Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 853–868 | Cite as

Gastrointestinal and hepatic enzyme activities in juvenile silvery-black porgy (Sparidentex hasta) fed essential amino acid-deficient diets

  • Morteza Yaghoubi
  • Mansour Torfi Mozanzadeh
  • Omid Safari
  • Jasem G. Marammazi


As amino acids (AAs) are vital molecules in the metabolism of all living organisms and are the building blocks of enzymes, a 6-week feeding trial was conducted for determining the influence of dietary essential amino acid (EAA) deficiencies on pancreatic, plasma, and hepatic enzyme activities in silvery-black porgy (initial weight 4.7 ± 0.01 g) juveniles. Eleven isoproteic (ca. 47%) and isoenergetic (ca. 20.5 MJ kg−1) diets were formulated including a control diet, in which 60% of dietary nitrogen were provided by intact protein (fish meal, gelatin, and wheat meal) and 40% by crystalline AA. The other 10 diets were formulated by 40% reduction in each EAA from the control diet. At the end of the experiment, fish fed with threonine-deficient diet showed the lowest survival rate (P < 0.05), whereas growth performance decreased in fish fed all EAA-deficient diets, although the reduction in body growth varied depending on the EAA considered. Pancreatic enzymes (trypsin, lipase, α-amylase, and carboxypeptidase A) activities significantly decreased in fish fed the EAA-deficient diets in comparison with fish fed the control diet (P < 0.05). Fish fed with the arginine-deficient diet had the highest plasma and liver alanine aminotransferase, aspartate aminotransferase, and alkaline phosphatase levels (P < 0.05). Plasma and liver lactate dehydrogenase and superoxide dismutase showed the highest and lowest values, respectively, in fish fed the arginine and lysine-deficient diets (P < 0.05). Plasma metabolites were significantly affected by dietary EAA deficiencies (P < 0.05). The results of this study suggesting dietary EAA deficiencies led to reduction in growth performance as well as pancreatic and liver malfunction. Furthermore, arginine and lysine are the most limited EAA for digestive enzyme activities and liver health in silvery-black porgy.


Digestive enzymes Essential amino acid deficiency Liver health Plasma biochemistry Sparidentex hasta 



This article is extracted from the project recorded under code number of 92011610 and financially supported by Iran National Science Foundation. We are grateful to the director and staff of the Mariculture Research Station, Sarbandar, Iran, for providing the necessary facilities for the experiment.


  1. Ajeniyi SA, Solomon RJ (2014) Urea and creatinine of Clarias gariepinus in three different commercial ponds. Nat Sci 12:124–138Google Scholar
  2. Aldman G, Grove D, Holmgren S (1992) Duodenal acidification and intra-arterial injection of CCK8 increase gallbladder motility in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 86:20–25CrossRefPubMedGoogle Scholar
  3. Andersen SM, Taylor R, Holen E, Aksnes A, Espe M (2014) Arginine supplementation and exposure time affects polyamine and glucose metabolism in primary liver cells isolated from Atlantic salmon. Amino Acids 46:1225–1233CrossRefPubMedGoogle Scholar
  4. Andersen S, Waagbo R, Espe M (2015) Functional amino acids in fish nutrition, health and welfare. Front Biosci (Elite Ed) 8:143–169Google Scholar
  5. Andreasen P (1985) Free and total calcium concentrations in the blood of rainbow trout, Salmo gairdneri, during ‘stress’ conditions. J Exp Biol 118:111–120Google Scholar
  6. AOAC (2005) Official methods of analysis of AOAC international, AOAC InternationalGoogle Scholar
