Abstract
The aim of this study was to evaluate the effects of increasing dietary arachidonic acid (ARA) levels (from 1 to 6% of total fatty acids) on European sea bass (Dicentrarchus labrax) juveniles’ growth performance, tissue fatty acid profile, liver morphology as well as long-chain polyunsaturated fatty acids (LC-PUFA) biosynthesis, triglyceride and cholesterol synthesis and lipid transport. A diet with total fish oil (FO) replacement and defatted fish meal (FM) containing a 0.1-g ARA g−1 diet was added to the experimental design as a negative control diet. Dietary ARA inclusion levels below 0.2 g ARA g−1 diet significantly worsened growth even only 30 days after the start of the feeding trial, whereas dietary ARA had no effect on fish survival. Liver, muscle and whole body fatty acid profile mainly reflected dietary contents and ARA content increased accordingly with ARA dietary levels. Tissue eicosapentaenoic acid (EPA), docosapentaenoic acid (DPA) and docosahexaenoic acid (DHA) levels were positively correlated among them. Hepatic lipid vacuolization increased with reduced dietary ARA levels. Expressions of fatty acyl desaturase 2 and 3-hydroxy-3-methylglutaryl-coenzyme genes were upregulated in fish fed the negative control diet compared to the rest of the dietary treatments denoting the influence of ARA on lipid metabolism. Results obtained highlight the need to include adequate n-6 levels and not only n-3 LC-PUFA levels in European sea bass diets.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- LC-PUFA:
-
Long-chain polyunsaturated fatty acid
- DHA:
-
Docosahexaenoic acid
- ARA:
-
Arachidonic acid
- EPA:
-
Eicosapentaenoic acid
- DPA:
-
Docosapentaenoic acid
- HSI:
-
Hepatosomatic index
- PFI:
-
Perivisceral fat index
- VSI:
-
Viscerosomatic index
- K:
-
Condition factor
- SGR:
-
Specific growth rate
- FCR:
-
Feed conversion ratio
- fads2 :
-
Fatty acid desaturase gene
- gck :
-
Glycerol kinase gene
- hmgrc :
-
3-Hydroxy-3-methylglutaryl-coenzyme A reductase gene
- fabp7 :
-
Fatty acid binding protein gene
References
AOAC (2000) Official methods of analysis. Association of Official Analytical Chemists, Washington, DC
Atalah E, Hernández-Cruz CM, Benítez-Santana T, Ganga R, Roo J, Izquierdo M (2011) Importance of the relative levels of dietary arachidonic acid and eicosapentaenoic acid for culture performance of gilthead seabream (Sparus aurata) larvae. Aquac Res 42:1279–1288. https://doi.org/10.1111/j.1365-2109.2010.02716.x
Bell JG, Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218:491–499. https://doi.org/10.1016/S0044-8486(02)00370-8
Bessonart M, Izquierdo MS, Salhi M, Hernández-Cruz CM, González MM, Fernández-Palacios H (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream (Sparus aurata L.) larvae. Aquaculture 179:265–275. https://doi.org/10.1016/S0044-8486(99)00164-7
Betancor MB, Howarth FJE, Glencross BD, Tocher DR (2014) Influence of dietary docosahexaenoic acid in combination with other long-chain polyunsaturated fatty acids on expression of biosynthesis genes and phospholipid fatty acid compositions in tissues of post-smolt Atlantic salmon (Salmo salar). Comp Biochem Physiol 172-173B:74–89. https://doi.org/10.1016/j.cbpb.2014.04.007
Betancor MB, Sprague M, Usher S, Sayanova O, Campbell PJ, Napier JA, Tocher DR (2015a) A nutritionally-enhanced oil from transgenic Camelina sativa effectively replaces fish oil as a source of eicosapentaenoic acid for fish. Sci Rep 5:8104. https://doi.org/10.1038/srep08104
