INFLUENCE OF A BLEND OF DIETARY ESSENTIAL AMINO ACIDS ON GROWTH, ENZYMATIC ACTIVITY, AND INTESTINAL HISTOLOGY OF BLUE DISCUS
DOI:
https://doi.org/10.20950/1678-2305/bip.2021.47.e599Keywords:
aquaculture;, amino acids;, ornamental fish;, protein;, Symphysodon aequifasciatus.Abstract
Symphysodon aequifasciatus is a fish with a disk-shaped body and bright colors, important characteristics of ornamental fish. We evaluated amino acid supplementation strategies to reduce crude protein in the diet for evaluation of performance, the content of digestive enzymes, liver metabolism, and intestinal histopathology. A total of 180 fish were randomly distributed in 12 separate 50 L glass aquariums, consisting of a completely randomized design with four treatments (DC - Control diet with 34.4% crude protein; DL - Control diet plus 1% of lysine; DEAA - Control diet plus 1% free essential amino acids (threonine, phenylalanine, leucine, valine, arginine, and tryptophan); and DHP - Diet with a high level of crude protein 48.4%), three repetitions, lasting 60 days. The use of DL and DEAA diets resulted in higher intestinal villus height and higher zootechnical performance. The use of DL diet increased alkaline phosphatase and digestive amylase activity. The use of DHP diets promotes severe liver changes due to increased activity of Alanine aminotraserase. Therefore, it was possible to observe that the use of amino acids can supply the nutritional need of blue discus. Supplementation of diets with AAs allows the reduction of dietary protein, which is a strategy for feeding management.
References
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Bomfim, M.D.; Lanna, E.A.T.; Donzele, J.L.; Quadros, M.; Ribeiro, F.B.; Sousa, M.P.D. 2010. Níveis de lisina, com base no conceito de proteína ideal, em rações para alevinos de tilápia-do-nilo. Revista Brasileira de Zootecnia, 39(1): 1-8. https://doi.org/10.1590/S1516-35982010000100001.
Botaro, D.; Furuya, W.M.; Silva, L.C.R.; Santos, L.D.D.; Silva, T.S.D.C.; Santos, V.G.D. 2007. Redução de proteína na dieta com base no conceito ideal de proteína para tilápia do Nilo (Oreochromis niloticus) cultivada em viveiro. Revista Brasileira de Zootecnia, 36(3): 517-525. https://doi.org/10.1590/S1516-35982007000300001.
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2): 248-254. https://doi.org/10.1016/0003-2697(76)90527-3.
Chellapan, A.; Rajagopalsamy, C.B.T.; Jasmine, G.I. 2013. Effect of clove oil and benzocaine on the respiratory metabolism of Angel Fish, Pterophyllum scalare. Indian Journal of Science and Technology, 6(7): 4853-4861. https://doi.org/10.17485/ijst/2013/v6i7.1.
Cheng, Z.J.; Hardy, R.W.; Usry, J.L. 2003. Plant protein ingredients with lysine supplementation reduce dietary protein level in rainbow trout (Oncorhynchus mykiss) diets, and reduce ammonia nitrogen and soluble phosphorus excretion. Aquaculture, 218(1-4): 553-565. https://doi.org/10.1016/S0044-8486(02)00502-1.
Chong, A.S.C.; Hashim, R.; Ali, A.B. 2008. Dietary protein requirements for discus (Symphysodon spp). Aquaculture Nutrition, 6(4): 275-278. https://doi.org/10.1046/j.1365-2095.2000.00151.x.
Chong, A.S.C.; Hashim, R.; Chow-Yang, L.; Ali, A.B. 2002. Partial characterization and activities of proteases from the digestive tract of discus fish (Symphysodon aequifasciata). Aquaculture, 203(3-4): 321-333. https://doi.org/10.1016/S0044-8486(01)00630-5.