  7. Arias I, Jakoby W, Popper H, Schachter D, Shafritz D (1988) The liver: biology and pathobiology, 2nd edn. Raven Press, New YorkGoogle Scholar
  8. Barcellos L, Nicolaiewsky S, De Souza S, Lulhier F (1999) Plasmatic levels of cortisol in the response to acute stress in Nile tilapia, Oreochromis niloticus (L.), previously exposed to chronic stress. Aquac Res 30(6):437–444. CrossRefGoogle Scholar
  9. Barcellos LJG, Kreutz LC, Quevedo RM, da Rosa JGS, Koakoski G, Centenaro L, Pottker E (2009) Influence of color background and shelter availability on jundiá (Rhamdia quelen) stress response. Aquaculture 288(1-2):51–56. CrossRefGoogle Scholar
  10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2):248–254. CrossRefPubMedGoogle Scholar
  11. Brosnan JT, da Silva R, Brosnan ME (2007) Amino acids and the regulation of methyl balance in humans. Curr Opin Clin Nutr Metab Care 10(1):52–57. CrossRefPubMedGoogle Scholar
  12. Buentello JA, Gatlin DM (1999) Nitric oxide production in activated macrophages from channel catfish (Ictalurus punctatus): influence of dietary arginine and culture media. Aquaculture 179(1-4):513–521. CrossRefGoogle Scholar
  13. Chen G, Feng L, Kuang S, Liu Y, Jiang J, Hu K, Jiang W, Li S, Tang L, Zhou X (2012) Effect of dietary arginine on growth, intestinal enzyme activities and gene expression in muscle, hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Br J Nutr 108(02):195–207. CrossRefPubMedGoogle Scholar
  14. Coz-Rakovac R, Strunjak-Perovic I, Hacmanjek M, Lipej Z, Sostaric B (2005) Blood chemistry and histological properties of wild and cultured sea bass (Dicentrarchus labrax) in the North Adriatic Sea. Vet Res Commun 29:677–687CrossRefPubMedGoogle Scholar
  15. Deng J, Mai K, Ai Q, Zhang W, Tan B, Xu W, Liufu Z (2010) Alternative protein sources in diets for Japanese flounder Paralichthys olivaceus (Temminck and Schlegel): II. Effects on nutrient digestibility and digestive enzyme activity. Aquac Res 41:861–870CrossRefGoogle Scholar
  16. Dong M, Feng L, Kuang SY, Liu Y, Jiang J, Hu K, Jiang WD, Li SH, Tang L, Zhou XQ (2013) Growth, body composition, intestinal enzyme activities and microflora of juvenile Jian carp (Cyprinus carpio var. Jian) fed graded levels of dietary valine. Aquac Nutr 19(1):1–14. CrossRefGoogle Scholar
  17. Dorcas IK, Solomon RJ (2014) Calculation of liver function test in Clarias gariepinus collected from three commercial fish ponds. Nat Sci 12:107–123Google Scholar
  18. Erlanger BF, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278CrossRefPubMedGoogle Scholar
  19. Feng L, Li W, Liu Y, Jiang WD, Kuang SY, Jiang J, Tang L, Wu P, Tang WN, Zhang YA, Zhou XQ (2015) Dietary phenylalanine-improved intestinal barrier health in young grass carp (Ctenopharyngodon idella) is associated with increased immune status and regulated gene expression of cytokines, tight junction proteins, antioxidant enzymes and related signalling molecules. Fish Shellfish Immunol 45(2):495–509. CrossRefPubMedGoogle Scholar
  20. Folk J, Schirmer E (1963) The porcine pancreatic carboxypeptidase A system I. Three forms of the active enzyme. J Biol Chem 238:3884–3894PubMedGoogle Scholar
  21. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64(1):97–112. CrossRefPubMedGoogle Scholar
  22. Gao YJ, Yang HJ, Liu YJ, Chen SJ, Guo DQ, Yy Y, Tian LX (2014) Effects of graded levels of threonine on growth performance, biochemical parameters and intestine morphology of juvenile grass carp Ctenopharyngodon idella. Aquaculture 424:113–119CrossRefGoogle Scholar