Betancor MB, Sprague M, Sayanova O, Usher S, Campbell PJ, Napier JA, Caballero MJ, Tocher DR (2015b) Evaluation of a high-EPA oil from transgenic Camelina sativa in feeds for Atlantic salmon (Salmo salar L.): effects on tissue fatty acid composition, histology and gene expression. Aquaculture 444:1–12. https://doi.org/10.1016/j.aquaculture.2015.03.020
Betancor MB, Sprague M, Sayanova O, Usher S, Metochis C, Campbell PJ, Napier JA, Tocher DR (2016a) Nutritional evaluation of an EPA-DHA oil from transgenic Camelina sativa in feeds for post-smolt Atlantic salmon (Salmo salar L.) PLoS One 11:e0159934. https://doi.org/10.1371/journal.pone.0159934
Betancor MB, Sprague M, Montero D, Usher S, Sayanova O, Campbell PJ, Napier JA, Caballero MJ, Izquierdo M, Tocher DR (2016b) Replacement of marine fish oil with de novo omega-3 oils from transgenic Camelina sativa in feeds for gilthead sea bream (Sparus aurata L.) Lipids 51:1171–1191. https://doi.org/10.1007/s11745-016-4191-4
Boglino A, Wishkerman A, Darias MJ, de la Iglesia P, Andree KP, Gisbert E, Estévez A (2014) Senegalese sole (Solea senegalensis) metamorphic larvae are more sensitive to pseudo-albinism induced by high dietary arachidonic acid levels than post-metamorphic larvae. Aquaculture 433:276–287. https://doi.org/10.1016/j.aquaculture.2014.06.012
Caballero MJ, Obach A, Rosenlund G, Montero E, Gisvold M, Izquierdo MS (2002) Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture 214:253–271. https://doi.org/10.1016/S0044-8486(01)00852-3
Caballero MJ, Gallardo G, Robaina L, Montero D, Fernández A, Izquierdo M (2006) Vegetable lipid sources affect in vitro biosynthesis of triacylglycerols and phospholipids in the intestine of sea bream (Sparus aurata). Br J Nutr 95:448–454. https://doi.org/10.1079/BJN20051529
Caballero MJ, Izquierdo MS, Kjorsvik E, Montero D, Socorro J, Fernández A, Rosenlund G (2003) Morphological aspects of the intestinal cells from gilthead seabream (Sparus aurata) fed diets containing different lipid sources. Aquaculture 225:325-340. https://doi.org/10.1016/S0044-8486(03)00299-0
Calder PC (2006) N-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83(6):S1505–S119S
Calder PC (2008) The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot Essent Fat Acids 79:101–108. https://doi.org/10.1016/j.plefa.2008.09.016
Carrier JK, Watanabe WO, Harel M, Rezek TC, Seaton PJ, Shafer TH (2011) Effects of dietary arachidonic acid on larval performance, fatty acid profiles, stress resistance, and expression of Na+/K+ ATPase mRNA in black sea bass Centropristis striata. Aquaculture 319:111–121. https://doi.org/10.1016/j.aquaculture.2011.06.027
Castell JD, Bell JG, Tocher DR, Sargent JR (1994) Effects of purified diets containing different combinations of arachidonic and docosahexaenoic acid on survival, growth and fatty acid composition of juvenile turbot (Scophthalmus maximus). Aquaculture 128:315–333. https://doi.org/10.1016/0044-8486(94)90320-4
Castro C, Corraze G, Panserat S, Oliva-Teles A (2015) Effects of fish oil replacement by a vegetable oil blend on digestibility, postprandial serum metabolite profile, lipid and glucose metabolism of European sea bass (Dicentrarchus labrax) juveniles. Aquac Nutr 21:592–603. https://doi.org/10.1111/anu.12184
Christie WW (2003) Lipid Analysis, 3rd edn. Oily Press, Bridgwater
