° 30′ 0″ W.
Now Mérinov Inc. (https://www.merinov.ca/fr/).
Ambient natural seawater was cooled during the summer and heated in the winter to maintain 8 °C.
References
AquaAgri Nomaculture (2015) Development of novel, high quality marine aquaculture in Sweden—with focus on environmental and economic sustainability. Annual report, Second reporting period, 2015. http://www.aquaagri.se/images/Artikel/annual_report_nomaculture_for_2015_uppdaterad.pdf. Cited 10 Nov 2017
Blythe WG, Helfrich LA, Sullivan CV (1994) Sex steroid hormone and vitellogenin levels in striped bass (Morone saxatilis) maturing under 6-, 9-, and 12-month photothermal cycles. Gen Comp Endocrinol 94:122–134
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
Chabot D, Savoie A, Dufresne F, Le François NR (2012) Détermination du taux de croissance du loup tacheté (Anarhichas minor) de souche québécoise. Rapport technique canadien des sciences halieutique et aquatiques 3016, 68 pp. http://www.dfo-mpo.gc.ca/Library/348154.pdf. Cited 7 Sept 2017
Davie A, Porter MJ, Bromage N, Migaud H (2007) The role of seasonally altering photoperiod in regulating physiology in Atlantic cod (Gadus morhua). Part I. Sexual maturation. Can J Fish Aquat Sci 64:84–97
Davies B, Bromage N (2002) The effects of fluctuating seasonal and constant water temperatures on the photoperiodic advancement of reproduction in female rainbow trout, Oncorhynchus mykiss. Aquaculture 205:183–200
Falk-Petersen I-B, Hansen TK, Fieler R, Sunde LM (1999) Cultivation of the spotted wolffish Anarhichas minor (Olafsen)—a new candidate for cold-water fish farming. Aquac Res 30:711–718
Findlay JWA, Smith WC, Lee JW, Nordblom GD, Das I, DeSilva BS, Khan MN, Bowsher RR (2000) Validation of immunoassays for bioanalysis: a pharmaceutical industry perspective. J Pharmaceut Biomed 21:1249–1273
Foss A, Imsland AK, Falk-Petersen I-B, Oiestad V (2004) A review of the culture potential of spotted wolffish Anarhichas minor Olafsen. Rev Fish Biol Fish 2:277–294
Fostier A, Jalabert B (2004) Domestication et reproduction chez les poissons. INRA Productions Animales 12:199–204
Gaudreau CM, Le François NR, Ditlecadet D, Tveiten H, Blier PU (2009) Characterization of the early-stages of the wolffish hybrid, Anarhichas minor × Anarhichas lupus: conservation and aquaculture applications. Aquat Living Resour 22:371–377
Gharib SD, Wierman ME, Shupnik MA, Chin WW (1990) Molecular biology of the pituitary gonadotropins. Endocr Rev 11:177–199
Gillooly JF, Charnov EL, West GB, Savage WM, Brown JH (2002) Effects of size and temperature on developmental time. Nature 417:70–73
Gunnarsson A (2017) Spatio-temporal variability in fecundity and atresia of Atlantic wolffish (Anarhichas lupus) population in Icelandic waters. Fish Res 195:214–221
Gunnarsson A, Hjorleifsson E, Thorarinsson K, Marteinsdottir G (2008) Growth, maturity and fecundity of female spotted wolffish Anarhichas minor in Icelandic waters. J Fish Biol 73:1393–1406
Gunnarsson A, Hjorleifsson E, Thorarinsson K, Marteinsdottir G (2014) Growth, maturity and fecundity of wolffish Anarhichas lupus L. in Icelandic waters. J Fish Biol 4:1158–1176
Gunnarsson A, Bjornsson H, Elvarsson, Pampoulie C (2016) Spatio-temporal variation in the reproduction timing of Atlantic wolffish (Anarhichas lupus L.) in Icelandic waters and its relationship with size. Fish Res 183:404–409
Hansen TK, Falk-Petersen I-B (2001) The influence of rearing temperature on early development and growth of spotted wolffish Anarhichas minor (Olafsen). Aquac Res 32:369–378
Harmin SA, Crim LW, Wiegand MD (1995) Plasma sex steroid profiles and the seasonal reproductive cycle in male and female winter flounder, Pleuronectes americanus. Mar Biol 121:601–610
Hermelink B, Kleiner W, Schulz C, Kloas W, Wuertz S (2017) Photo-thermal manipulation for the reproductive management of pikeperch Sander lucioperca. Aquac Int 25:1–20
Hinchcliffe J, Carlsson NG, Jönsson E, Erikson S, Sundell K, Undeland I (2016) Sustainable feed formulation for swedish aquaculture from herring by-product. Aquaculture Europe 2016, Edinburg, Scotland https://www.was.org/EasOnline/AbstractDetail.aspx?i=6446. Cited 10 Nov 2017
