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Evaluation of shrimp protein hydrolysate and krill meal supplementation in low fish meal diet for red seabream (Pagrus major)

  • Gunathilaka, Buddhi E. (Department of Marine Life Sciences, Jeju National University) ;
  • Khosravi, Sanaz (Department of Marine Bioscience and Technology, Gangneung-Wonju National University) ;
  • Shin, Jaebeom (Department of Marine Life Sciences, Jeju National University) ;
  • Shin, Jaehyeong (Department of Marine Life Sciences, Jeju National University) ;
  • Herault, Mikael (Research & Development Aqua Platform, AQUATIV Corporation, ZA du Gohelis) ;
  • Fournier, Vincent (Research & Development Aqua Platform, AQUATIV Corporation, ZA du Gohelis) ;
  • Lee, Kyeong-Jun (Department of Marine Life Sciences, Jeju National University)
  • Received : 2020.11.28
  • Accepted : 2021.02.15
  • Published : 2021.03.31

Abstract

Protein hydrolysates and krill meal (KM) are used as protein sources in aquafeeds. The study was conducted to examine the supplemental effects of shrimp protein hydrolysates (SH) or KM in a high-plant-protein diet for red seabream (Pagrus major). A fish meal (FM)-based diet (40%) was considered as the high-FM diet (HFM) and a diet containing 25% FM and soy protein concentrate, in the expense of FM protein from HFM diet, was considered as the low fish meal (LFM) diet. Two other experimental diets (SH and KM) were prepared by including SH and KM into LFM diet at 5% inclusion levels in exchange of 5% FM from the LFM diet. A feeding trial was conducted for fifteen weeks using triplicate group of fish (Initial mean body weight, 8.47 ± 0.05 g) for a diet. Growth performance and feed efficiency of fish were significantly enhanced by HFM, KM and SH supplemented diets over those of fish fed LFM diet. Interestingly, these parameters of fish fed SH diet showed better performance than KM and HFM groups. Liver IGF-I expression of fish fed SH diet was comparable to HFM group and higher than KM and LFM diets. Protein digestibility of SH diet was significantly higher than KM, HFM, and LFM diets. Dry matter digestibility of SH diet was comparable to HFM diet and significantly higher than KM and LFM diets. Nitro blue tetrazolium and superoxide dismutase activities of HFM, SH and KM groups were significantly elevated than the LFM group and SH diet increased catalase and glutathione peroxidase activities of fish compared to KM and LFM groups. Hemoglobin level and hematocrit of fish fed SH and KM diets were significantly higher than LFM group. A diet containing 20% FM with KM is comparable to a HFM diet which contains 40% FM for red seabream. SH can be used to replace FM from red seabream diet down to 20% and fish performance can be improved better than a diet containing 40% FM. Overall, it seems that SH is more effective ingredient in red seabream diet compared to KM.

Keywords

Acknowledgement

This study was supported by AQUATIV (Aquaculture Division of DIANA, Member of SYMRISE Group), Elven, France and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A03033553).

References

  1. Anderson DP, Siwicki AK. Basic hematology and serology for fish health programs. In: Shariff M, Arthur JR, Subasinghe RP, editors. Diseases in Asian aquaculture II. Selangor, Malaysia: Fish Health Section, Asian Fisheries Society; 1995. p. 185-202.
  2. AOAC [Association of Official Analytical Chemists] International. Official methods of analysis of AOAC International. 18th ed. Gaithersburg, MD: AOAC International; 2005.
  3. Biswas AK, Seoka M, Inoue Y, Takii K, Kumai H. Photoperiod influences the growth, food intake, feed efficiency and digestibility of red sea bream (Pagrus major). Aquaculture. 2005;250:666-73. https://doi.org/10.1016/j.aquaculture.2005.04.047
  4. Biswas AK, Seoka M, Takii K, Kumai H. Comparison of apparent digestibility coefficient among replicates and different stocking density in red sea bream Pagrus major. Fish Sci. 2007;73:19-26. https://doi.org/10.1111/j.1444-2906.2007.01297.x
  5. Bjorndal B, Vik R, Brattelid T, Vigerust NF, Burri L, Bohov P, et al. Krill powder increases liver lipid catabolism and reduces glucose mobilization in tumor necrosis factor-alpha transgenic mice fed a high-fat diet. Metabolism. 2012;61:1461-72. https://doi.org/10.1016/j.metabol.2012.03.012
  6. Brown BA. Routine hematology procedures. In: Brown BA, editor. Hematology, principles and procedures. Philadelphia, PA: Leo and Febiger; 1980. p. 71-112.