Dantagnan P, González K, Hevia M, Betancor MB, Hernández AJ, Borquez A, Montero D (2017) Effect of the arachidonic acid/vitamin E interaction on the immune response of juvenile Atlantic salmon (Salmo salar) challenged against Piscirickettsia salmonis. Aquac Nutr 23:710–720. https://doi.org/10.1111/anu.12438
Folch J, Lees N, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Fountoulaki E, Alexis MN, Nengas I, Venou B (2003) Effects of dietary arachidonic acid (20:4n-6) on growth, body composition and tissue fatty acid profile of gilthead sea bream fingerlings (Sparus aurata L.) Aquaculture 225:309–323. https://doi.org/10.1016/S0044-8486(03)00298-9
Furuita H, Yamamoto T, Shima T, Suzuki N, Takeuchi T (2003) Effect of arachidonic acid levels in broodstock diet on larval and egg quality of Japanese flounder Paralichthys olivaceus. Aquaculture 220:725–735. https://doi.org/10.1016/S0044-8486(02)00617-8
Geay F, Santigosa E, Corporeau C, Boudry P, Dreano Y, Corcos L, Bodin N, Vandeputte M, Zambonino-Infante JL, Mazurais D, Cahu CL (2010) Regulation of FADS2 expression and activity in European sea bass (Dicentrarchus labrax) fed a vegetable oil. Comp Biochem Physiol Part B: Biochem Mol Biol 156:237–243. https://doi.org/10.1016/j.cbpb.2010.03.008
Geay F, Ferraresso S, Zambonino-Infante JL, Bargelloni L, Quentel C, Vandeputte M, Kaushik S, Cahu CL, mazurais D (2011) Effects of the total replacement of fish-based diet with plant-based diet on the hepatic transcriptome of two European sea bass (Dicentrarchus labrax) half-sibfamilies showing different growth rates with the plant-based diet. BMC Genomics 12:522. https://doi.org/10.1186/1471-2164-12-522
Gilman CI, Leusch FD, Breckenridge WC, MacLatchy DL (2003) Effects of a phytosterol mixture on male fish plasma lipoprotein fractions and testis P450scc activity. Gen Comp Endocrinol 130:172–184. https://doi.org/10.1016/S0016-6480(02)00590-7
González-Rovira A, Mourent G, Zheng X, Tocher DR, Pendon C (2009) Molecular and functional characterization and expression analysis of a delta-6 fatty acyl desaturase cDNA of European sea bass (Dicentrarchus labrax L.) Aquaculture 298:90–100. https://doi.org/10.1016/j.aquaculture.2009.10.012
Higgs DA, Dong FM (2000) Lipids and fatty acids. The encyclopedia of aquaculture. John Wiley and Sons, New York, pp 476–496
Izquierdo MS, Koven (2011) Lipids. In: Holt J (ed) Larval fish nutrition. Wiley-Blackwell, John Wiley and Sons Publisher, Oxford, pp 47–82
Izquierdo MS, Arakawa T, Takeuchi T, Haroun R, Watanabe T (1992) Effect of n-3 HUFA levels in Artemia on growth of larval Japanese flounder (Paralichthys olivaceus). Aquac Nutr 2:183–191. https://doi.org/10.1016/0044-8486(92)90163-F
Izquierdo MS, Obach A, Arantzamendi L, Montero D, Robaina LE, Rosenlund G (2003) Dietary lipid sources for seabream and sea bass: growth performance, tissue composition and flesh quality. Aquac Nutr 9:397–407. https://doi.org/10.1046/j.1365-2095.2003.00270.x
Kiron V, Thawonsuwan J, Panigrahi A, Scharsack J, Satoh S (2011) Antioxidant and immune defences of rainbow trout (Oncorhynchus mykiss) offered plant oils differing in fatty acid profiles from early stages. Aquac Nutr 17:130–140. https://doi.org/10.1111/j.1365-2095.2009.00715.x
Koven W, Barr Y, Luzky S, Ben-Atia I, Weiss R, Harel M et al (2001) The effect of dietary arachidonic acid (20:4n-6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193:107–122. https://doi.org/10.1016/S0044-8486(00)00479-8
