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Dietary nitrogen and fish welfare

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Abstract

Little research has been done in optimizing the nitrogenous fraction of the fish diets in order to minimize welfare problems. The purpose of this review is to give an overview on how amino acid (AA) metabolism may be affected when fish are under stress and the possible effects on fish welfare when sub-optimal dietary nitrogen formulations are used to feed fish. In addition, it intends to evaluate the current possibilities, and future prospects, of using improved dietary nitrogen formulations to help fish coping with predictable stressful periods. Both metabolomic and genomic evidence show that stressful husbandry conditions affect AA metabolism in fish and may bring an increase in the requirement of indispensable AA. Supplementation in arginine and leucine, but also eventually in lysine, methionine, threonine and glutamine, may have an important role in enhancing the innate immune system. Tryptophan, as precursor for serotonin, modulates aggressive behaviour and feed intake in fish. Bioactive peptides may bring important advances in immunocompetence, disease control and other aspects of welfare of cultured fish. Fishmeal replacement may reduce immune competence, and the full nutritional potential of plant-protein ingredients is attained only after the removal or inactivation of some antinutritional factors. This review shows that AA metabolism is affected when fish are under stress, and this together with sub-optimal dietary nitrogen formulations may affect fish welfare. Furthermore, improved dietary nitrogen formulations may help fish coping with predictable stressful events.

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References

  • Ai QH, Mai KS, Zhang L, Tan BP, Zhang WB, Xu W, Li HT (2007) Effects of dietary beta-1, 3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol 22:394–402

    Article  PubMed  CAS  Google Scholar 

  • Aksnes A, Mundheim H, Toppe J, Albrektsen S (2008) The effect of dietary hydroxyproline supplementation on salmon (Salmo salar L.) fed high plant protein diets. Aquaculture 275:242–249

    Article  CAS  Google Scholar 

  • Aldegunde M, Garcia J, Soengas JL, Rozas G (1998) Uptake of tryptophan into brain of rainbow trout (Oncorhynchus mykiss). J Exp Zool 282:285–289

    Article  CAS  Google Scholar 

  • Aldegunde M, Soengas JL, Rozas G (2000) Acute effects of l-tryptophan hydroxylation rate in brain regions (hypothalamus and medulla) of rainbow trout (Oncorhynchus mykiss). J Exp Zool 286:131–135

    Article  PubMed  CAS  Google Scholar 

  • Alves RN, Cordeiro O, Silva TS, Richard N, de Vareilles M, Marino G, Di Marco P, Rodrigues PM, Conceição LEC (2010) Metabolic molecular indicators of chronic stress in gilthead seabream (Sparus aurata) using comparative proteomics. Aquaculture 299:57–66

    Article  CAS  Google Scholar 

  • Anderson RL, Wolf WJ (1995) Compositional changes in trypsin inhibitors, phytic acid, saponins and isoflavones related to soybean processing. J Nutr 125:581S–588S

    PubMed  CAS  Google Scholar 

  • Anderson WG, Takei Y, Hazon N (2002) Osmotic and volaemic effects on drinking rate in elasmobranch fish. J Exp Biol 205:1115–1122

    PubMed  Google Scholar 

  • Aragão C, Corte-Real J, Costas B, Dinis MT, Conceição LEC (2008) Stress response and changes in amino acid requirements in Senegalese sole (Solea senegalensis Kaup 1858). Amino Acids 34:143–148

    Article  PubMed  CAS  Google Scholar 

  • Aragão C, Costas B, Vargas-Chacoff L, Ruiz-Jarabo I, Dinis MT, Mancera JM, Conceição LEC (2010) Changes in plasma amino acid levels in a euryhaline fish exposed to different environmental salinities. Amino Acids 38:311–317

    Article  PubMed  CAS  Google Scholar 

  • Armand A, Launay T, Pariset C, Della Gaspera B, Charbonnier F, Chanoine C (2003) Injection of FGF6 accelerates regeneration of the soleus muscle in adult mice. Bioch Biophys Acta 1642:97–105