Crampton, W.G. 2008. Ecology and life history of an Amazon floodplain cichlid: the discus fish Symphysodon (Perciformes: Cichlidae). Neotropical Ichthyology, 6(4): 599-612. https://doi.org/10.1590/S1679-62252008000400008.
Degani, G. 1993. Growth and body composition of juveniles of Pterophyllum scalare (Lichtenstein) (Pisces; Cichlidae) at different densities and diets. Aquaculture Research, 24(6): 725-730. https://doi.org/10.1111/j.1365-2109.1993.tb00651.x.
Diemer, O.; Bittencourt, F.; Barcellos, L.G.; Boscolo, W.R.; Feiden, A.; Romagosa, E. 2014. Lysine in the diet of Rhamdia voulezi male brood stocks confined in net cages. Aquaculture, 434: 93-99. https://doi.org/10.1016/j.aquaculture.2014.07.029.
Dorce, L.S.; Mendonça, W.C.B.; Siqueira, M.S.; Santos, R.F.B.; Sousa, R.M.; Ziemniczak, H.M.; Honoraro, C.A. 2020. Atividade das enzimas digestivas frente a restrição alimentar de peixes ornamentais. Agrarian, 13(47): 107-113. https://doi.org/10.30612/agrarian.v13i47.9912.
Froese, R.; Pauly, D. 2019. FishBase. World Wide Web electronic publication. Available at: <https://www.fishbase.se/summary/Symphysodon-aequifasciatus.html> Accessed: Jun. 29, 2020.
Honorato, C.A.; De Almeida, L.C.; Da Silva, N.C.; Carneiro, D.J.; Moraes, G. 2010. Effects of processing on physical characteristics of diets with distinct levels of carbohydrates and lipids: the outcomes on the growth of pacu (Piaractus mesopotamicus). Aquaculture Nutrition, 16(1): 91-99. https://doi.org/10.1111/j.1365-2095.2008.00644.x.
Honorato, C.A.; Ushizima, T.T.; Quintana, C.I.F.; Campos, C.M.; Marcondes, V.M.; Nascimento, C.A.; Santamaria, F.M. 2014. Níveis de proteína digestível para surubim (Pseudoplatystoma sp.) criados em tanque-rede. Semina: Ciências Agrárias, 35(5): 2781-2792. http://dx.doi.org/10.5433/1679-0359.2014v35n5p2781.
Liquori, G.E.; Mastrodonato, M.; Zizza, S.; Ferri, D. 2007. Glycoconjugate histochemistry of the digestive tract of Triturus carnifex (Amphibia, Caudata). Journal of Molecular Histology, 38(3): 191-199. https://doi.org/10.1007/s10735-007-9087-4.
Magouz, F.I.; Dawood, M.A.; Salem, M.F.; El-Ghandour, M.; Van Doan, H.; Mohamed, A.A. 2020. The role of a digestive enhancer in improving the growth performance, digestive enzymes activity, and health condition of Nile tilapia (Oreochromis niloticus) reared under suboptimal temperature. Aquaculture, 526: 735388. https://doi.org/10.1016/j.aquaculture.2020.735388.
McManus, J.F.A. 1948. Histological and histochemical uses of periodic acid. Stain Technology, 23(3): 99-108. https://doi.org/10.3109/10520294809106232.
Meng, X.L.; Li, S.; Qin, C.B.; Zhu, Z.X.; Hu, W.P.; Yang, L.P.; Lu, R.H.; Li, W.J.; Nie, G.X. 2018. Intestinal microbiota and lipid metabolism responses in the common carp (Cyprinus carpio L.) following copper exposure. Ecotoxicology and Environmental Safety, 160: 257-264. https://doi.org/10.1016/j.ecoenv.2018.05.050.