  7. Bueno-Solano C, Lopez-Cervantes J, Campas-Baypoli ON, Lauterio-Garcia R, Adan-Bante NP, Sanchez-Machado DI. Chemical and biological characteristics of protein hydrolysates from fermented shrimp by-products. Food Chem. 2009;112:671-75. https://doi.org/10.1016/j.foodchem.2008.06.029
  8. Bui HTD, Khosravi S, Fournier V, Herault M, Lee KJ. Growth performance, feed utilization, innate immunity, digestibility and disease resistance of juvenile red seabream (Pagrus major) fed diets supplemented with protein hydrolysates. Aquaculture. 2014;418-419:11-16. https://doi.org/10.1016/j.aquaculture.2013.09.046
  9. Cahu TB, Santos SD, Mendes A, Cordula CR, Chavante SF, Carvalho LB, et al. Recovery of protein, chitin, carotenoids and glycosaminoglycans from Pacific white shrimp (Litopenaeus vannamei) processing waste. Process Biochem. 2012;47:570-77. https://doi.org/10.1016/j.procbio.2011.12.012
  10. Cederlund A, Gudmundsson GH, Agerberth B. Antimicrobial peptides important in innate immunity. FEBS J. 2011;278:3942-51 https://doi.org/10.1111/j.1742-4658.2011.08302.x
  11. Chalamaiah M, Dinesh Kumar B, Hemalatha R, Jyothirmayi T. Fish protein hydrolysates: proximate composition, amino acid composition, antioxidant activities and applications: a review. Food Chem. 2012;135:3020-38. https://doi.org/10.1016/j.foodchem.2012.06.100
  12. Chalamaiah M, Hemalatha R, Jyothirmayi T, Diwan PV, Bhaskarachary K, Vajreswari A, et al. Chemical composition and immunomodulatory effects of enzymatic protein hydrolysates from common carp (Cyprinus carpio) egg. Nutrition. 2015;31:388-98. https://doi.org/10.1016/j.nut.2014.08.006
  13. Chalamaiah M, Yu W, Wu J. Immunomodulatory and anticancer protein hydrolysates (peptides) from food proteins: a review. Food Chem. 2018;245:205-22. https://doi.org/10.1016/j.foodchem.2017.10.087
  14. Cheng CH, Guo ZX, Ye CX, Wang AL. Effect of dietary astaxanthin on the growth performance, non-specific immunity, and antioxidant capacity of pufferfish (Takifugu obscurus) under high temperature stress. Fish Physiol. Biochem. 2018;44:209-18. https://doi.org/10.1007/s10695-017-0425-5
  15. Chiou PP, Khoo J, Bols NC, Douglas S, Chen TT. Effects of linear cationic α-helical antimicrobial peptides on immune-relevant genes in trout macrophages. Dev Comp Immunol. 2006;30:797-806. https://doi.org/10.1016/j.dci.2005.10.011
  16. Cho JH, Haga Y, Masuda R, Satoh S. 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. Fish Sci. 2018;84:699-713. https://doi.org/10.1007/s12562-018-1205-6
  17. de Cruz CR, Yamamoto FY, Ju M, Chen K, Velasquez A, Gatlin DM. Efficacy of purified nucleotide supplements on the growth performance and immunity of hybrid striped bass Morone chrysops × Morone saxatilis. Fish Shellfish Immunol. 2020;98:868-74. https://doi.org/10.1016/j.fsi.2019.11.046
  18. Divakaran S, Obaldo LG, Forster IP. Note on the methods for determination of chromic oxide in shrimp feeds. J Agric Food Chem. 2002;50:464-67. https://doi.org/10.1021/jf011112s
  19. Dong S, Zeng M, Wang D, Liu Z, Zhao Y, Yang H. Antioxidant and biochemical properties of protein hydrolysates prepared from Silver carp (Hypophthalmichthys molitrix). Food Chem. 2008;107:1485-93. https://doi.org/10.1016/j.foodchem.2007.10.011
  20. Dossou S, Koshio S, Ishikawa M, Yokoyama S, Dawood MAO, El Basuini MF, et al. Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji). Fish Shellfish Immunol. 2018;75:253-62. https://doi.org/10.1016/j.fsi.2018.01.032