Koven W, Anholt RV, Lutzsky S, Atia IB, Nixon O, Ron B et al (2003) The effect of dietary arachidonic acid on growth, survival, and cortisol levels in different-age gilthead seabream larvae Sparus auratus exposed to handling or daily salinity change. Aquaculture 228:307–320. https://doi.org/10.1016/S0044-8486(03)00317-X
Le Boucher R, Vandeputte M, Dupont-Nivet M, Quillet E, Mazurais D, Robin J, Vergnet A, Médale F, Kaushik S, Chatain B (2011) A first insight into genotype × diet interactions in European sea bass (Dicentrarchus labrax L. 1756) in the context of plant-based diet use. Aquac Res 42:583–592
Le Boucher R, Vandeputte M, Dupont-Nivet M, Quillet E, Ruelle F, Vergnet A, Kaushik S, Allamellou M, Médale F, Chatain B (2013) Genotype by diet interactions in European sea bass (Dicentrarchus labrax L.): nutritional challenge with totally plant-based diets. J Anim Sci 91:44–56
Le Martelot G, Claudel T, Gatfield D, Schaad O, Kornman, Lo Sasso G, Moschetta A, Schibler U (2009) REV-ERBa participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol 7(9):e1000181. https://doi.org/10.1371/journal.pbio.1000181
Leaver MJ, Villeneuve LAN, Obach A, Jensen L, Bron JE, Tocher DR, Taggart JB (2008) Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 9:299. https://doi.org/10.1186/1471-2164-9-299
Lilleeng E, Frøystad MK, Vekterud K, Valen EC, Krogdahl Å (2007) Comparison of intestinal gene expression in Atlantic cod (Gadus morhua) fed standard fish meal or soybean meal by means of suppression subtractive hybridization and real-time PCR. Aquaculture 267:269–283. https://doi.org/10.1016/j.aquaculture.2007.01.048
Livak KJ, Schimittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lund I, Steenfeldt SJ, Hansen BW (2007) Effect of dietary ARA, EPA and DHA on the fatty acid composition, survival, growth and pigmentation of larvae of common sole (Solea solea L.) Aquaculture 273:532–544. https://doi.org/10.1016/j.aquaculture.2007.10.047
Lund I, Steenfeldt SJ, Hansen BW (2010) Influence of dietary arachidonic acid combined with light intensity and tank colour on pigmentation of common sole (Solea solea L.) larvae. Aquaculture 308:159–165. https://doi.org/10.1016/j.aquaculture.2010.08.004
Luo Z, Tan XY, Li XD, Yin G-J (2012) Effect of dietary arachidonic acid levels on growth performance, hepatic fatty acid profile, intermediary metabolism and antioxidant responses for juvenile Synechogobius hasta. Aquac Nutr 18:340–348. https://doi.org/10.1111/j.1365-2095.2011.00906.x
Martins DA, Rocha F, Martínez-Rodríguez G, Bell G, Morais S, Castanheira F, Bandarra N, Coutinho J, Yúfera M, Conceição L (2012) Teleost fish larvae adapt to dietary arachidonic acid supply through modulation of the expression of lipid metabolism and stress response genes. Br J Nutr 108:864–874. https://doi.org/10.1017/S0007114511006143
Martoja R, Martoja-Pearson M (1970) Técnicas de Histología Animal. Toray-Masson SA (ed), Barcelona, p350
Monroig O, Zheng X, Morais S, Leaver MJ, Taggart JB, Tocher DR (2010) Multiple genes for functional Δ6 fatty acyl desaturases (Fad) in Atlantic salmon (Salmo salar L.): gene and cDNA characterization, functional expression, tissue distribution and nutritional regulation. Biochim Biophys Acta 1801:1072–1081. https://doi.org/10.1016/j.bbalip.2010.04.007
Montero D, Izquierdo MS (2010) Welfare and health of fish fed vegetable oils as alternative lipid sources to fish oil. In: Turchini G, Ng W, Tocher D (eds) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Cambridge, pp 439–485