Morales, A.; Buenabad, L.; Castillo, G.; Vázquez, L.; Espinoza, S.; Htoo, J.K.; Cervantes, M. 2017. Dietary levels of protein and free amino acids affect pancreatic proteases activities, amino acids transporters expression and serum amino acid concentrations in starter pigs. Journal of Animal Physiology and Animal Nutrition, 101(4): 723-732. https://doi.org/10.1111/jpn.12515.
Murashita, K.; Matsunaria, H.; Furuita, H.; Rí¸nnestad, I.; Oku, H.; Yamamoto, T. 2018. Effects of dietary soybean meal on the digestive physiology of red seabream Pagrus major. Aquaculture, 493: 219-228. https://doi.org/10.1016/j.aquaculture.2018.05.005.
NRC í National Research Council. 2011. Nutrient requirements of warmwater fishes and shellfishes. Washington, D.C.: NRC. 392p.
Nunes, C.S.; Moraes, G.; Fabrizzi, F.; Hackbarth, A.; Arbeláez-Rojas, G.A. 2013. Growth and hematology of pacu subjected to sustained swimming and fed different protein levels. Pesquisa Agropecuária Brasileira, 48(6): 645-650. https://doi.org/10.1590/S0100-204X2013000600010.
Ortiz-Delgado, J.B.; Darias, M.J.; Caí±avate, J.P.; Yúfera, M.; Sarasquete, C. 2003. Organogenesis of the digestive tract in the white seabream, Diplodus sargus. Histological and histochemical approaches. Histology and Histopathology, 18: 1141-1154. https://doi.org/10.14670/HH-18.1141.
Ota, C.E.; Honorato, C.A.; Heredia-Vieira, S.C.; Flores-Quintana, C.I.; Castro Silva, T.S.; Inoue, L.A.K.A.; Cardoso, C.A.L. 2019. Hepatic and gastroprotective activity of Serjania marginata leaf aqueous extract in Nile tilapia (Oreochromis niloticus). Fish Physiology and Biochemistry, 45: 1051-1065. https://doi.org/10.1007/s10695-019-00622-9.
Park, J.T.; Johnson, M.J. 1949. A sub micro determination of glucose. The Journal of Biological Chemistry, 181: 149-151.
Pujante, I.M.; Díaz-López, M.; Mancera, J.M.; Moyano, F.J. 2017. Characterization of digestive enzymes protease and alpha-amylase activities in the thick-lipped grey mullet (Chelon labrosus, Risso 1827). Aquaculture Research, 48(2): 367-376. https://doi.org/10.1111/are.13038.
Reitman, S.; Frankel, S. 1957. A colorimetric method for determination of serum glutamic oxaloacetic and glutamic pyruvic transaminase. American Journal of Clinical Pathology, 28(1): 56-63. https://doi.org/10.1093/ajcp/28.1.56.
Ren, M.; He, J.; Liang, H.; Ji, K.; Ge, X.; Sun, A.; Pan, L.; Masagounder, K. 2019. Use of supplemental amino acids on the success of reducing dietary protein levels for Jian carp (Cyprinus carpio var. Jian). Aquaculture Nutrition, 25(3): 567-576. https://doi.org/10.1111/anu.12879.
Ribeiro, F.D.A.S.; De Lima Preto, B.; Fernandes, J.B.K. 2008. Sistemas de criação para o acará-bandeira (Pterophyllum scalare). Acta Scientiarum. Animal Sciences, 30(4): 459-466. https://doi.org/10.4025/actascianimsci.v30i4.685.
Romarheim, O.H.; Zhang, C.; Penn, M.; Liu, Y.J.; Tian, L.X.; Skrede, A.; Krogdahl, A.; Storebakken, T. 2008. Growth and intestinal morphology in cobia (Rachycentron canadum) fed extruded diets with two types of soybean meal partly replacing fish meal. Aquaculture Nutrition, 14(2): 174-180. https://doi.org/10.1111/j.1365-2095.2007.00517.x.
