Fish Physiology and Biochemistry

, Volume 43, Issue 6, pp 1629–1644 | Cite as

Dietary substitution of fishmeal by alternative protein with guanosine monophosphate supplementation influences growth, digestibility, blood chemistry profile, immunity, and stress resistance of red sea bream, Pagrus major



We determined the effects of complete fishmeal (FM) replacement by alternative protein (soy protein concentrate, SPC) with guanosine monophosphate (GMP) supplementation on growth, digestibility, immunity, blood chemistry profile, and stress resistance of juvenile red sea bream, Pagrus major. FM protein of a FM-based control diet (FM0) was replaced with 33.3 (FM33.3), 66.6 (FM66.7), and 100% (FM100) by SPC protein, and each replacement group was supplemented with 0.4% GMP to formulate four experimental diets. Each diet was randomly allocated to triplicate groups of fish (4.8 g) for 56 days. Results demonstrated that fish fed diet group FM33.3 had the significantly highest final weight, weight gain-specific growth rate, and feed intake. Meanwhile, in comparison to control, growth performance and feed utilization did not significantly differ with 66.7% FM replacement by SPC with GMP supplementation. Apparent digestibility coefficient of protein and lipid also followed a similar trend. All growth, feed utilization, and digestibility parameters were significantly lower in FM100 diet group. Blood urea nitrogen (BUN) and triglycerides (TG) increased (P < 0.05) with increasing FM replacement level by SPC. Interestingly, total cholesterol level reduces with the increasing level of FM replacement by SPC with GMP supplementation. Fish fed FM0 diet group showed the best condition of both oxidative and freshwater stress resistance. Meanwhile, FM33.3 and FM66.7 diet groups showed acceptable conditions. Innate immune responses enhanced with the increasing FM replacement level by SPC with GMP supplementation. In conclusion, FM could be replaced ≤66.7% by SPC with GMP supplementation in diets for red sea bream without any adverse effects on fish performances.


Guanosine monophosphate Alternative protein Growth Immune responses Stress resistance Pagrus major 



The first author would like to thank the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MONBUKAGAKUSHO) for supporting this research work. The research was partially funded by the Management Expenses Grants of the United Graduate School of Agricultural Sciences, Kagoshima University, provided to Dr. Shunsuke Koshio.


  1. Afuang W, Siddhuraju P, Becker K (2003) Comparative nutritional evaluation of raw, methanol extracted residues and methanol extracts of moringa (Moringa oleifera Lam.) leaves on growth performance and feed utilization in Nile tilapia (Oreochromis niloticus L.) Aquac Res 34:1147–1159CrossRefGoogle Scholar
  2. Anderson DP, Siwicki AK (1995) Basic hematology and serology for fish health programs. In: Shariff M, Arthur JR, Subasinghe RP (eds) Diseases in Asian aquaculture II. Philippines, Fish Health Section, Asian Fisheries Society, Manila, pp 185–202Google Scholar
  3. AOAC (1990) Official methods of analysis of the Association of Official Analytical Chemists, 15th edn. Association of Official Analytical Chemists, ArlingtonGoogle Scholar
  4. Aragão C, Conceicção LEC, Dias J, Marques AC, Gomes E, Dinis MT (2003) Soy protein concentrate as a protein source for Senegalese sole (Solea senegalensis Kaup 1858) diets: effects on growth and amino acid metabolism of postlarvae. Aquac Res 34:1443–1452CrossRefGoogle Scholar