    Article  CAS  Google Scholar 

  • Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235

    Article  Google Scholar 

  • Bakke S, Jordal A-EO, Gomez-Requeni P, Verri T, Kousoulaki K, Aksnes A, Rønnestad I (2010) Dietary protein hydrolysates and free amino acids affect the spatial expression of peptide transporter PepT1 in the digestive tract of Atlantic cod (Gadus morhua). Comp Biochem Physiol B-Biochem Mol Biol 156:48–55

    Article  PubMed  CAS  Google Scholar 

  • Bass J, Oldham J, Sharma M, Kambadur R (1999) Growth factors controlling muscle development. Domest Anim Endocrin 17:191–197

    Google Scholar 

  • Bauchart C, Morzel M, Chambon C, Mirand PP, Reynes C, Buffiere C, Redmond D (2007) Peptides reproducibly released by in vivo digestion of beef meat and trout flesh in pigs. Br J Nutr 98:1187–1195

    Article  PubMed  CAS  Google Scholar 

  • Bernier NJ (2006) The corticotropin-releasing factor system as a mediator of the appetite-suppressing effects of stress in fish. Gen Comp Endocrinol 146:45–55

    Article  PubMed  CAS  Google Scholar 

  • Blazer VS (1992) Nutrition and disease resistance in fish. Annu Rev Fish Dis 2:309–323

    Article  Google Scholar 

  • Boadle-Biber MC (1993) Regulation of serotonin synthesis. Prog Biophys Mol Biol 60:1–15

    Article  PubMed  CAS  Google Scholar 

  • Bransden MP, Carter CG, Nowak BF (2001) Effects of dietary protein source on growth, immune function, blood chemistry and disease resistance of Atlantic salmon (Salmo salar L.) parr. Anim Sci 73:105–113

    CAS  Google Scholar 

  • Brodeur JC, Peck LS, Johnston LA (2002) Feeding increases MyoD and PCNA expression in myogenic progenitor cells of Notothenia coriiceps. J Fish Biol 60:1475–1485

    Google Scholar 

  • Buentello JA, Gatlin DM (2001) Effects of elevated dietary arginine on resistance of channel catfish to exposure to Edwardsiella ictaluri. J Aquat Anim Health 13:194–201

    Article  Google Scholar 

  • Buentello JA, Reyes-Becerril M, Romero-Geraldo Mde J, Ascencio-Valle Fde J (2007) Effects of dietary arginine on hematological parameters and innate immune function of channel catfish. J Aquat Anim Health 19:195–203

    Article  PubMed  Google Scholar 

  • 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 72:277–288

    Article  PubMed  CAS  Google Scholar 

  • Chatzifotis S, Polemitou I, Divanach P, Antonopoulou E (2008) Effect of dietary taurine supplementation on growth performance and bile salt activated lipase activity of common dentex, Dentex dentex, fed a fish meal/soy protein concentrate-based diet. Aquaculture 275:201–208

    Article  CAS  Google Scholar 

  • Clements KD, Raubenheimer D (2006) Feeding and nutrition. In: Evans DH, Claiborne JB (eds) The Physiology of Fishes, 3rd edn. CRC Press, Boca Raton, pp 47–81

    Google Scholar 

  • Clotfelter ED, O’Hare EP, McNitt MM, Carpenter RE, Summers CH (2007) Serotonin decreases aggression via 5-HT1A receptors in the fighting fish Betta splendens. Pharmacol Biochem Behav 87:222–231

    Article  PubMed  CAS  Google Scholar 

  • Conceição LEC, Houlihan DF, Verreth JAJ (1997) Fast growth, protein turnover and costs of protein metabolism in yolk-sac larvae of the African catfish (Clarias gariepinus). Fish Physiol Biochem 16:291–302

    Article  Google Scholar 

  • Conceição LEC, Skjermo J, Skjåk-Bræk G, Verreth JAJ (2001) Effect of an immunostimulating alginate on protein turnover of turbot (Scophthalmus maximus L.) larvae. Fish Physiol Biochem 24:207–212

    Article  Google Scholar 

  • Conceição LEC, Morais SJ, Dinis MT, Rønnestad I (2008) Tracer studies in fish larvae. In: Cyrino JEP, Bureau D, Kapoor BG (eds) Feeding and digestive functions in fishes. Science Publishers, Enfield, New Hampshire, pp 349–392

