Fisheries Science

, Volume 84, Issue 4, pp 699–713 | Cite as

Periodic changes in the growth performance and biochemical composition of juvenile red sea bream Pagrus major fed non-heated and heated squid and krill meal-based diets

  • Jeong-Hyeon Cho
  • Yutaka HagaEmail author
  • Reiji Masuda
  • Shuichi Satoh
Original Article Aquaculture


In finfish aquaculture, fish meal is heated during the manufacturing process, which affects the digestibility and protein absorption by fish. However, manufactured fishmeal that is not heated does not undergo thermal denaturation. Few studies have investigated the effects of non-heated animal protein sources on the growth performance of fish. We investigated the effects of heated and non-heated squid and krill meal as diets for red sea bream. Five test diets were formulated to contain heated squid meal, non-heated squid meal, heated krill meal, non-heated krill meal, and fish meal as a control. Fifty fish (initial mean weight = 3.5 g) were distributed in ten 100-l experimental tanks. Fish were fed one of the five diets 3 times daily until satiation for 5 weeks. Regarding growth performance, fish fed the krill meal diet exhibited better growth than those fed squid meal during the first week of the rearing period. However, the squid meal diet group showed better performance than the krill meal diet group during the third week. Moreover, differences in body weight among treatments were greater during the fifth week. Better weight gain and thermal growth coefficient were recorded in the non-heated diet groups than in the heated diet groups. Higher feed intake was observed in the non-heated diet groups than in the heated diet groups. These results suggest higher performance of non-heated squid and krill meal as the protein source of the red sea bream diet. Further, the suitability of the diet type (e.g., squid and krill) might depend on the feeding period and/or developmental stage of fish.


Red sea bream Pagrus major Squid and krill meal Non-heat treatment meal Fish growth Proximate composition Water soluble protein 



This study was supported by a Grant-in-Aid for Scientific Research (26252034) from the Japanese Society for Promotion of Science to S. S. and a scholarship from the Tokyu Foundation for Foreign Students to J-H.C.