Saavedra, M.; Pereira, T.G.; Candeias-Mendes, A. 2017. Dietary amino acid profile affects muscle cellularity, growth, survival and ammonia excretion of meagre (Argyrosomus regius) larvae. Aquaculture Nutrition, 24(2): 814-820. https://doi.org/10.1111/anu.12610.
Walter, H.E. 1984. Probionases: methods with haemoglobin casein and azocoll as substrates In: Bergmeyer, H.U. (ed.). Methods of enzymatic analysis. Germany: Verlag Chemie. pp. 270-277.
Wen, B.; Chen, Z.; Qu, H.; Gao, J. 2018. Growth and fatty acid composition of discus fish Symphysodon haraldi given varying feed ratios of beef heart, duck heart, and shrimp meat. Aquaculture and Fisheries, 3(2): 84-89. https://doi.org/10.1016/j.aaf.2018.01.002.
Xiao, W.W.; Feng, L.; Liu, Y.; Jiang, J.; Hu, K.; Jiang, W.D.; Li, S.H.; Zhou, X.Q. 2011. Effects of dietary methionine hydroxy analogue supplement on growth, protein deposition and intestinal enzymes activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture Nutrition, 17(4): 408-417. https://doi.org/10.1111/j.1365-2095.2010.00818.x.
Xu, D.; He, G.; Mai, K.; Wang, Q.; Li, M.; Zhou, H.; Xu, W.; Song, F. 2017. Effect of fish meal replacement by plant protein blend on amino acid concentration, transportation and metabolism in juvenile turbot (Scophthalmus maximus L). Aquaculture Nutrition, 23(5): 1169-1178. https://doi.org/10.1111/anu.12486.
Zambonino Infante, J.L.; Cahu, C.L. 2007. Dietary modulation of some digestive enzymes and Metabolic processes in developing marine fish: Applications to diet formulation. Aquaculture, 268(1-4): 98-105. https://doi.org/10.1016/j.aquaculture.2007.04.032.
Zuanon, J.A.S.; Morais, J.A.; Souza, A.P. 2016. Dietary crude protein levels for juvenile beta. Boletim do Instituto de Pesca, 42(3): 590-597. https://doi.org/10.20950/1678-2305.2016v42n3p590.
Zuanon, J.A.S.; Salaro, A.L.; Moraes, S.S.S.; Alves, L.M.D.O.; Balbino, E.M.; Araújo, E.S. 2009. Dietary protein and energy requirements of juvenile freshwater angelfish. Revista Brasileira de Zootecnia, 38(6): 989-993. https://doi.org/10.1590/S1516-35982009000600003.
AOAC í Association of Official Analytical Chemists. 1999. Official methods of analysis of the association of official analytical chemists, 16th ed. Arlington, D.C: AOAC. 1141p.
Bernfeld, P. 1955. Amylases, α and β. In: Colowick, S.P.; Kaplan, N.O. (eds.). Methods in enzymology. USA: Elsevier. v. 1, p. 149-158. https://doi.org/10.1016/0076-6879(55)01021-5.
Bomfim, M.D.; Lanna, E.A.T.; Donzele, J.L.; Quadros, M.; Ribeiro, F.B.; Sousa, M.P.D. 2010. Níveis de lisina, com base no conceito de proteína ideal, em rações para alevinos de tilápia-do-nilo. Revista Brasileira de Zootecnia, 39(1): 1-8. https://doi.org/10.1590/S1516-35982010000100001.
Botaro, D.; Furuya, W.M.; Silva, L.C.R.; Santos, L.D.D.; Silva, T.S.D.C.; Santos, V.G.D. 2007. Redução de proteína na dieta com base no conceito ideal de proteína para tilápia do Nilo (Oreochromis niloticus) cultivada em viveiro. Revista Brasileira de Zootecnia, 36(3): 517-525. https://doi.org/10.1590/S1516-35982007000300001.
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2): 248-254. https://doi.org/10.1016/0003-2697(76)90527-3.