    Google Scholar 

  • Costas B, Aragão C, Mancera JM, Dinis MT, Conceição LEC (2008) High stocking density induces crowding stress and affects amino acid metabolism in Senegalese sole Solea senegalensis (Kaup 1858) juveniles. Aquacult Res 39:1–9

    Article  CAS  Google Scholar 

  • Costas B, Aragão C, Soengas JL, Míguez JM, Rema P, Dias J, Afonso A, Conceição LEC (2011a) Effects of dietary amino acids and repeated handling on stress response and brain monoaminergic neurotransmitters in Senegalese sole (Solea senegalensis Kaup, 1858) juveniles. Comp Biochem Physiol A. doi:10.1016/j.cbpa.2011.08.014

  • Costas B, Conceição LEC, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011b) Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: effects on non-specific immune parameters, plasma free amino acids and energy metabolism. Aquaculture 316:68–76

    Article  CAS  Google Scholar 

  • Costas B, Aragão C, Ruiz-Jarabo I, Vargas-Chacoff L, Arjona FJ, Dinis MT, Mancera JM, Conceição LEC (2011c) Feed deprivation in Senegalese sole (Solea senegalensis, Kaup 1858) juveniles: effects on blood plasma metabolites and free amino acid levels. Fish Physiol Biochem 37:495–504

    Article  PubMed  CAS  Google Scholar 

  • Costas B, Aragão C, Ruiz-Jarabo I, Vargas-Chacoff L, Arjona FJ, Mancera JM, Dinis MT, Conceição LEC (2011d) Different environmental temperatures affect amino acid metabolism in the eurytherm teleost Senegalese sole (Solea senegalensis Kaup, 1858) as indicated by changes in plasma metabolites. Amino Acids. doi:10.1007/s00726-011-1082-0

  • Costas B, Conceição LEC, Dias J, Novoa B, Figueras A, Afonso A (2011e). Dietary arginine and repeated handling increase disease resistance and modulate innate immune mechanisms of Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol. doi:10.1016/j.fsi.2011.07.024

  • Dawkins MS (1990) From an animal’s point of view: motivation, fitness and animal welfare. Behav Brain Sci 13:1–161

    Article  Google Scholar 

  • Dawkins MS (2001) Who needs animal suffering? Anim Welf 10:S19–S31

    Google Scholar 

  • de Pedro N, Pinillos ML, Valenciano AI, Alonso-Bedate M, Delgado MJ (1998) Inhibitory effect of serotonin on feeding behavior in goldfish: involvement of CRF. Peptides 19:505–511

    Article  PubMed  Google Scholar 

  • Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S

    PubMed  CAS  Google Scholar 

  • Duarte J, Vinderola G, Ritz B, Perdigo G, Matar C (2006) Immunomodulating capacity of commercial fish protein hydrolysate for diet supplementation. Immunobiology 211:341–350

    Article  PubMed  CAS  Google Scholar 

  • Duncan IJH (2005) Science-based assessment of animal welfare: Farm animals. Rev Sci Tech Off Int Epiz 24:483–492

    CAS  Google Scholar 

  • Espe M, Lemme A, Petri A, El-Mowafi A (2006) Can Atlantic salmon grow on diets devoid of fish meal? Aquaculture 255:255–262

    Article  CAS  Google Scholar 

  • Fauconneau B, Paboeuf G (2000) Effect of fasting and refeeding on in vitro muscle cell proliferation in rainbow trout (Oncorhynchus mykiss). Cell Tissue Res 3101:459–463

    Article  Google Scholar 

  • Fernstrom JD, Wurtman RJ (1997) Brain serotonin content: physiological regulation by plasma neutral amino acids (reprinted). Obes Res 5:377–380

    PubMed  CAS  Google Scholar 

  • Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227

    Article  CAS  Google Scholar 

  • Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579

    Article  CAS  Google Scholar 

  • Gaylord TG, Barrows FT, Teague AM, Johansen KA, Overturf KE, Shephed B (2007) Supplementation of taurine and methionine to all-plant protein diets for rainbow trout (Oncorhynchus mykiss). Aquaculture 269:514–524