  23. García-Gasca A, Galaviz MA, Gutiérrez JN, García-Ortega A (2006) Development of the digestive tract, trypsin activity and gene expression in eggs and larvae of the bullseye puffer fish Sphoeroides annulatus. Aquaculture 251(2-4):366–376. CrossRefGoogle Scholar
  24. Gawlicka A, Parent B, Horn MH, Ross N, Opstad I, Torrissen OJ (2000) Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture 184(3-4):303–314. CrossRefGoogle Scholar
  25. Gilloteaux J, Kashouty R, Yono N (2008) The perinuclear space of pancreatic acinar cells and the synthetic pathway of zymogen in Scorpaena scrofa L.: ultrastructural aspects. Tissue Cell 40:7–20CrossRefPubMedGoogle Scholar
  26. Gisbert E, Giménez G, Fernández I, Kotzamanis Y, Estévez A (2009) Development of digestive enzymes in common dentex Dentex dentex during early ontogeny. Aquaculture 287:381–387CrossRefGoogle Scholar
  27. Glover CN, Bury NR, Hogstrand C (2003) Zinc uptake across the apical membrane of freshwater rainbow trout intestine is mediated by high affinity, low affinity, and histidine-facilitated pathways. Biochim Biophys Acta Biomembr 1614(2):211–219. CrossRefGoogle Scholar
  28. Habte-Tsion H-M, Ge X, Liu B, Xie J, Ren M, Zhou Q, Miao L, Pan L, Chen R (2015a) A deficiency or an excess of dietary threonine level affects weight gain, enzyme activity, immune response and immune-related gene expression in juvenile blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immunol 42(2):439–446. CrossRefPubMedGoogle Scholar
  29. Habte-Tsion H-M, Liu B, Ren M, Ge X, Xie J, Zhou Q, Miao L, Pan L, Chen R (2015b) Dietary threonine requirement of juvenile blunt snout bream (Megalobrama amblycephala). Aquaculture 437:304–311. CrossRefGoogle Scholar
  30. Habte-Tsion H-M, Ren M, Liu B, Ge X, Xie J, Chen R, Zhou Q, Pan L (2015c) Threonine influences the absorption capacity and brush-border enzyme gene expression in the intestine of juvenile blunt snout bream (Megalobrama amblycephala). Aquaculture 448:436–444. CrossRefGoogle Scholar
  31. Habte-Tsion H-M, Ren M, Liu B, Xie J, Ge X, Chen R, Zhou Q, Pan L (2015d) Threonine affects digestion capacity and hepatopancreatic gene expression of juvenile blunt snout bream (Megalobrama amblycephala). Br J Nutr 114(04):533–543. CrossRefPubMedGoogle Scholar
  32. Habte-Tsion H-M, Ren M, Liu B, Ge X, Xie J, Chen R (2016) Threonine modulates immune response, antioxidant status and gene expressions of antioxidant enzymes and antioxidant-immune-cytokine-related signaling molecules in juvenile blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immunol 51:189–199. CrossRefPubMedGoogle Scholar
  33. Harpaz S (2005) L-carnitine and its attributed functions in fish culture and nutrition: a review. Aquaculture 249(1-4):3–21. CrossRefGoogle Scholar
  34. Hasch E, Jarnum S, Tygstrup N (1967) Albumin synthesis rate as a measure of liver function in patients with cirrhosis. Acta Med Scand 182:83–92CrossRefPubMedGoogle Scholar
  35. Infante JZ, Cahu C (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol Part C: Toxicol Pharmacol 130:477–487Google Scholar
  36. Jaroli D, Sharma B (2005) Effect of organophosphate insecticide on the organic constituents in liver of Channa punctatuus. Asian J Exp Sci 19:121–129Google Scholar
  37. Jaworek J (2006) Ghrelin and melatonin in the regulation of pancreatic exocrine secretion and maintaining of integrity. J Physiol Pharmacol 57:83PubMedGoogle Scholar
  38. Kiron V (2012) Fish immune system and its nutritional modulation for preventive health care. Anim Feed Sci Technol 173(1-2):111–133. CrossRefGoogle Scholar