Montero D, Robaina LE, Caballero MJ, Gin_es R, Izquierdo MS (2005) Growth, feed utilization and flesh quality of European sea bass (Dicentrarchus labrax) fed diets containing vegetable oils. A time-course study on the effects of re-feeding period with a 100% fish oil diet. Aquaculture 248:121–134. https://doi.org/10.1016/j.aquaculture.2005.03.003
Montero D, Terova G, Rimoldi S, Betancor MB, Atalah E, Torrecillas S, Caballero MJ, Zamorano MJ, Izquierdo M (2015) Modulation of the expression of components of the stress response by dietary arachidonic acid in European sea bass (Dicentrarchus labrax) larvae. Lipids 50:1026–1041. https://doi.org/10.1007/s11745-015-4057-1
Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12:255. https://doi.org/10.1186/1471-2164-12-255
Mourente G, Dick JR, Bell JG, Tocher DR (2005) Effects of partial substitution of dietary fish oil by vegetable oils on desaturation and β-oxidation of [1-14-C] 18:3n-3 (LNA) and [1-14C] 20:5n-3 (EPA) in hepatocytes and enterocytes of European sea bass (Dicentrarchus labrax L.) Aquaculture 248:173–186. https://doi.org/10.1016/j.aquaculture.2005.04.023
Norambuena F, Estévez A, Sánchez-Vázquez FJ, Carazo I, Duncan N (2012) Self-selection of diets with different content of arachidonic acid by Senegalese sole (Solea senegalensis) broodstock. Aquaculture 364:198–205. https://doi.org/10.1016/j.aquaculture.2012.08.016
Norambuena F, Lewis M, Hadid NKA, Hermon K, Donald JA, Turchini GM (2013) Fish oil replacement in current aquaculture feed: is cholesterol a hidden treasure for fish nutrition? PLoS One 8:e81705. https://doi.org/10.1371/journal.pone.0081705
Norambuena F, Rombenso A, Turchini GM (2016) Towards the optimization of Atlantic salmon reared at different water temperatures via the manipulation of dietary ARA/EPA ratio. Aquaculture 450:48–57. https://doi.org/10.1016/j.aquaculture.2015.06.044
Palmer RM (1990) Prostaglandins and the control of muscle protein synthesis and degradation. Prostaglandins Leukot Essent Fatty Acids 39:95–104. https://doi.org/10.1016/0952-3278(90)90017-F
Panserat S, Hortopan GA, Plagnes-Juan E, Kolditz C, Lansard M, Skiba-Cassy S, Esquerré D, Geurden I, Médale F, Kaushik S, Corraze G (2009) Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–131. https://doi.org/10.1016/j.aquaculture.2009.05.013
Rezek TC, Watanabe WO, Harel M, Seaton PJ (2010) Effects of dietary docosahexaenoic acid (22:6n-3) and arachidonic acid (20:4n-6) on the growth, survival, stress resistance and fatty acid composition in black sea bass, Centropristis striata (Linnaeus 1758) larvae. Aquac Res 41:1302–1314. https://doi.org/10.1111/j.1365-2109.2009.02418.x
Rombenso AN, Trushenki JT, Jirsa D, Drawbridge M (2016) Docosahexaenoic acid (DHA) and arachidonic acid (ARA) are essential to meet LC-PUFA requirements of juvenile California Yellowtail (Seriola dorsalis). Aquaculture 463:123–134. https://doi.org/10.1016/j.aquaculture.2016.05.004
Salini MJ, Wade NM, Araújo BC, Turchini GM, Glencross BD (2016) Eicosapentaenoic acid, arachidonic acid and eicosanoid metabolism in juvenile Barramundi Lates calcarifer. Lipids 51:973–988. https://doi.org/10.1007/s11745-016-4167-4
Smith WL, Murphy RC (2002) The eicosanoids: cyclooxygenase, lipoxygenase, and epoxygenase pathways. In: Vance DE, Vance JE (Eds) Biochemistry of Lipids, Lipoproetins and Membranes (4th Ed). Elsevier Sicence BV. 36:341–371