  1. Ajandouz EH, Puigserver A (1999) Nonenzymatic browning reaction of essential amino acids: effect of pH on caramelization and Maillard reaction kinetics. J Agric Food Chem 47:1786–1793CrossRefPubMedGoogle Scholar
  2. Amaya EA, Davis DA, Rouse DB (2007) Replacement of fish meal in practical diets for the Pacific white shrimp (Litopenaeus vannamei) reared under pond conditions. Aquaculture 262:393–401CrossRefGoogle Scholar
  3. AOAC (1995) Official methods of analysis. Association of the Official Analytical Chemists, ArlingtonGoogle Scholar
  4. Bell JG, McEvoy LA, Estevez A, Shields RJ, Sargent JR (2003) Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227:211–220CrossRefGoogle Scholar
  5. Bessonart M, Izquierdo MS, Salhi M, Hernández CCM, González MM, Fernández PH (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream Sparus aurata larvae. Aquaculture 179:265–275CrossRefGoogle Scholar
  6. Biswas AK, Kaku H, Ji SC, Seoka M, Takii K (2007) Use of soybean meal and phytase for partial replacement of fish meal in the diet of red sea bream, Pagrus major. Aquaculture 267:284–291CrossRefGoogle Scholar
  7. Boonyoung S, Haga Y, Satoh S (2012) Preliminary study on effects of methionine hydroxyl analog and taurine supplementation in a soy protein concentrate-based diet on the biological performance and amino acid composition of rainbow trout Oncorhynchus mykiss (Wallbaum). Aquac Res 44:1339–1347CrossRefGoogle Scholar
  8. Boyd CE, Tucker C, McNevin A, Bostick K, Clay J (2007) Indicators of resource use efficiency and environmental performance in fish and crustacean aquaculture: a review. Fish Sci 15:327–360CrossRefGoogle Scholar
  9. Cho SH, Lee SM, Lee SM, Park BH, Park IS, Choi CY, Min BH, Hur SB, Jo JY (2005) Effect of partial replacement of fish meal with squid liver meal™ in the diet on growth and body composition of juvenile olive flounder (Paralichthys olivaceus) during winter season. Fish Aquat Sci 8:65–69Google Scholar
  10. Cho JH, Haga Y, Kamimura Y, Akazawa A, Itoh A, Satoh S (2016) Production performance of Pacific bluefin tuna Thunnus orientalis larvae and juveniles fed commercial diets and effects of switching diets. Aquac Sci 64:359–370Google Scholar
  11. De Schrijver R, Ollevier F (2000) Protein digestion in juvenile turbot (Scophthalmus maximus) and effects of dietary administration of Vibrio proteolyticus. Aquaculture 186:107–116CrossRefGoogle Scholar
  12. Everson I (2000) Krill: biology, ecology, and fisheries. Blackwell Science, OxfordCrossRefGoogle Scholar
  13. FAO (2015) The state of world fisheries and aquaculture 2014. Accessed 11 May 2015
  14. Floreto EA, Bayer RC, Brown PB (2000) The effects of soybean-based diets, with and without amino acid supplementation, on growth and biochemical composition of juvenile American lobster, Homarus americanus. Aquaculture 189:211–235CrossRefGoogle Scholar
  15. Folch J, Lees M, Stanley GHS (1957) A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–507PubMedGoogle Scholar
  16. Forster I, Ogata HY (1998) Lysine requirement of juvenile Japanese flounder Paralichthys olivaceus and juvenile red sea bream Pagrus major. Aquaculture 161:131–142CrossRefGoogle Scholar
  17. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  18. Furuita H, Takeuchi T, Watanabe T, Fujimoto H, Sekiya S, Imaizumi K (1996) Requirement of larval yellowtail for eicosapentaenoic acid, docosahexaenoic acid, and n-3 highly unsaturated fatty acid. Fish Sci 62:372–379CrossRefGoogle Scholar
  19. Fyhn HJ (1989) First feeding of marine fish larvae: are free amino acids the source of energy? Aquaculture 80:111–120CrossRefGoogle Scholar
  20. Fyhn HJ, Serigstad B (1987) Free amino acids as energy substrate in developing eggs and larvae of the cod Gudas morhua. Mar Biol 96:335–341CrossRefGoogle Scholar
  21. Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579CrossRefGoogle Scholar
  22. Glencross BD, Booth M, Allan GL (2007) A feed is only as good as its ingredients—a review of ingredient evaluation strategies for aquaculture feeds. Aquac Nutr 13:17–34CrossRefGoogle Scholar
  23. Hansen JØ, Shearer KD, Øverland M, Penn MH, Krogdahl Å, Mydland LT, Storebakken T (2011) Replacement of LT fish meal with a mixture of partially deshelled krill meal and pea protein concentrates in diets for Atlantic salmon (Salmo salar). Aquaculture 315:275–282CrossRefGoogle Scholar