Chellapan, A.; Rajagopalsamy, C.B.T.; Jasmine, G.I. 2013. Effect of clove oil and benzocaine on the respiratory metabolism of Angel Fish, Pterophyllum scalare. Indian Journal of Science and Technology, 6(7): 4853-4861. https://doi.org/10.17485/ijst/2013/v6i7.1.
Cheng, Z.J.; Hardy, R.W.; Usry, J.L. 2003. Plant protein ingredients with lysine supplementation reduce dietary protein level in rainbow trout (Oncorhynchus mykiss) diets, and reduce ammonia nitrogen and soluble phosphorus excretion. Aquaculture, 218(1-4): 553-565. https://doi.org/10.1016/S0044-8486(02)00502-1.
Chong, A.S.C.; Hashim, R.; Ali, A.B. 2008. Dietary protein requirements for discus (Symphysodon spp). Aquaculture Nutrition, 6(4): 275-278. https://doi.org/10.1046/j.1365-2095.2000.00151.x.
Chong, A.S.C.; Hashim, R.; Chow-Yang, L.; Ali, A.B. 2002. Partial characterization and activities of proteases from the digestive tract of discus fish (Symphysodon aequifasciata). Aquaculture, 203(3-4): 321-333. https://doi.org/10.1016/S0044-8486(01)00630-5.
Crampton, W.G. 2008. Ecology and life history of an Amazon floodplain cichlid: the discus fish Symphysodon (Perciformes: Cichlidae). Neotropical Ichthyology, 6(4): 599-612. https://doi.org/10.1590/S1679-62252008000400008.
Degani, G. 1993. Growth and body composition of juveniles of Pterophyllum scalare (Lichtenstein) (Pisces; Cichlidae) at different densities and diets. Aquaculture Research, 24(6): 725-730. https://doi.org/10.1111/j.1365-2109.1993.tb00651.x.
Diemer, O.; Bittencourt, F.; Barcellos, L.G.; Boscolo, W.R.; Feiden, A.; Romagosa, E. 2014. Lysine in the diet of Rhamdia voulezi male brood stocks confined in net cages. Aquaculture, 434: 93-99. https://doi.org/10.1016/j.aquaculture.2014.07.029.
Dorce, L.S.; Mendonça, W.C.B.; Siqueira, M.S.; Santos, R.F.B.; Sousa, R.M.; Ziemniczak, H.M.; Honoraro, C.A. 2020. Atividade das enzimas digestivas frente a restrição alimentar de peixes ornamentais. Agrarian, 13(47): 107-113. https://doi.org/10.30612/agrarian.v13i47.9912.
Froese, R.; Pauly, D. 2019. FishBase. World Wide Web electronic publication. Available at: <https://www.fishbase.se/summary/Symphysodon-aequifasciatus.html> Accessed: Jun. 29, 2020.
Honorato, C.A.; De Almeida, L.C.; Da Silva, N.C.; Carneiro, D.J.; Moraes, G. 2010. Effects of processing on physical characteristics of diets with distinct levels of carbohydrates and lipids: the outcomes on the growth of pacu (Piaractus mesopotamicus). Aquaculture Nutrition, 16(1): 91-99. https://doi.org/10.1111/j.1365-2095.2008.00644.x.
Honorato, C.A.; Ushizima, T.T.; Quintana, C.I.F.; Campos, C.M.; Marcondes, V.M.; Nascimento, C.A.; Santamaria, F.M. 2014. Níveis de proteína digestível para surubim (Pseudoplatystoma sp.) criados em tanque-rede. Semina: Ciências Agrárias, 35(5): 2781-2792. http://dx.doi.org/10.5433/1679-0359.2014v35n5p2781.
Liquori, G.E.; Mastrodonato, M.; Zizza, S.; Ferri, D. 2007. Glycoconjugate histochemistry of the digestive tract of Triturus carnifex (Amphibia, Caudata). Journal of Molecular Histology, 38(3): 191-199. https://doi.org/10.1007/s10735-007-9087-4.