  5. Berge GM, Grisdale-Helland B, Helland SJ (1999) Soy protein concentrate in diets for Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 178:139–148CrossRefGoogle Scholar
  6. Bjerkeng B, Refstie S, Fjalestad KT, Storebakken T, Rodbotten M, Roem AJ (1997) Quality parameters of the flesh of Atlantic salmon (Salmo salar) as affected by dietary fat content and full-fat soy bean meal as a partial substitute for fish meal in the diet. Aquaculture 157:297–309CrossRefGoogle Scholar
  7. Burrells C, Williams PD, Southgate PJ, Crampton VO (1999) Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet Immunol Immunopathol 72:277–288CrossRefPubMedGoogle Scholar
  8. Carroll KK, Hamilton RMG (1975) Effects of dietary protein and carbohydrate on plasma cholesterol levels in relation to atherosclerosis. J Food Sci 40:18–23CrossRefGoogle Scholar
  9. Carter CG, Sajjadi M (2011) Low fish meal diets for Atlantic salmon, Salmo salar L., using soy protein concentrate treated with graded levels of phytase. Aquacult Int 19:431–444CrossRefGoogle Scholar
  10. Carver JD, Walker WA (1995) The role of nucleotides in human nutrition. Nutr Biochem 6:58–72CrossRefGoogle Scholar
  11. Celi P, Sullivan M, Evans D (2010) The stability of the reactive oxygen metabolites (d-ROMs) and biological antioxidant potential (BAP) tests on stored horse blood. Vet J 183:217–218CrossRefPubMedGoogle Scholar
  12. Chen W, Ai QH, Mai KS, Xu W, Liufu ZG, Zhang WB, Cai YH (2011) Effects of dietary soybean saponins on feed intake, growth performance, digestibility and intestinal structure in juvenile Japanese flounder (Paralichthys olivaceus). Aquaculture 318:95–100CrossRefGoogle Scholar
  13. Cheng ZJ, Hardy RW (2004) Protein and lipid sources affect cholesterol concentrations of juvenile Pacific white shrimp, Litopenaeus vannamei (Boone). J Anim Sci 82:1136–1145CrossRefPubMedGoogle Scholar
  14. Cheng ZJ, Hardy RW, Verlhac V, Gabaudan J (2004) Effects of microbial phytase supplementation and dosage on apparent digestibility coefficients of nutrients and dry matter in soybean product-based diets for rainbow trout Oncorhynchus mykiss. J World Aquac Soc 35:1–15CrossRefGoogle Scholar
  15. Chou RL, Her BY, Su MS, Hwang G, Wu YH, Chen HY (2004) Substituting fishmeal with soybean meal in diets of juvenile cobia (Rachycentron canadum). Aquaculture 229:325–333CrossRefGoogle Scholar
  16. Colburn HR, Walker AB, Breton T, Stilwell JM, Sidor IF, Gannam AL, Berlinsky DL (2012) Partial replacement of fishmeal with soybean meal and soy protein concentrate in diets of Atlantic Cod. N Am J Aquac 74:330–337CrossRefGoogle Scholar
  17. Davis DA, Jirsa D, Arnold CR (1995) Evaluation of soybean proteins as replacements for menhaden fish meal in practical diets for red drum (Sciaenops ocellatus). J World Aquac Soc 26:48–58CrossRefGoogle Scholar
  18. Day OJ, Plascencia-Gonzalez HG (2000) Soybean protein concentrate as a protein source for turbot (Scophthalmus maximus L.) Aquac Nut 6:221–228CrossRefGoogle Scholar
  19. Deng JM, Mai KS, Ai QH, Zhang WB, Wang XJ, Xu W, Liufu ZG (2006) Effects of replacing fish meal with soy protein concentrate on feed intake and growth of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture 258:503–513CrossRefGoogle Scholar
  20. Dias J (1999) Lipid deposition in rainbow trout, Oncorhynchus mykiss and European seabass, Dicentrarchus labrax L.: nutritional regulation of hepatic lipogenesis. PhD thesis, Univ. Porto (Portugal) and Univ. Bordeaux I (France), pp. 190Google Scholar
  21. Drew MD, Borgeson TL, Thiessen DL (2007) A review of processing of feed ingredients to enhance diet digestibility in finfish. Anim Feed Sci Tech 138:118–136CrossRefGoogle Scholar