Sokal RR, Rolf SJ (1995) Biometry. In: Taylor, Francis (eds) The principles and practice of statistics in biological research, 3rd edn. Freeman, New York, p 419
Tian JJ, Ji H, Oku H, Zhou JS (2014) Effects of dietary arachidonic acid (ARA) on lipid metabolism and health status of juvenile grass carp, Ctenopharyngodon idellus. Aquaculture 430:57–65. https://doi.org/10.1016/j.aquaculture.2014.03.020
Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquac Res 41:717–732. https://doi.org/10.1111/j.1365-2109.2008.02150.x
Torrecillas S, Caballero MJ, Montero D, Sweetman J, Izquierdo MS (2016) Combined effects of dietary mannan oligosaccharides and total fish oil substitution by soybean oil on European sea bass (Dicentrarchus labrax) juvenile diets. Aquac Nutr 22:1079–1090. https://doi.org/10.1111/anu.12322
Torrecillas S, Robaina L, Caballero MJ, Montero D, Calandra G, Mompel D, Karalazos V, Kaushik S, Izquierdo MS (2017a) Combined replacement of fishmeal and fish oil in European sea bass (Dicentrarchus labrax): production performance, tissue composition and liver morphology. Aquaculture 474:101–112. https://doi.org/10.1016/j.aquaculture.2017.03.031.
Torrecillas S, Román L, Rivero-Ramírez F, Caballero MJ, Pascual C, Robaina L, Izquierdo MS, Acosta F, Montero D (2017b) Supplementation of arachidonic acid rich oil in European sea bass juveniles (Dicentrarchus labrax) diets: effects on leucocytes and plasma fatty acid profiles, selected immune parameters and circulating prostaglandins levels. Fish Shellfish Immunol 64:437–445. https://doi.org/10.1016/j.fsi.2017.03.041
Waagbø R (2006) Chapter 13 Feeding and disease resistance in fish. In: Mosenthin R, Zentek J and Żebrowska T (eds) Biology of Growing Animals 4, p 387–415. https://doi.org/10.1016/S1877-1823(09)70100-6
Xu H, Ai Q, Mai K, Xu W, Wang J, Ma H, Zhang W, Wang X, Liufu Z (2010) Effects of dietary arachidonic acid on growth performance, survival, immune response and tissue fatty acid composition of juvenile Japanese seabass, Lateolabrax japonicus. Aquaculture 307:75–82. https://doi.org/10.1016/j.aquaculture.2010.07.001
Yuan YH, Li SL, Mai KS, Xu W, Zhang YJ, Ai QH (2015) The effect of dietary arachidonic acid (ARA) on growth performance. Fatty acid composition and expression of ARA metabolism-related genes in larval half-smooth tongue sole (Cynoglossus semilaevis). Br J Nutr 113:1518–1530. https://doi.org/10.1017/S0007114515000781
Funding
This work was funded by the Spanish Ministry of Economy and Competitiveness (MINECO). Project AGL2012-39919 (PROINMUNOIL). Complementarily, it has been financed through a ULPGC postdoctoral fellowship (PICULPGC-2013-CIENCIAS, concept 643.00.06) and a predoctoral fellowship (ULPGC-2013).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The animal experiments described comply with the guidelines of the European Union Council (86/609/EU) and Spanish legislation (RD 1201/2005) for the use of laboratory animals and have been approved by the Bioethical Committee of the University of Las Palmas de Gran Canaria.
Rights and permissions
About this article
Cite this article
Torrecillas, S., Betancor, M.B., Caballero, M.J. et al. Supplementation of arachidonic acid rich oil in European sea bass juveniles (Dicentrarchus labrax) diets: effects on growth performance, tissue fatty acid profile and lipid metabolism. Fish Physiol Biochem 44, 283–300 (2018). https://doi.org/10.1007/s10695-017-0433-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-017-0433-5