  39. Konturek J, Hengst K, Kulesza E, Gabryelewicz A, Konturek S, Domschke W (1997) Role of endogenous nitric oxide in the control of exocrine and endocrine pancreatic secretion in humans. Gut 40(1):86–91. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kuang S-Y, Xiao WW, Feng L, Liu Y, Jiang J, Jiang WD, Hu K, Li SH, Tang L, Zhou XQ (2012) Effects of graded levels of dietary methionine hydroxy analogue on immune response and antioxidant status of immune organs in juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 32(5):629–636. CrossRefPubMedGoogle Scholar
  41. 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
  42. Li P, Yin Y-L, Li D, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98(02):237–252. CrossRefPubMedGoogle Scholar
  43. Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37(1):43–53. CrossRefPubMedGoogle Scholar
  44. Li W, Feng L, Liu Y, Jiang WD, Kuang SY, Jiang J, Li SH, Tang L, Zhou XQ (2015) Effects of dietary phenylalanine on growth, digestive and brush border enzyme activities and antioxidant capacity in the hepatopancreas and intestine of young grass carp (Ctenopharyngodon idella). Aquac Nutr 21(6):913–925. CrossRefGoogle Scholar
  45. Li M, Lai H, Li Q, Gong S, Wang R (2016) Effects of dietary taurine on growth, immunity and hyperammonemia in juvenile yellow catfish Pelteobagrus fulvidraco fed all-plant protein diets. Aquaculture 450:349–355CrossRefGoogle Scholar
  46. Lin S, Pan Y, Luo L, Luo L (2011) Effects of dietary β-1, 3-glucan, chitosan or raffinose on the growth, innate immunity and resistance of koi (Cyprinus carpio koi). Fish Shellfish Immunol 31(6):788–794. CrossRefPubMedGoogle Scholar
  47. Lindroth P, Mopper K (1979) High performance liquid chromatographic determination of subpicomole amounts of amino acids by precolumn fluorescence derivatization with o-phthaldialdehyde. Anal Chem 51(11):1667–1674. CrossRefGoogle Scholar
  48. Liou AP, Sei Y, Zhao X, Feng J, Lu X, Thomas C, Pechhold S, Raybould HE, Wank SA (2011) The extracellular calcium-sensing receptor is required for cholecystokinin secretion in response to L-phenylalanine in acutely isolated intestinal cells. Am J Physiol Gastrointest Liver Physiol 300(4):G538–G546. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Mambrini M, Kaushik S (1994) Partial replacement of dietary protein nitrogen with dispensable amino acids in diets of Nile tilapia, Oreochromis niloticus. Comp Biochem Physiol A Physiol 109(2):469–477. CrossRefGoogle Scholar
  50. Marammazi JG, Yaghoubi M, Safari O, Peres H, Mozanzadeh MT (2017) Establishing the optimum dietary essential amino acids pattern for silvery-black porgy (Sparidentex hasta) juveniles by deletion method. Aquac Nutr 00:1–9Google Scholar
  51. Mensinger AF, Walsh PJ, Hanlon RT (2005) Blood biochemistry of the oyster toadfish. J Aquat Anim Health 17(2):170–176. CrossRefGoogle Scholar
  52. Metón Teijeiro I, Salgado Martín MdC, Anemaet IG, González JD, Fernández González FJ, Vázquez Baanante MI (2015) Alanine aminotransferase: a target to improve utilisation of dietary nutrients in aquaculture. Recent Advances in Pharmaceutical Sciences V, 2015, Research Signpost Editors: Diego Muñoz Torrero, M Pilar Vinardell & Javier Palazón ISBN: 978–81–308-0561-0 Chapter 9, p 133–148Google Scholar
  53. Molero X, Guarner F, Salas A, Mourelle M, Puig V, Malagelada JR (1995) Nitric oxide modulates pancreatic basal secretion and response to cerulein in the rat: effects in acute pancreatitis. Gastroenterology 108(6):1855–1862. CrossRefPubMedGoogle Scholar
  54. Mozanzadeh MT, Marammazi JG, Yaghoubi M, Agh N, Pagheh E, Gisbert E (2017) Macronutrient requirements of silvery-black porgy (Sparidentex hasta): a comparison with other farmed sparid species. Aust Fish 2:5CrossRefGoogle Scholar