  22. Fletcher TC (1997) Dietary effects on stress and health. In: Iwama GK, Pickering AD, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 223–244Google Scholar
  23. 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
  24. Freitas LEL, Nunes AJP, Sa MVC (2011) Growth and feeding responses of the mutton snapper, Lutjanus analis (Cuvier 1828), fed on diets with soy protein concentrate in replacement of Anchovy fish meal. Aquac Res 42:866–877CrossRefGoogle Scholar
  25. Furukawa A, Tsukahara H (1966) On the acid digestion method for the determination of chromic oxides as an index substance in the study of digestion of fish feed. Nippon Suisan Gakkaishi 32:502–506CrossRefGoogle Scholar
  26. Gabrielsen BO, Austreng E (1998) Growth, product quality and immune status of Atlantic salmon, Salmo salar L., fed wet feed with alginate. Aquac Res 29:397–401CrossRefGoogle Scholar
  27. Gatlin DM III, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, 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
  28. Goth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–152CrossRefPubMedGoogle Scholar
  29. Hagemeister H, Scholz-Ahrens KE, Schulte-Coerne H, Barth CA (1990) Plasma amino acids and cholesterol following consumption of dietary casein or soy protein in minipigs. J Nutr 120(11):1305–1311PubMedGoogle Scholar
  30. Hernández PV, Olvera-Novoa MA, Rouse DB (2004) Effect of dietary cholesterol on growth and survival of juvenile redclaw crayfish Cherax quadricarinatus under laboratory conditions. Aquaculture 236:405–411CrossRefGoogle Scholar
  31. Hernández MD, Martínez FJ, Jover M, García GB (2007) Effects of partial replacement of fish meal by soybean meal in sharpsnout seabream (Diplodus puntazzo) diet. Aquaculture 263:159–167CrossRefGoogle Scholar
  32. Holme MH, Zeng C, Southgate PC (2006) The effects of supplemental dietary cholesterol on growth, development and survival of mud crab, Scylla serrata, megalopa fed semi-purified diets. Aquaculture 261:1328–1334CrossRefGoogle Scholar
  33. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM (2016a) Effects of dietary administration of guanosine monophosphate on the growth, digestibility, innate immune responses and stress resistance of juvenile red sea bream, Pagrus major. Fish and shellfish Immunol 57:96–106CrossRefGoogle Scholar
  34. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM (2016b) Dietary nucleotide administration influences growth, immune responses and oxidative stress resistance of juvenile red sea bream (Pagrus major). Aquaculture 455:41–49CrossRefGoogle Scholar
  35. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Ono S, Fujieda T (2016c) Comparison of the effects of inosine and inosine monophosphate on growth, immune response, stress resistance and gut morphology of juvenile red sea bream, Pagrus major. Aquaculture 458:64–74CrossRefGoogle Scholar
  36. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM (2016d) Dietary effects of adenosine monophosphate to enhance growth, digestibility, innate immune responses and stress resistance of juvenile red sea bream, Pagrus major. Fish and shellfish Immunol 56:523–533CrossRefGoogle Scholar
  37. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Maekawa M, Fujieda T (2017a) Effects of dietary administration of inosine on growth, immune response, oxidative stress and gut morphology of juvenile amberjack Seriola dumerili. Aquaculture 468:534–544CrossRefGoogle Scholar
  38. Hossain MS, Kader MA, Dey T, Sony NM, Bulbul M, Koshio S (2017b) Effect of high inclusion of rendered animal by-product ingredients on growth, digestibility and economic performances in climbing perch Anabas testudineus. Aquac Res 48:931–940CrossRefGoogle Scholar