  24. Huang SSY, Oo AN, Higgs DA, Brauner CJ, Satoh S (2007) Effect of dietary canola oil level on the growth performance and fatty acid composition of juvenile red sea bream, Pagrus major. Aquaculture 271:420–431CrossRefGoogle Scholar
  25. Ishihara K, Saito H (1996) The docosahexaenoic acid content of the lipid of juvenile bluefin tuna Thunnus orientalis caught in the sea off Japanese coast. Fish Sci 62:840–841CrossRefGoogle Scholar
  26. Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M, Honda Y, Mamauag RE, Laining A (2011) Growth, nutrient utilization, oxidative condition, and element composition of juvenile red sea bream Pagrus major fed with fermented soybean meal and scallop by-product blend as fish meal replacement. Fish Sci 77:119–128CrossRefGoogle Scholar
  27. Koshio S (2002) Red sea bream, Pagrus major. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New York, pp 51–63CrossRefGoogle Scholar
  28. Lim SJ, Lee KJ (2009) Partial replacement of fish meal by cottonseed meal and soybean meal with iron and phytase supplementation for parrot fish Oplegnathus fasciatus. Aquaculture 290:283–289CrossRefGoogle Scholar
  29. Lu HFS, Bruheim I, Jacobsen C (2014) Oxidative stability and non-enzymatic browning reactions in Antarctic krill oil (Euphausia superba). Lipid Tech 26:111–114CrossRefGoogle Scholar
  30. MAFF (2017) Statistics Division from Ministry of Agriculture, Forestry and Fisheries of Japan: Fisheries and aquaculture production statistics report (inclusive of fisheries economics, October 2015)Google Scholar
  31. Matsukura K, Iino S, Haga Y, Kitagima R, Satoh S (2017) Effect of supplementation with enzyme complex to non-fish meal diet in adult red sea bream Pagrus major. Aquac Sci 65:19–27Google Scholar
  32. McCallum IM, Higgs DA (1989) An assessment of processing effects on the nutritive value of marine protein sources for juvenile chinook salmon (Oncorhynchus tshawytscha). Aquaculture 77:181–200CrossRefGoogle Scholar
  33. MMAF (2013) Aquaculture Statistic from Ministry of Maritime Affairs and Fisheries of Korea (2013)Google Scholar
  34. Morrison WR, Smith LM (1964) Preparation of fatty acid methylesters and dimethyl acetals from lipids with boron trifluoridemethanol. J Lipid Res 5:600–608PubMedGoogle Scholar
  35. Nordgreen A, Tonheim S, Hamre K (2009) Protein quality of larval feed with increased concentration of hydrolysed protein: effects of heat treatment and leaching. Aquac Nutr 15:525–536CrossRefGoogle Scholar
  36. Olsen RE, Suontama J, Langmyhr E, Mundheim H, Ringø E, Melle W, Malde MK, Hemre GI (2006) The replacement of fish meal with Antarctic krill, Euphausia superba in diets for Atlantic salmon, Salmo salar. Aquac Nutr 12:280–290CrossRefGoogle Scholar
  37. Ostaszewska T, Dabrowski K, Palacios ME, Olejniczak M, Wieczorek M (2005) Growth and morphological changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture 245:273–286CrossRefGoogle Scholar
  38. Pérez-Jiménez A, Guedes MJ, Morales AE, Olivia-Teles A (2007) Metabolic responses to short starvation and refeeding in Dicentrarchus labrax. Effect of dietary composition. Aquaculture 265:325–335CrossRefGoogle Scholar
  39. Rehbein H (1981) Amino acid composition and pepsin digestibility of krill meal. J Agric Food Chem 29:682–684CrossRefPubMedGoogle Scholar
  40. Sáez MI, Navarro G, García MS, Martínez TF, García GM, Suárez MD (2013) Influence of pre-slaughtering feed restriction on muscle characteristics of farmed sea bass (Dicentrarchus labrax L.) during cold storage. J Sci Food Agric 93:2323–2330CrossRefPubMedGoogle Scholar
  41. Saito H, Ishihara K, Murase T (1996) Effect of prey fish lipids on the docosahexaenoic acid content of total fatty acids in the lipid of Thunnus albacores yellowfin tuna. Biosci Biotech Biochem 60:962–965CrossRefGoogle Scholar
  42. Sargent J, McEvoy L, Estevez A, Bell G, Bell M, Henderson J, Tocher D (1999) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179:217–229CrossRefGoogle Scholar
  43. Shiau SY (1997) Utilization of carbohydrates in warmwater fish—with particular reference to tilapia, Oreochromis niloticus × O. aureus. Aquaculture 151:79–96CrossRefGoogle Scholar
  44. Skalli A, Hidalgo MC, Abellán E, Arizcum M, Cardenete G (2004) Effects of the dietary protein/lipid ratio on growth and nutrient utilization in common dentex (Dentex dentex L.) at different growth stages. Aquaculture 235:1–11CrossRefGoogle Scholar