  21. Escobar S, Fuentes EN, Poblete E, Valdes JA, Safian D, Reyes AE, et al. Molecular cloning of IGF-1 and IGF-1 receptor and their expression pattern in the Chilean flounder (Paralichthys adspersus). Comp Biochem Physiol B Biochem Mol Biol. 2011;159:140-147. https://doi.org/10.1016/j.cbpb.2011.03.003
  22. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509. https://doi.org/10.1016/S0021-9258(18)64849-5
  23. Gaber MMA. The effect of different levels of krill meal supplementation of soybean-based diets on feed intake, digestibility, and chemical composition of Juvenile Nile tilapia Oreochromis niloticus, L. J World Aquac Soc. 2007;36:346-53. https://doi.org/10.1111/j.1749-7345.2005.tb00338.x
  24. Goto T, Takagi S, Ichiki T, Sakai T, Endo M, Yoshida T, et al. Studies on the green liver in cultured red sea bream fed low level and non-fish meal diets: relationship between hepatic taurine and biliverdin levels. Fish Sci. 2001;67:58-63. https://doi.org/10.1046/j.1444-2906.2001.00199.x
  25. Gunathilaka BE, Khosravi S, Herault M, Fournier V, Lee C, Jeong JB. Evaluation of shrimp or tilapia protein hydrolysate at graded dosages in low fish meal diet for olive flounder (Paralichthys olivaceus). Aquac Nutr. 2020;26:1592-603. https://doi.org/10.1111/anu.13105
  26. Haghbayan S, Shamsaie Mehrgan M. The effect of replacing fish meal in the diet with enzyme-treated soybean meal (HP310) on growth and body composition of rainbow trout fry. Molecules. 2015;20:21058-66. https://doi.org/10.3390/molecules201219751
  27. Hansen JO, Penn M, Overland M, Shearer KD, Krogdahl A, Mydland LT, et al. High inclusion of partially deshelled and whole krill meals in diets for Atlantic salmon (Salmo salar). Aquaculture. 2010;310:164-72. https://doi.org/10.1016/j.aquaculture.2010.10.003
  28. Hardy RW. Alternative marine sources of fish feed and farmed fish quality. In: Lie O, editor. Improving farmed fish quality and safety. Cambridge, MA: Woodhead; 2008. p. 328-42.
  29. Harris J, Bird DJ. Modulation of the fish immune system by hormones. Vet Immunol Immunopathol. 2000;77:163-76. https://doi.org/10.1016/S0165-2427(00)00235-X
  30. Hatlen B, Berge K, Nordrum S, Johnsen K, Kolstad K, Morkore T. The effect of low inclusion levels of Antarctic krill (Euphausia superba) meal on growth performance, apparent digestibility and slaughter quality of Atlantic salmon (Salmo salar). Aquac Nutr. 2017;23:721-9. https://doi.org/10.1111/anu.12439
  31. Hermannsdottir R, Johannsdottir J, Smaradottir H, Sigurgisladottir S, Gudmundsdottir BK, Bjornsdottir R. Analysis of effects induced by a pollock protein hydrolysate on early development, innate immunity and the bacterial community structure of first feeding of Atlantic halibut (Hippoglossus hippoglossus L.) larvae. Fish Shellfish Immunol. 2009;27:595-602. https://doi.org/10.1016/j.fsi.2009.05.007
  32. Heu MS, Kim JS, Shahidi F. Components and nutritional quality of shrimp processing by-products. Food Chem. 2003;82:235-42. https://doi.org/10.1016/S0308-8146(02)00519-8
  33. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Dawood MAO. Efficacy of nucleotide related products on growth, blood chemistry, oxidative stress and growth factor gene expression of juvenile red sea bream, Pagrus major. Aquaculture. 2016;464:8-16. https://doi.org/10.1016/j.aquaculture.2016.06.004
  34. Huang D, Yang L, Wang C, Ma S, Cui L, Huang S, et al. Immunostimulatory activity of protein hydrolysate from oviductus ranae on macrophage in vitro. Evid-Based Complement Alternat Med. 2014;1-11.