  39. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Fujieda T (2017c) Nucleoside by-product dietary supplementation influences blood chemistry, immune response, oxidative stress resistance and intestinal morphology of juvenile amberjack, Seriola dumerili. Aquac Nutr: 1–11. doi: 10.1111/anu.12514
  40. 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
  41. Ikeda I, Hosokawa H, Shimeno S, Takeda M (1991) Feeding stimulant activity of nucleotides, tryptophan, and their related compounds of jack mackerel. Nippon Suisan Gakkaishi 57(42):1539–1515CrossRefGoogle Scholar
  42. Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M (2010) Supplemental effects of some crude ingredients in improving nutritive values of low fishmeal diets for red sea bream, Pagrus major. Aquaculture 308:136–144CrossRefGoogle Scholar
  43. Kader MA, Bulbul M, Koshio S, Ishikawa M, Yokoyama S, Nguyen BT, Komilus CF (2012) Effect of complete replacement of fishmeal by dehulled soybean meal with crude attractants supplementation in diets for red sea bream, Pagrus major. Aquaculture 350–353:109–116CrossRefGoogle Scholar
  44. Kaushik SJ, Cravedi JP, Lalles JP, Sumpter J, Fauconneau B, Laroche M (1995) Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture 133:257–274CrossRefGoogle Scholar
  45. Kaushik SJ, Covès D, Dutto G, Blanc D (2004) Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the European seabass, Dicentrarchus labrax. Aquaculture 230:391–404CrossRefGoogle Scholar
  46. Kim JD, Kaushik SJ, Breque J (1998) Nitrogen and phosphorus utilization in rainbow trout, Oncorhynchus mykiss fed diets with or without fish meal. Aquacult Living Res 11:261–264CrossRefGoogle Scholar
  47. Kiron V, Puangkaew J, Ishizaka K, Satoh S, Watanabe T (2004) Antioxidant status and nonspecific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of vitamin E along with three lipid sources. Aquaculture 234:361–379CrossRefGoogle Scholar
  48. Kissil GW, Lupatsch I, Higgs DA, Hardy RW (2000) Dietary substitution of soy and rapeseed protein concentrates for fish meal, and their effects on growth and nutrient utilization in gilthead seabream Sparus aurata L. Aquac Res 31:595–601CrossRefGoogle Scholar
  49. Kofuji PYM, Hosokawa H, Masumoto T (2006) Effects of dietary supplementation with feeding stimulants on yellowtail Seriola quinqueradiata (Temminck & Schlegel; Carangidae) protein digestion at low water temperatures. Aquac Res 37:366–373CrossRefGoogle Scholar
  50. Krogdahl A, Bakke-Mckellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.) Aquac Nutr 9:361–371CrossRefGoogle Scholar
  51. Kubilay A, Ulukoy G (2002) The effects of acute stress on rainbow trout (Oncorhynchus mykiss). Turk J Zool 26(2):249–254Google Scholar
  52. Lanari D, Agaro E, Turri C (1998) Use of nonlinear regression to evaluate the effects of phytase enzyme treatment of plant protein diets for rainbow trout, Oncorhynchus mykiss. Aquaculture 161:345–356CrossRefGoogle Scholar
  53. Lemaire P, Drai P, Mathieu A, Lemaire S, Carriere S, Giudicelli J, Lafaurie M (1991) Changes with different diets in plasma enzymes (GOT, GPT, LDH, ALP) and plasma lipids (cholesterol, triglycerides) of sea bass (Dicentrarchus labrax). Aquaculture 93:63–75CrossRefGoogle Scholar
  54. Li P, Gatlin DM (2006) Nucleotide nutrition in fish: current knowledge and future applications. Aquaculture 251:141–152CrossRefGoogle Scholar