  45. Skipnes D, Plancken IV, Loey AV, Hendrickx ME (2008) Kinetics of heat denaturation of proteins from farmed Atlantic cod (Gadus morhua). J Food Eng 85:51–58CrossRefGoogle Scholar
  46. Storebakken T, Refstie S, Ruyter B (2000) Soy products as fat and protein sources in fish feeds for intensive aquaculture. In: Drackly JK (ed) Soy in animal nutrition. Federation of Animal Science Societies, Champaign, pp 127–170Google Scholar
  47. Takeuchi T, Arai S, Watanabe T, Shimma Y (1980) Requirement of eel Anguilla japonica for essential fatty acids. Nippon Suisan Gakkaishi 46:345–353 (in Japanese with English abstract) CrossRefGoogle Scholar
  48. Takeuchi T, Toyota M, Satoh S, Watanabe T (1990) Requirement of juvenile red sea bream Pagrus major for eicosapentaenoic and docosahexaenoic acids. Nippon Suisan Gakkaishi 58:1263–1269CrossRefGoogle Scholar
  49. Takii K, Seoka M, Izumi M, Hosokawa H, Shimeno S, Ukawa M, Kohbara J (2007) Apparent digestibility coefficient and energy partition of juvenile Pacific bluefin tuna, Thunnus orientalis and chub mackerel, Scomber japonicus. Aquac Sci 55:571–577Google Scholar
  50. Taşbozan O, Emre Y, Gökçe MA, Erbaş C, Özcan F, Kıvrak E (2016) The effects of different cycles of starvation and re-feeding on growth and body composition in rainbow trout (Oncorhynchus mykiss, Walbaum, 1792). J Appl Ichthyol 32:583–588CrossRefGoogle Scholar
  51. Tibbetts SM, Olsen RE, Lall SP (2011) Effects of partial or total replacement of fish meal with freeze-dried krill (Euphausia superba) on growth and nutrient utilization of juvenile Atlantic cod (Gadus morhua) and Atlantic halibut (Hippoglossus hippoglossus) fed the same practical diets. Aquac Nutr 17:287–303CrossRefGoogle Scholar
  52. Tonheim SK, Nordgreen A, Høgøy I, Hamre K, Rønnestad I (2007) In vitro digestibility of water-soluble and water-insoluble protein fractions of some common fish larvae feeds and feed ingredients. Aquaculture 262:426–435CrossRefGoogle Scholar
  53. van der Meeren T, Olsen R, Hamre K, Fyhn H (2008) Biochemical composition of copepods for evaluation of feed quality in production of juvenile marine fish. Aquaculture 274:375–397CrossRefGoogle Scholar
  54. Venou B, Alexis MN, Fountoulaki E, Haralabous J (2009) Performance factors, body composition and digestion characteristics of gilthead sea bream (Sparus aurata) fed pelleted or extruded diets. Aquac Nutr 15:390–401CrossRefGoogle Scholar
  55. Watanabe T, Arakawa T, Kitajima C, Fujita S (1984a) Effect of nutritional quality of broodstock diets on reproduction of red sea bream. Nippon Suisan Gakkaishi 50:495–501CrossRefGoogle Scholar
  56. Watanabe T, Itoh A, Murakami A, Tsukashima Y, Kitajima C, Fujita S (1984b) Effect of nutritional quality of diets given to broodstock on the verge of spawning on reproduction of red sea bream. Nippon Suisan Gakkaishi 50:1023–1028CrossRefGoogle Scholar
  57. Wilson RP (1989) Amino acids and proteins. In: Halver JE (ed) Fish nutrition. Academic Press Inc., San Diego, pp 112–151Google Scholar
  58. Wu G (1998) Intestinal mucosal amino acid catabolism. J Nutr 128:1249–1252CrossRefPubMedGoogle Scholar
  59. Xu HG, Zhao M, Zheng KK, Wei YL, Yan L, Liang MQ (2017) Antarctic krill (Euphausia superba) meal in the diets improved the reproductive performance of tongue sole (Cynoglossus semilaevis) broodstock. Aquac Nutr 23:1287–1295CrossRefGoogle Scholar
  60. Yamamoto S, Sakamoto S, Takeuchi M (2002) Estimation of protein sources and effects of water-soluble nitrogen components in artificial diets on larval ayu. Nippon Suisan Gakkaishi 68:327–333 (in Japanese with English abstract) CrossRefGoogle Scholar
  61. Yoshitomi B, Aoki M, Oshima S, Hata K (2006) Evaluation of krill (Euphausia superba) meal as a partial replacement for fish meal in rainbow trout (Oncorhynchus mykiss) diets. Aquaculture 261:440–446CrossRefGoogle Scholar
  62. Zhou QC, Tan BP, Mai KS, Liu YJ (2004) Apparent digestibility of selected feed ingredients for juvenile cobia Rachycentron canadum. Aquaculture 241:441–451CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2018

Authors and Affiliations

  • Jeong-Hyeon Cho
    • 1
  • Yutaka Haga
    • 1
    Email author
  • Reiji Masuda
    • 2
  • Shuichi Satoh
    • 1
  1. 1.Graduate School of Marine Science and TechnologyTokyo University of Marine Science and TechnologyTokyoJapan
  2. 2.Maizuru Fisheries Research Station, Field Science Education and Research CenterKyoto UniversityMaizuruJapan

Personalised recommendations