Magouz, F.I.; Dawood, M.A.; Salem, M.F.; El-Ghandour, M.; Van Doan, H.; Mohamed, A.A. 2020. The role of a digestive enhancer in improving the growth performance, digestive enzymes activity, and health condition of Nile tilapia (Oreochromis niloticus) reared under suboptimal temperature. Aquaculture, 526: 735388. https://doi.org/10.1016/j.aquaculture.2020.735388.
McManus, J.F.A. 1948. Histological and histochemical uses of periodic acid. Stain Technology, 23(3): 99-108. https://doi.org/10.3109/10520294809106232.
Meng, X.L.; Li, S.; Qin, C.B.; Zhu, Z.X.; Hu, W.P.; Yang, L.P.; Lu, R.H.; Li, W.J.; Nie, G.X. 2018. Intestinal microbiota and lipid metabolism responses in the common carp (Cyprinus carpio L.) following copper exposure. Ecotoxicology and Environmental Safety, 160: 257-264. https://doi.org/10.1016/j.ecoenv.2018.05.050.
Morales, A.; Buenabad, L.; Castillo, G.; Vázquez, L.; Espinoza, S.; Htoo, J.K.; Cervantes, M. 2017. Dietary levels of protein and free amino acids affect pancreatic proteases activities, amino acids transporters expression and serum amino acid concentrations in starter pigs. Journal of Animal Physiology and Animal Nutrition, 101(4): 723-732. https://doi.org/10.1111/jpn.12515.
Murashita, K.; Matsunaria, H.; Furuita, H.; Rí¸nnestad, I.; Oku, H.; Yamamoto, T. 2018. Effects of dietary soybean meal on the digestive physiology of red seabream Pagrus major. Aquaculture, 493: 219-228. https://doi.org/10.1016/j.aquaculture.2018.05.005.
NRC í National Research Council. 2011. Nutrient requirements of warmwater fishes and shellfishes. Washington, D.C.: NRC. 392p.
Nunes, C.S.; Moraes, G.; Fabrizzi, F.; Hackbarth, A.; Arbeláez-Rojas, G.A. 2013. Growth and hematology of pacu subjected to sustained swimming and fed different protein levels. Pesquisa Agropecuária Brasileira, 48(6): 645-650. https://doi.org/10.1590/S0100-204X2013000600010.
Ortiz-Delgado, J.B.; Darias, M.J.; Caí±avate, J.P.; Yúfera, M.; Sarasquete, C. 2003. Organogenesis of the digestive tract in the white seabream, Diplodus sargus. Histological and histochemical approaches. Histology and Histopathology, 18: 1141-1154. https://doi.org/10.14670/HH-18.1141.
Ota, C.E.; Honorato, C.A.; Heredia-Vieira, S.C.; Flores-Quintana, C.I.; Castro Silva, T.S.; Inoue, L.A.K.A.; Cardoso, C.A.L. 2019. Hepatic and gastroprotective activity of Serjania marginata leaf aqueous extract in Nile tilapia (Oreochromis niloticus). Fish Physiology and Biochemistry, 45: 1051-1065. https://doi.org/10.1007/s10695-019-00622-9.
Park, J.T.; Johnson, M.J. 1949. A sub micro determination of glucose. The Journal of Biological Chemistry, 181: 149-151.
Pujante, I.M.; Díaz-López, M.; Mancera, J.M.; Moyano, F.J. 2017. Characterization of digestive enzymes protease and alpha-amylase activities in the thick-lipped grey mullet (Chelon labrosus, Risso 1827). Aquaculture Research, 48(2): 367-376. https://doi.org/10.1111/are.13038.
Reitman, S.; Frankel, S. 1957. A colorimetric method for determination of serum glutamic oxaloacetic and glutamic pyruvic transaminase. American Journal of Clinical Pathology, 28(1): 56-63. https://doi.org/10.1093/ajcp/28.1.56.