  55. Li Y, Ai QH, Mai KS, Cheng ZY (2011) Effects of the partial substitution of dietary fishmeal by two types of soybean meals on the growth performance of juvenile Japanese seabass, Lateolabrax japonicus (Cuvier 1828). Aquac Res 1–9. doi: 10.1111/j.1365-2109.2011.02849.x
  56. Lin YH, Wang H, Shiau SY (2009) Dietary nucleotide supplementation enhances growth and immune responses of grouper (Epinephelus malabaricus). Aquac Nutr 15:117–122CrossRefGoogle Scholar
  57. Lygren B, Sveier H, Hjeltnes B, Waagbo R (1999) Examination of the immunomodulatory properties and the effect on disease resistance of dietary bovine lactoferrin and vitamin C fed to Atlantic salmon (Salmo salar) for a short-term period. Fish Shellfish Immunol 9:95–107CrossRefGoogle Scholar
  58. Mambrini M, Roem AJ, Cravedi JP, Lalles JP, Kaushik SJ (1999) Effects of replacing fish meal with soy protein concentrate and of DL-methionine supplementation in high energy, extruded diets on the growth and nutrient utilization of rainbow trout, Oncorhynchus mykiss. J Anim Sci 77:2990–2999CrossRefPubMedGoogle Scholar
  59. Martinez-Alvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15(1–2):75–88CrossRefGoogle Scholar
  60. Meilahn CW, Davis DA, Arnold CR (1996) Effects of commercial fish meal analog and menhaden fish meal on growth of red drum fed isonitrogenous diets. Progres Fish-Cult 58:111–116CrossRefGoogle Scholar
  61. Morganti P, Bruno C, Guarneri F, Cardillo A, Del Ciotto P, Valenzano F (2002) Role of topical and nutritional supplement to modify the oxidative stress. Int J Cosmet Sci 24(6):331–339CrossRefPubMedGoogle Scholar
  62. Ngandzali BO, Zhou F, Xiong W, Shao QJ, Xu JZ (2011) Effect of dietary replacement of fish meal by soybean protein concentrate on growth performance and phosphorus discharging of juvenile black sea bream, Acanthopagrus schlegelii. Aquac Nutr 17:526–535CrossRefGoogle Scholar
  63. Papatryphon E, Soares JH Jr (2000) The effect of dietary feeding stimulants on growth performance of striped bass, Morone saxatilis, fed-a-plant feedstuff-based diet. Aquaculture 185:329–338CrossRefGoogle Scholar
  64. Peng M, Xu W, Ai Q, Mai K, Liufu Z, Zhang K (2013) Effects of nucleotide supplementation on growth, immune responses and intestinal morphology in juvenile turbot fed diets with graded levels of soybean meal (Scophthalmus maximus L.) Aquaculture 392–395:51–58CrossRefGoogle Scholar
  65. Reigh RC, Ellis SC (1992) Effects of dietary soybean and fish-protein ratios on growth and body composition of red drum (Sciaenops ocellatus) fed isonitrogenous diets. Aquaculture 104:279–292CrossRefGoogle Scholar
  66. Rumsey GL, Siwicki AK, Anderson DP, Bowser PR (1994) Effect of soybean protein on serological response, nonspecific defense-mechanisms, growth, and protein-utilization in rainbow-trout. Vet Immunol Immunopathol 41:323–339CrossRefPubMedGoogle Scholar
  67. Sagstad A, Sanden M, Krogdahl Å, Bakke-Mckellep AM, Frøystad M, Hemre GI (2008) Organs development, gene expression and health of Atlantic salmon (Salmo salar L.) fed genetically modified soybeans compared to the near-isogenic nonmodified parental line. Aquac Nutr 14:556–572CrossRefGoogle Scholar
  68. Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A, Furones D, Cuesta A, Meseguer J, Esteban MA (2008) Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.) Fish Shellfish Immunol 25:114–123CrossRefPubMedGoogle Scholar
  69. Salze G, McLean E, Battle PR, Schwarz MH, Craig SR (2010) Use of soy protein concentrate and novel ingredients in the total elimination of fish meal and fish oil in diets for juvenile cobia, Rachycentron canadum. Aquaculture 298:294–299CrossRefGoogle Scholar