  55. Nayak J, Nair P, Mathew S, Ammu K (2004) A study on the intestinal lipase of Indian major carp Labeo rohita. Asian Fish Sci 17:333–339Google Scholar
  56. NRC (1993) Nutrient Requirements of Fish. The National Academies Press, Washington, DC.Google Scholar
  57. NRC (2011) Nutrient requirements of fish and shrimp. The National Academies Press, Washington, DCGoogle Scholar
  58. Pavlidis M, Mylonas C (2011) Sparidae: biology and aquaculture of gilthead sea bream and other species. Blackwell publishing Ltd, UK. CrossRefGoogle Scholar
  59. Peres H, Oliva-Teles A (2009) The optimum dietary essential amino acid profile for gilthead seabream (Sparus aurata) juveniles. Aquaculture 296(1-2):81–86. CrossRefGoogle Scholar
  60. Péres A, Cahu C, Infante JZ (1997) Dietary spermine supplementation induces intestinal maturation in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 16(6):479–485. CrossRefGoogle Scholar
  61. Peres H, Santos S, Oliva Teles A (2013) Selected plasma biochemistry parameters in gilthead seabream (Sparus aurata) juveniles. J Appl Ichthyol 29:630–636CrossRefGoogle Scholar
  62. Peres H, Santos S, Oliva-Teles A (2014) Blood chemistry profile as indicator of nutritional status in European seabass (Dicentrarchus labrax). Fish Physiol Biochem 40:1339–1347CrossRefPubMedGoogle Scholar
  63. Polgar L (2005) The catalytic triad of serine peptidases. Cell Mol Life Sci CMLS 62(19-20):2161–2172. CrossRefPubMedGoogle Scholar
  64. Popović NT, Strunjak-Perović I, Čož-Rakovac R, Hacmanjek M (2006) Plasma metabolites and enzymes of bluefin tuna, Thunnus thynnus and liver histology. Period Biol 108:127–131Google Scholar
  65. Rahimnejad S, Lee K-J (2014a) Dietary arginine requirement of juvenile red sea bream Pagrus major. Aquaculture 434:418–424. CrossRefGoogle Scholar
  66. Rahimnejad S, Lee K-J (2014b) Dietary isoleucine influences non-specific immune response in juvenile olive flounder (Paralichthys olivaceus). Turk J Fish Aquat Sci 14:853–862CrossRefGoogle Scholar
  67. Ramaswamy M, Thangavel P, Selvam NP (1999) Glutamic oxaloacetic transaminase(GOT) and glutamic pyruvic transaminase(GPT) enzyme activities in different tissues of Sarotherodon mossambicus (Peters) exposed to a carbamate pesticide, carbaryl. Pestic Sci 55:1217–1221CrossRefGoogle Scholar
  68. Riche M (2007) Analysis of refractometry for determining total plasma protein in hybrid striped bass (Morone chrysops × M. saxatilis) at various salinities. Aquaculture 264:279–284. CrossRefGoogle Scholar
  69. Rønnestad I, Kamisaka Y, Conceição L, Morais S, Tonheim S (2007) Digestive physiology of marine fish larvae: hormonal control and processing capacity for proteins, peptides and amino acids. Aquaculture 268:82–97CrossRefGoogle Scholar
  70. Rosalki S, Mcintyre N (1999) Biochemical investigations in the management of liver disease. Oxford textbook of clinical. Hepatology 2:503–521Google Scholar
  71. Sidransky H, Baba T (1960) Chemical pathology of acute amino acid deficiencies. 3. Morphologic and biochemical changes in young rats fed valine-or lysine-devoid diets. J Nutr 70(4):463–483. CrossRefPubMedGoogle Scholar
  72. Storebakken T, Shearer KD, Roem AJ (2000) Growth, uptake and retention of nitrogen and phosphorus, and absorption of other minerals in Atlantic salmon Salmo salar fed diets with fish meal and soy–protein concentrate as the main sources of protein. Aquac Nutr 6(2):103–108. CrossRefGoogle Scholar
  73. Tang L Wang GX, Jiang J, Feng L, Yang L, et al (2009) Effect of methionine on intestinal enzymes activities, microflora and humoral immune of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 15(5):477–483.