Imsland AK, Hannssen H, Foss A, Vikingstad E, Roth B, Bjornevik M, Powell M, Solberg C, Norberg B (2013) Short-term exposure to continuous light delays sexual maturation and increases growth of Atlantic cod in sea pens. Aquac Res 44:1665–1676
Johannessen T, Gjøsæter J, Moksness E (1993) Reproduction, spawning behaviour and captive breeding of the common wolffish Anarhichas lupus. Aquaculture 115:41–51
Kamler E (2002) Ontogeny of yolk-feeding fish: an ecological perspective. Rev Fish Biol Fish 12:79–103
Kelly M, DeSilva B (2007) Key elements of bioanalytical method validation for macromolecules. AAPS J 9:E156–E163
Kleinbaum DG, Kupper LL, Muller KE, Nizam A (1988) One-way analysis of variance. In: Curns AT, Nizam A (eds) Applied regression analysis and other multivariable methods. Duxbury Press, Belmont, CA, USA, pp 447–450
Kugathaj S (2005) Effect of 11-ketotestosterone on sperm production by male spotted wolffish (Anarhichas minor). M.Sc. thesis, Norwegian College of Fishery Science, University of Tromsø, Norway, 48 pp. https://munin.uit.no/bitstream/handle/10037/329/thesis.pdf?sequence=1&isAllowed=y. Cited 10 Nov 2017
Lamarre SG, Le François NR, Falk-Petersen I-B, Blier PU (2004) Can digestive and metabolic enzyme activity levels predict growth rate and survival of newly hatched Atlantic wolffish (Anarhichas lupus Olafsen)? Aquac Res 35:608–613
Le François NR, Lemieux H, Blier PU (2002) Biological and technical evaluation of the potential of marine and anadromous fish species for cold-water mariculture. Aquac Res 33:95–108
Le François NR, Lamarre SG, Tveiten H, Blier PU, Bailey J (2008) Sperm cryoconservation in Anarhichas sp., endangered cold-water aquaculture species with internal fertilization. Aquac Int 16:273–279
Le François NR, Savoie A, Blier PU (2010) Quantitative approaches for identifying finfish species suitable for sustainable and productive aquaculture. In: Le François NR, Jobling M, Carter C, Blier PU (eds) Finfish aquaculture diversification. CAB International, Oxfordshire, UK, pp 147–177
Maltais D, Roy RL (2014) Effects of nonylphenol and ethinylestradiol on copper redhorse (Moxostoma hubbsi), an endangered species. Ecotoxicol Environ Saf 108:168–178
Methven DA, Crim LW, Norberg B, Brown JA, Goff GP, Huse I (1992) Seasonal reproduction and plasma levels of sex steroids and vitellogenin in Atlantic halibut (Hippoglossus hippoglossus). Can J Fish Aquat Sci 49:754–759
Migaud H, Wang N, Gardeur JN, Fontaine P (2006) Influence of photoperiod on reproductive performances in Eurasian perch Perca fluviatilis. Aquaculture 252:385–393
Moksness EE, Pavlov DA (1996) Management by lifecycle of wolffish, Anarhichas lupus L., a new species for cold-water aquaculture. Aquac Res 27:865–883
Morehead DT, Ritar AJ, Pankhurst NW (2000) Effect of consecutive 9- or 12-month photothermal cycles and handling on sex steroid levels, oocyte development, and reproductive performance in female striped trumpeter Latris lineata (Latrididae). Aquaculture 189:293–305
Mylonas CC, Fostier A, Zanuy S (2010) Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 165:516–534
Norberg B, Weltzien FA, Karlsen Ø, Holm JC (2001) Effects of photoperiod on sexual maturation and somatic growth in male Atlantic halibut (Hippoglossus hippoglossus L.). Comp Biochem Physiol B Biochem Mol Biol 129:357–365
Pavlov DA, Knudsen P, Moksness E (1997) Spermatozoon ultrastructure and sperm production in wolffish (Anarhichas lupus), a species with internal fertilization. Aquat Living Resour 10:187–194
Plykaytis BD, Holder PF, Pais LB, Maslanka SE, Gheesling LL, Carlone GM (1994) Determination of parallelism and nonparallelism in bioassay dilution curves. J Clin Microbiol 32:2441–2447
R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
Ringo E, Lorentsen E (1987) Brood protection of wolffish (Anarhichas lupus L.) eggs. Aquaculture 65:239–241
Rosten TW, Poulsen H, Alanära A, Eskelinen U, Bergsson AB, Olafsen T (2013) Perspectives for sustainable development of Nordic aquaculture. The Pavan-Report. TemaNord 2013:546. http://norden.diva-portal.org/smash/get/diva2:701192/FULLTEXT01.pdf. Cited October 24 2017