  70. Sato N, Murakami Y, Nakano T, Sugawara M, Kawakami H, Idota T, Nakajima I (1995) Effects of dietary nucleotides on lipid metabolism and learning ability of rats. Biosci Biotechnol Biochem 59(7):1267–1271CrossRefPubMedGoogle Scholar
  71. Storebakken T, Shearer KD, Roem AJ (1998) Availability of protein, phosphorus and other elements in fish meal, soy-protein concentrate and phytase-treated soy-protein-concentrate-based diets to Atlantic salmon, Salmo salar. Aquaculture 161:365–379CrossRefGoogle Scholar
  72. Storebakken T, Refstie S, Ruyter B (2000) Soy products as fat and protein sources in fish feeds for intensive aquaculture. In: Drackley JK (ed) Soy in animal nutrition. Federation of Animal Science Societies, Savoy IL, USA, pp 127–170Google Scholar
  73. Swain P, Dash S, Sahoo P, Routray P, Sahoo S, Gupta SD, Meher PK, Sarangi N (2007) Non-specific immune parameters of brood Indian major carp Labeo rohita and their seasonal variations. Fish Shellfish Immunol 22:38–43CrossRefPubMedGoogle Scholar
  74. Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158CrossRefGoogle Scholar
  75. Takagi S, Hosokawa H, Shimeno S, Maita M, Ukawa M, Ueno S (1999) Utilization of soy protein concentrate in a diet for red sea bream, Pagrus major. Suisanzoshoku 47:77–87Google Scholar
  76. Takagi S, Shimeno S, Hosokawa H, Ukawa M (2001) Effect of lysine and methionine supplementation to a soy protein concentrate diet for red sea bream, Pagrus major. Fish Sci 67:1088–1096CrossRefGoogle Scholar
  77. Takii K, Shimeno S, Takeda M, Kamekawa S (1986) The effects of feeding stimulants in diet on digestive enzyme activities of eel. Bull Jpn Soc Sci Fish 52:1449–1454CrossRefGoogle Scholar
  78. Takii K, Shimeno S, Akutsu M, Takeda M (1990) Dietary supplement of feeding stimulants on performance and digestive function of yellowtail, Seriola quinqueradiata. Bull Fish Lab, Kinki Univ 4:127–137Google Scholar
  79. Vielma J, Lall SP, Koskela J, Schoner FJ, Mattila P (1998) Effects of dietary phytase and cholecalciferol on phosphorus bioavailability in rainbow trout (Oncorhynchus mykiss). Aquaculture 163:309–323CrossRefGoogle Scholar
  80. Vielma J, Makinen T, Ekholm P, Koskela J (2000) Influence of dietary soy and phytase levels on performance and body composition of large rainbow trout (Oncorhynchus mykiss) and algal availability of phosphorus load. Aquaculture 183:349–362Google Scholar
  81. Waagbø R (1994) The impact of nutritional factors on the immune system in Atlantic salmon, Salmo salar L.: a review. Aquacult Fish Manag 25:175–197Google Scholar
  82. Walker AB, Sidor IF, O’Keefe T, Cremer M, Berlinsky DL (2010) Partial replacement of fish meal with soy protein concentrate in diets of Atlantic cod. N Am J Aquac 72:343–353CrossRefGoogle Scholar
  83. Wu Y, Han H, Qin J, Wang Y (2015) Replacement of fishmeal by soya protein concentrate with taurine supplementation in diets for golden pompano (Trachinotus ovatus). Aquacult Nutri 21:214–222CrossRefGoogle Scholar
  84. Yokoyama S, Koshio S, Takakura N, Oshida K, Ishikawa M, Gallardo-Cigarroa FJ, Teshima S (2005) Dietary bovine lactoferrin enhances tolerance to high temperature stress in Japanese flounder Paralichthys olivaceus. Aquaculture 249:367–373CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Laboratory of Aquatic Animal Nutrition, Faculty of FisheriesKagoshima UniversityKagoshimaJapan
  2. 2.The United Graduate School of Agricultural SciencesKagoshima UniversityKagoshimaJapan
  3. 3.Department of Aquaculture, Faculty of FisheriesSylhet Agricultural UniversitySylhetBangladesh

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