  74. Tang L Tang L, Feng L, Sun CY, Chen GF, Jiang WD, Hu K et al (2013) Effect of tryptophan on growth, intestinal enzyme activities and TOR gene expression in juvenile Jian carp (Cyprinus carpio var. Jian): studies in vivo and in vitro. Aquaculture 412:23–33Google Scholar
  75. Vaquero E, Molero X, Puig-Divi V, Malagelada J (1998) Contrasting effects of circulating nitric oxide and nitrergic transmission on exocrine pancreatic secretion in rats. Gut 43(5):684–691. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Von der Decken A, Lied E (1993) Metabolic effects on growth and muscle of soya-bean protein feeding in cod (Gadus morhua). Br J Nutr 69(03):689–697. CrossRefPubMedGoogle Scholar
  77. Wagner T, Congleton JL (2004) Blood chemistry correlates of nutritional condition, tissue damage, and stress in migrating juvenile chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 61(7):1066–1074. CrossRefGoogle Scholar
  78. Wang T, Fuller M (1989) The optimum dietary amino acid pattern for growing pigs. Br J Nutr 62(01):77–89. CrossRefPubMedGoogle Scholar
  79. Wen H, Feng L, Jiang W, Liu Y, Jiang J, Li S, Tang L, Zhang Y, Kuang S, Zhou X (2014) Dietary tryptophan modulates intestinal immune response, barrier function, antioxidant status and gene expression of TOR and Nrf2 in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 40(1):275–287. CrossRefPubMedGoogle Scholar
  80. Worthington C (1991) Worthington enzyme manual related biochemical. Freehold, New JerseyGoogle Scholar
  81. Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37(1):1–17. CrossRefPubMedGoogle Scholar
  82. Wu G, Meininger CJ (2000) Arginine nutrition and cardiovascular function. J Nutr 130(11):2626–2629. CrossRefPubMedGoogle Scholar
  83. Yaghoubi M, Mozanzadeh M, Marammazi J, Safari O, Gisbert E (2017) Effects of dietary essential amino acid deficiencies on the growth performance and humoral immune response in silvery-black porgy (Sparidentex hasta) juveniles. Aquac Res 00:1–13Google Scholar
  84. Yamamoto Y (1981) Determination of toxicity by biochemical method. In: Fishes as Laboratory. pp 568–574Google Scholar
  85. Yan L, Qiu-Zhou X (2006) Dietary glutamine supplementation improves structure and function of intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture 256(1-4):389–394. CrossRefGoogle Scholar
  86. Zhao B et al (2012a) Effects of dietary histidine levels on growth performance, body composition and intestinal enzymes activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 18(2):220–232. CrossRefGoogle Scholar
  87. Zhao J et al (2012b) Effects of dietary isoleucine on growth, the digestion and absorption capacity and gene expression in hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture 368:117–128CrossRefGoogle Scholar
  88. Zhao J, Liu Y, Jiang J, Wu P, Jiang W, Li S, Tang L, Kuang S, Feng L, Zhou X (2013) Effects of dietary isoleucine on the immune response, antioxidant status and gene expression in the head kidney of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 35(2):572–580. CrossRefPubMedGoogle Scholar
  89. Zhou F, Xiong W, Xiao JX, Shao QJ, Bergo ON, Hua Y, Chai X (2010) Optimum arginine requirement of juvenile black sea bream, Sparus macrocephalus. Aquac Res 41:e418–e430Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Morteza Yaghoubi
    • 1
  • Mansour Torfi Mozanzadeh
    • 1
  • Omid Safari
    • 2
  • Jasem G. Marammazi
    • 1
  1. 1.Agriculture Research, Education and Extension, Iran Fisheries Research Organization (IFRO)South Iran Aquaculture Research CenterAhwazIran
  2. 2.Department of Fisheries, Faculty of Natural Resources and EnvironmentFerdowsi University of MashhadKhorasan RazaviIran

Personalised recommendations