  35. Huang GR, Zhao J, Jiang JX. Effect of defatting and enzyme type on antioxidative activity of shrimp processing byproducts hydrolysate. Food Sci Biotechnol. 2011;20:651-7. https://doi.org/10.1007/s10068-011-0092-8
  36. Kader MA, Bulbul M, Koshio S, Ishikawa M, Yokoyama S, Nguyen BT, et al. Effect of complete replacement of fishmeal by dehulled soybean meal with crude attractants supplementation in diets for red sea bream, Pagrus major. Aquaculture. 2012;350:109-16. https://doi.org/10.1016/j.aquaculture.2012.04.009
  37. Kader MA, Koshio S. Effect of composite mixture of seafood by-products and soybean proteins in replacement of fishmeal on the performance of red sea bream, Pagrus major. Aquaculture. 2012;368:95-102. https://doi.org/10.1016/j.aquaculture.2012.09.014
  38. Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M. Supplemental effects of some crude ingredients in improving nutritive values of low fishmeal diets for red sea bream, Pagrus major. Aquaculture. 2010;308:136-44. https://doi.org/10.1016/j.aquaculture.2010.07.037
  39. Kalinowski CT, Robaina LE, Izquierdo MS. Effect of dietary astaxanthin on the growth performance, lipid composition and post-mortem skin colouration of red porgy Pagrus pagrus. Aquac Int. 2011;19:811-23. https://doi.org/10.1007/s10499-010-9401-0
  40. Karnjanapratum S, O'Callaghan YC, Benjakul S, O'Brien N. Antioxidant, immunomodulatory and antiproliferative effects of gelatin hydrolysate from unicorn leatherjacket skin. J Sci Food Agric. 2016;96:3220-6. https://doi.org/10.1002/jsfa.7504
  41. Khosravi S, Bui HTD, Herault M, Fournier V, Kim KD, Lee BJ, et al. Supplementation of protein hydrolysates to a low-fishmeal diet improves growth and health status of juvenile olive flounder, Paralichthys olivaceus. J World Aquac Soc. 2018;49:897-911. https://doi.org/10.1111/jwas.12436
  42. Khosravi S, Bui HTD, Rahimnejad S, Herault M, Fournier V, Jeong JB. Effect of dietary hydrolysate supplementation on growth performance, non-specific immune response and disease resistance of olive flounder (Paralichthys olivaceus) challenged with Edwardsiella tarda. Aquac Nutr. 2015b;21:321-31. https://doi.org/10.1111/anu.12157
  43. Khosravi S, Rahimnejad S, Herault M, Fournier V, Lee CR, Bui HTD, et al. Effects of protein hydrolysates supplementation in low fish meal diets on growth performance, innate immunity and disease resistance of red sea bream Pagrus major. Fish Shellfish Immunol. 2015a;45:858-68. https://doi.org/10.1016/j.fsi.2015.05.039
  44. Kim DH, Lipton D, Choi JY. Analyzing the economic performance of the red sea bream Pagrus major offshore aquaculture production system in Korea. Fish Sci. 2012;78:1337-42. https://doi.org/10.1007/s12562-012-0540-2
  45. Kleekayai T, Harnedy PA, O'Keeffe MB, Poyarkov AA, CunhaNeves A, Suntornsuk W. Extraction of antioxidant and ACE inhibitory peptides from Thai traditional fermented shrimp pastes. Food Chem. 2015;176:441-7. https://doi.org/10.1016/j.foodchem.2014.12.026
  46. Kondo F, Ohta T, Iwai T, Ido A, Miura C, Miura T. Effect of the squid viscera hydrolysate on growth performance and digestion in the red sea bream Pagrus major. Fish Physiol Biochem. 2017;43:1543-55. https://doi.org/10.1007/s10695-017-0391-y
  47. Koshio S. Red sea bream, Pagrus major. In: Webster CD, Lim CE, editors. Nutrient requirements and feeding of finfish for aquaculture. New York, NY: CABI; 2002. p. 51-63.