SARA (2008) Recovery strategy for Northen wolffish (Anarhichas denticulatus) and spotted wolffish (Anarhichas minor) and management plan for Atlantic wolffish (Anarhichas lupus) in Canada. Fisheries and Oceans Canada: Newfoundland and Labrador region. St. John’s, NL, 103 pp. https://www.registrelepsararegistry.gc.ca/virtual_sara/files/plans/mp_Atlantic_Northern_and_Spotted_Wolffish_0208_e.pdf. Cited October 24 2017
Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:545–556
Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York, p 887
Sumpter JP (1990) General concepts of seasonal reproduction. In: Muro AD, Scott AP, Lam TJ (eds) Reproductive seasonality in Teleosts: environmental influences. CRC Press, Boca Raton, FL, USA
Taranger GL, Haux C, Stefansson SO, Björnsson BT, Walther BT, Hansen T (1998) Abrupt changes in photoperiod affect age at maturity, timing of ovulation and plasma testosterone and oestradiol-17β profiles in Atlantic salmon, Salmo salar. Aquaculture 162:85–98
Taranger GL, Haux C, Hansen T, Stefansson SO, Björnsson BT, Walther BT, Kryvi H (1999) Mechanisms underlying photoperiodic effects on age at sexual maturity in Atlantic salmon, Salmo salar. Aquaculture 177:47–60
Teletchea F, Fostier A, Kamler E, Gardeur JN, Le Bail P-Y, Jalabert B, Fontaine P (2009) Comparative analysis of reproductive traits in 65 freshwater fish species: application to the domestication of new fish species. Rev Fish Biol Fish 19:403–430
Templeman W (1986a) Contribution to the biology of the spotted wolffish (Anarhichas minor) in the Northwest Atlantic. J Northwest Atl Fish Sci 7:47–55
Templeman W (1986b) Some biological aspects of Atlantic wolffish (Anarhichas lupus) in the Northwest Atlantic. J Northwest Atl Fish Sci 7:57–65
Tveiten H, Johnsen H (2001a) Temperature experienced during vitellogenesis influences ovarian maturation and the timing of ovulation in common wolffish. J Fish Biol 55:809–819
Tveiten H, Johnsen H (2001b) Thermal influences on temporal changes in plasma testosterone and oestradiol-17β concentrations during gonadal recrudescence in female common wolffish. J Fish Biol 59:175–178
Tveiten H, Solevåg S, Johnsen H (2001) Holding temperature during the breeding season influences final maturation and egg quality in common wolffish. J Fish Biol 58:374–385
Valdebenito I, Paiva L, Berland M (2011) Follicular atresia in teleost fish: a review. Archivos de medecina veterinaria 43:11–25
Van Der Kraak G, Pankhurst NW (1997) Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds) Global warming: implications of freshwater and marine fish. Society for Experimental Biology Seminar Series 61. Cambridge University Press, UK, pp 159–176
Von Bayer H (1910) A method of measuring fish eggs. Bulletin of the bureau of fisheries XXVII:1009–1014
Wang N, Teletchea F, Kestemont P, Milla S, Fontaine P (2010) Photothermal control of the reproductive cycle in temperate fishes. Rev Aquaculture 2:209–222
Weltzien FA, Andersson E, Andersen Ø, Shalchian-Tabrizi K, Norberg B (2004) The brain–pituitary–gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp Biochem Physiol A Mol Int Physiol 137:447–477
Acknowledgements
The present study was funded by the department of Fisheries and Oceans Canada under the Aquaculture Collaborative R&D Program (ACRDP-PCRDA) and the AquaNet excellence network (AP-34) in collaboration with the Ministère de l’agriculture, des pêcheries et de l’alimentation du Québec (MAPAQ). The authors acknowledge the meaningful contribution of Dr. Robert Roy of DFO-MPO (deceased in 2014) and would like to express their gratitude to D. Ouellet, A. Savoie, and T. Grenier for their technical assistance.
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Dupont Cyr, BA., Tveiten, H., Maltais, D. et al. Photoperiod manipulation for the reproductive management of captive wolffish populations: Anarhichas minor and A. lupus. Aquacult Int 26, 1051–1065 (2018). https://doi.org/10.1007/s10499-018-0267-x
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DOI: https://doi.org/10.1007/s10499-018-0267-x