Ren, M.; He, J.; Liang, H.; Ji, K.; Ge, X.; Sun, A.; Pan, L.; Masagounder, K. 2019. Use of supplemental amino acids on the success of reducing dietary protein levels for Jian carp (Cyprinus carpio var. Jian). Aquaculture Nutrition, 25(3): 567-576. https://doi.org/10.1111/anu.12879.
Ribeiro, F.D.A.S.; De Lima Preto, B.; Fernandes, J.B.K. 2008. Sistemas de criação para o acará-bandeira (Pterophyllum scalare). Acta Scientiarum. Animal Sciences, 30(4): 459-466. https://doi.org/10.4025/actascianimsci.v30i4.685.
Romarheim, O.H.; Zhang, C.; Penn, M.; Liu, Y.J.; Tian, L.X.; Skrede, A.; Krogdahl, A.; Storebakken, T. 2008. Growth and intestinal morphology in cobia (Rachycentron canadum) fed extruded diets with two types of soybean meal partly replacing fish meal. Aquaculture Nutrition, 14(2): 174-180. https://doi.org/10.1111/j.1365-2095.2007.00517.x.
Saavedra, M.; Pereira, T.G.; Candeias-Mendes, A. 2017. Dietary amino acid profile affects muscle cellularity, growth, survival and ammonia excretion of meagre (Argyrosomus regius) larvae. Aquaculture Nutrition, 24(2): 814-820. https://doi.org/10.1111/anu.12610.
Walter, H.E. 1984. Probionases: methods with haemoglobin casein and azocoll as substrates In: Bergmeyer, H.U. (ed.). Methods of enzymatic analysis. Germany: Verlag Chemie. pp. 270-277.
Wen, B.; Chen, Z.; Qu, H.; Gao, J. 2018. Growth and fatty acid composition of discus fish Symphysodon haraldi given varying feed ratios of beef heart, duck heart, and shrimp meat. Aquaculture and Fisheries, 3(2): 84-89. https://doi.org/10.1016/j.aaf.2018.01.002.
Xiao, W.W.; Feng, L.; Liu, Y.; Jiang, J.; Hu, K.; Jiang, W.D.; Li, S.H.; Zhou, X.Q. 2011. Effects of dietary methionine hydroxy analogue supplement on growth, protein deposition and intestinal enzymes activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture Nutrition, 17(4): 408-417. https://doi.org/10.1111/j.1365-2095.2010.00818.x.
Xu, D.; He, G.; Mai, K.; Wang, Q.; Li, M.; Zhou, H.; Xu, W.; Song, F. 2017. Effect of fish meal replacement by plant protein blend on amino acid concentration, transportation and metabolism in juvenile turbot (Scophthalmus maximus L). Aquaculture Nutrition, 23(5): 1169-1178. https://doi.org/10.1111/anu.12486.
Zambonino Infante, J.L.; Cahu, C.L. 2007. Dietary modulation of some digestive enzymes and Metabolic processes in developing marine fish: Applications to diet formulation. Aquaculture, 268(1-4): 98-105. https://doi.org/10.1016/j.aquaculture.2007.04.032.
Zuanon, J.A.S.; Morais, J.A.; Souza, A.P. 2016. Dietary crude protein levels for juvenile beta. Boletim do Instituto de Pesca, 42(3): 590-597. https://doi.org/10.20950/1678-2305.2016v42n3p590.
Zuanon, J.A.S.; Salaro, A.L.; Moraes, S.S.S.; Alves, L.M.D.O.; Balbino, E.M.; Araújo, E.S. 2009. Dietary protein and energy requirements of juvenile freshwater angelfish. Revista Brasileira de Zootecnia, 38(6): 989-993. https://doi.org/10.1590/S1516-35982009000600003.
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2021-06-24
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