  48. KOSTAT [Statistics Korea]. Preliminary results of the survey on the status of fish culture in 2016 [Internet]. 2017 [cited 2020 Mar 26]. http://kostat.go.kr/assist/synap/preview/skin/doc.html?fn=synapview360318_1&rs=/assist/synap/preview
  49. Laron Z. Insulin-like growth factor 1 (IGF-1): a growth hormone. J Clin Pathol Mol Pathol. 2001;54:311-6. https://doi.org/10.1136/mp.54.5.311
  50. Leal ALG, de Castro PF, de Lima JPV, de Souza Correia E, de Souza Bezerra R. Use of shrimp protein hydrolysate in Nile tilapia (Oreochromis niloticus, L.) feeds. Aquac Int. 2010;18:635-46. https://doi.org/10.1007/s10499-009-9284-0
  51. Leduc A, Zatylny-Gaudin C, Robert M, Corre E, Corguille GL, Castel H, et al. Dietary aquaculture by-product hydrolysates: impact on the transcriptomic response of the intestinal mucosa of European seabass (Dicentrarchus labrax) fed low fish meal diets. BMC Genomics. 2018;19: 396. https://doi.org/10.1186/s12864-018-4780-0
  52. Li F, Huang S, Lu X, Wang J, Lin M, An Y. Effects of dietary supplementation with algal astaxanthin on growth, pigmentation, and antioxidant capacity of the blood parrot (Cichlasoma citrinellum × Cichlasoma synspilum ). J Oceanol Limnol. 2018;36:1851-9. https://doi.org/10.1007/s00343-019-7172-7
  53. Li M, Wu W, Zhou P, Xie F, Zhou Q, Mai K. Comparison effect of dietary astaxanthin and Haematococcus pluvialis on growth performance, antioxidant status and immune response of large yellow croaker Pseudosciaena crocea. Aquaculture. 2014;434:227-32. https://doi.org/10.1016/j.aquaculture.2014.08.022
  54. Liang M, Wang J, Chang Q, Mai K. Effects of different levels of fish protein hydrolysate in the diet on the nonspecific immunity of Japanese sea bass, Lateolabrax japonicus (Cuvieret Valenciennes, 1828). Aquac Res. 2006;37:102-6. https://doi.org/10.1111/j.1365-2109.2005.01392.x
  55. Lim KC, Yusoff FM, Shariff M, Kamarudin MS. Astaxanthin as feed supplement in aquatic animals. Rev Aquac. 2018;10:738-73. https://doi.org/10.1111/raq.12200
  56. Lopez-Cervantes J, Sanchez-Machado DI, Rios-Vazquez NJ. High-performance liquid chromatography method for the simultaneous quantification of retinol, α-tocopherol, and cholesterol in shrimp waste hydrolysate. J Chromatogr A. 2006;1105:135-9. https://doi.org/10.1016/j.chroma.2005.08.010
  57. Machado M, Azeredo R, Diaz-Rosales P, Afonso A, Peres H, Oliva-Teles A. Dietary tryptophan and methionine as modulators of European seabass (Dicentrarchus labrax) immune status and inflammatory response. Fish Shellfish Immunol. 2015;42:353-62. https://doi.org/10.1016/j.fsi.2014.11.024
  58. Magnadottir B. Innate immunity of fish (overview). Fish Shellfish Immunol. 2006;20:137-51. https://doi.org/10.1016/j.fsi.2004.09.006
  59. McCormick SD. Effects of growth hormone and insulin-like growth factor I on salinity tolerance and gill Na+, K+-ATPase in Atlantic salmon (Salmo salar): interaction with cortisol. Gen Comp Endocrinol. 1996;101:3-11. https://doi.org/10.1006/gcen.1996.0002
  60. Merimee TJ, Laron Z. Growth hormone, IGF-I and growth: new views of old concepts. London, UK: Freund; 1996.
  61. Meton I, Caseras A, Canto E, Fernandez F, Baanante IV. Liver insulin-like growth factor-I mRNA is not affected by diet composition or ration size but shows diurnal variations in regularly-fed gilthead sea bream (Sparus aurata). J Nutr. 2000;130:757-60. https://doi.org/10.1093/jn/130.4.757
  62. Meyers SP. Utilization of shrimp processing wastes. Infofish Mark Dig. 1986;4:18-9.
  63. Moriyama S, Ayson FG, Kawauchi H. Growth regulation by insulin-like growth factor-I in fish. Biosci Biotechnol Biochem. 2000;64:1553-62. https://doi.org/10.1271/bbb.64.1553
  64. Nii Y, Fukuta K, Yoshimoto R, Sakai K, Ogawa T. Determination of antihypertensive peptides from an izumi shrimp hydrolysate. Biosci Biotechnol Biochem. 2008;72:861-4. https://doi.org/10.1271/bbb.70565
  65. Nwanna LC. Nutritional value and digestibility of fermented shrimp head waste meal by african catfish Clarias gariepinus. Pakistan J Nutr. 2003;2:339-45. https://doi.org/10.3923/pjn.2003.339.345
  66. Olsen RE, Suontama J, Langmyhr E, Mundheim H, Ringo E, Melle W, et al. The replacement of fish meal with Antarctic krill, Euphausia superba in diets for Atlantic salmon, Salmo salar. Aquac Nutr. 2006;12:280-90. https://doi.org/10.1111/j.1365-2095.2006.00400.x
  67. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45. https://doi.org/10.1093/nar/29.9.e45
  68. Plascencia-Jatomea M, Olvera-Novoa MA, Arredondo-Figueroa JL, Hall GM, Shirai K. Feasibility of fishmeal replacement by shrimp head silage protein hydrolysate in Nile tilapia (Oreochromis niloticus L) diets. J Sci Food Agric. 2002;82:753-9. https://doi.org/10.1002/jsfa.1092
  69. Pohlenz C, Buentello A, Criscitiello MF, Mwangi W, Smith R, Gatlin III DM. Synergies between vaccination and dietary arginine and glutamine supplementation improve the immune response of channel catfish against Edwardsiella ictaluri. Fish Shellfish Immunol. 2012;33:543-51. https://doi.org/10.1016/j.fsi.2012.06.005
  70. Quade MJ, Roth JA. A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol. 1997;58:239-48. https://doi.org/10.1016/S0165-2427(97)00048-2
  71. Rajanbabu V, Chen JY. Applications of antimicrobial peptides from fish and perspectives for the future. Peptides. 2011;32:415-20. https://doi.org/10.1016/j.peptides.2010.11.005
  72. Ringo E, Zhou Z, Olsen RE, Song SK. Use of chitin and krill in aquaculture - the effect on gut microbiota and the immune system: a review. Aquac Nutr. 2012;18:117-31. https://doi.org/10.1111/j.1365-2095.2011.00919.x
  73. Rosenlund G, Torstensen BE, Stubhaug I, Usman N, Sissener NH. Atlantic salmon require long-chain n-3 fatty acids for optimal growth throughout the seawater period. J Nutr Sci. 2016 ;5:e19. https://doi.org/10.1017/jns.2016.10
  74. Saleh R, Burri L, Benitez-Santana T, Turkmen S, Castro P, Izquierdo M. Dietary krill meal inclusion contributes to better growth performance of gilthead seabream juveniles. Aquac Res. 2018;49:3289-95. https://doi.org/10.1111/are.13792
  75. Shahidi F, Synowiecki J. Isolation and characterization of nutrients and value-added products from snow crab (Chinoecetes opilio) and shrimp (Pandalus borealis) processing discards. J Agric Food Chem. 1991;39:1527-32. https://doi.org/10.1021/jf00008a032
  76. Shamblott MJ, Cheng CM, Bolt D, Chen TT. Appearance of insulin-like growth factor mRNA in the liver and pyloric ceca of a teleost in response to exogenous growth hormone. Proc Natl Acad Sci USA. 1995;92:6943-6. https://doi.org/10.1073/pnas.92.15.6943
  77. Shimizu C, Ibrahim A, Tokoro T, Shirakawa Y. Feeding stimulation in sea bream, Pagrus major, fed diets supplemented with Antarctic krill meals. Aquaculture. 1990;89:43-53. https://doi.org/10.1016/0044-8486(90)90232-C
  78. Siddik MAB, Howieson J, Fotedar R. Beneficial effects of tuna hydrolysate in poultry by-product meal diets on growth, immune response, intestinal health and disease resistance to Vibrio harveyi in juvenile barramundi, Lates calcarifer. Fish Shellfish Immunol. 2019;89:61-70. https://doi.org/10.1016/j.fsi.2019.03.042
  79. Silva-Carrillo Y, Hernandez C, Hardy RW, Gonzalez-Rodriguez B, Castillo-Vargasmachuca S. The effect of substituting fish meal with soybean meal on growth, feed efficiency, body composition and blood chemistry in juvenile spotted rose snapper Lutjanus guttatus (Steindachner, 1869). Aquaculture. 2012;364:180-5. https://doi.org/10.1016/j.aquaculture.2012.08.007
  80. Takagi S, Shimeno S, Hosokawa H, Ukawa M. Effect of lysine and methionine supplementation to a soy protein concentrate diet for red sea bream Pagrus major. Fish Sci. 2001;67:1088-96. https://doi.org/10.1046/j.1444-2906.2001.00365.x
  81. Takii K, Konishi K, Ukawa M, Nakamura M, Kumai H. Influence of feeding rates on digestion and energy flow in tiger puffer and red sea bream. Fish Sci. 1997;63:355-60. https://doi.org/10.2331/fishsci.63.355
  82. Teshima SI, Koshio S, Ishikawa M, Alam MS, Hernandez LHH. Effects of protein and lipid sources on the growth and survival of red sea bream Pagrus major and Japanese flounder Paralichthys olivaceus receiving micro-bound diets during larval and early juvenile stage. Aquac Nutr. 2004;10:279-87. https://doi.org/10.1111/j.1365-2095.2004.00303.x
  83. Tharaka K, Benitez-Santana T, Gunathilaka BE, Kim MG, Lee C, Shin J, et al. Evaluation of Antarctic krill (Euphausia superba) meal supplementation in diets for olive flounder (Paralichthys olivaceus ). Aquac Res. 2020;51:2291-302. https://doi.org/10.1111/are.14573
  84. Tibbetts SM, Milley JE, Lall SP. Apparent protein and energy digestibility of common and alternative feed ingredients by Atlantic cod, Gadus morhua (Linnaeus, 1758). Aquaculture. 2006;261:1314-27. https://doi.org/10.1016/j.aquaculture.2006.08.052
  85. Tilseth S, Hostmark O. New method for making krill meal. United States patent US20090061067. 2009 Mar 5.
  86. Valero Y, Saraiva-Fraga M, Costas B, Guardiola FA. Antimicrobial peptides from fish: beyond the fight against pathogens. Rev Aquac. 2020;12:224-53. https://doi.org/10.1111/raq.12314
  87. Wei Y, Shen H, Xu W, Pan Y, Chen J, Zhang W, Mai K. Replacement of dietary fishmeal by Antarctic krill meal on growth performance, intestinal morphology, body composition and organoleptic quality of large yellow croaker Larimichthys crocea. Aquaculture 2019;512:734281. https://doi.org/10.1016/j.aquaculture.2019.734281
  88. Xie D, Gong M, Wei W, Jin J, Wang X, Wang X. Antarctic krill (Euphausia superba) oil: a comprehensive review of chemical composition, extraction technologies, health benefits, andApplications. Compr Rev Food Sci Food Saf. 2019;18:514-34. https://doi.org/10.1111/1541-4337.12427
  89. Xie JJ, Chen X, Liu YJ, Tian LX, Xie SW, Niu J. Effects of dietary astaxanthin on growth performance, hepatic antioxidative activity, hsp70, and HIF-1α gene expression of juvenile golden pompano (Trachinotus ovatus). Isr J Aquac. Bamidgeh. 2017;69:12.
  90. Yamamoto T, Akimoto A, Kishi S, Unuma T, Akiyama T. Apparent and true availabilities of amino acids from several protein sources for fingerling rainbow trout, common carp, and red sea bream. Fish Sci. 1998;64:448-58. https://doi.org/10.2331/fishsci.64.448
  91. Yan J, Chang Q, Chen S, Wang Z, Lu B, Liu C. Effect of dietary antarctic krill meal on growth performance, muscle proximate composition, and antioxidative capacity of juvenile spotted halibut, Verasper variegatus. J World Aquac Soc. 2018;49:761-69. https://doi.org/10.1111/jwas.12455
  92. Yoshitomi B, Aoki M, Oshima SI, Hata K. Evaluation of krill (Euphausia superba) meal as a partial replacement for fish meal in rainbow trout (Oncorhynchus mykiss) diets. Aquaculture. 2006;261:440-6. https://doi.org/10.1016/j.aquaculture.2006.06.036
  93. Zheng K, Liang M, Yao H, Wang J, Chang Q. Effect of dietary fish protein hydrolysate on growth, feed utilization and IGF-I levels of Japanese flounder (Paralichthys olivaceus). Aquac Nutr. 2012;18:297-303. https://doi.org/10.1111/j.1365-2095.2011.00896.x