    Article  CAS  Google Scholar 

  • Gilbert ER, Wong EA, Webb KE Jr (2008) Peptide absorption and utilization: implications for animal nutrition and health. J Anim Sci 86:2135–2155

    Article  PubMed  CAS  Google Scholar 

  • Gildberg A, Bogwald J, Johansen A, Stenberg E (1996) Isolation of acid peptide fractions from a fish protein hydrolysate with strong stimulatory effect on Atlantic Salmon (Salmo salar) head kidney leucocytes. Comp Biochem Physiol B 114:97–101

    Article  Google Scholar 

  • Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Requeni P, Mingarro M, Calduch-Giner JA, Médale F, Martin SAM, Houlihan DF, Kaushik S, Pérez-Sánchez J (2004) Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232:493–510

    Article  CAS  Google Scholar 

  • Gouillou-Coustans MF, Fournier V, Métailler R, Vachot C, Desbruyères E, Huelvan C, Moriceau J, Le Delliou H, Kaushik SJ (2002) Dietary arginine degradation is a major pathway in ureagenesis in turbot (Psetta Maxima). Comp Biochem Physiol A 132:305–319

    Article  CAS  Google Scholar 

  • Grimble RF, Grimble GK (1998) Immunonutrition: role of sulfur amino acids, related amino acids, and polyamines. Nutrition 14:605–610

    Article  PubMed  CAS  Google Scholar 

  • Harpaz S (2005) L-carnitine and its attributed functions in fish culture and nutrition—a review. Aquaculture 249:3–21

    Article  CAS  Google Scholar 

  • Hartmann R, Meisel H (2007) Food-derived peptides with biological activity: from research to food applications. Curr Opin Biotechnol 18:163–169. doi:10.1016/j.copbio.2007.01.013

    Google Scholar 

  • Henry Y, Sève B, Mounier A, Ganier P (1996) Growth performance and brain neurotransmitters in pigs as affected by tryptophan, protein, and sex. J Anim Sci 74:2700–2710

    PubMed  CAS  Google Scholar 

  • Herrero MJ, Martínez FJ, Míguez JM, Madrid JA (2007) Response of plasma and gastrointestinal melatonin, plasma cortisol and activity rhythms of European sea bass (Dicentrarchus labrax) to dietary supplementation with tryptophan and melatonin. J Comp Physiol B 177:319–326

    Article  PubMed  CAS  Google Scholar 

  • Höglund E, Balm PH, Winberg S (2002) Stimulatory and inhibitory effects of 5-HT1A receptors on adrenocorticotropic hormone and cortisol secretion in a teleost fish, the Arctic charr (Salvelinus alpinus). Neurosci Lett 324:193–196

    Article  PubMed  Google Scholar 

  • Höglund E, Bakke MJ, Øverli Ø, Winberg S, Nilsson GE (2005) Suppression of aggressive behaviour in juvenile Atlantic cod (Gadus morhua), by l-tryptophan supplementation. Aquaculture 249:525–531

    Article  CAS  Google Scholar 

  • Höglund E, Sorensen C, Bakke MJ, Nilsson GE, Øverli Ø (2007) Attenuation of stress-induced anorexia in brown trout (Salmo trutta) by pre-treatment with dietary l-tryptophan. Br J Nutr 97:786–789

    Article  PubMed  CAS  Google Scholar 

  • Houlihan DF (1991) Protein turnover in ectotherms and implications for energetics. In: Gilles R (ed) Advances in comparative and environmental biology 7. Springer, Berlin, pp 1–43

    Google Scholar 

  • Houlihan DF, Costello MJ, Secombes CJ, Stagg R, Brechin J (1994) Effects of sewage sludge exposure on growth, feeding and protein synthesis of dab Limanda limanda L. Mar Environ Res 37:331–353

    Article  CAS  Google Scholar 

  • Hseu JR, Lu FI, Su HM, Wang LS, Tsai CL, Hwang PP (2003) Effect of exogenous tryptophan on cannibalism, survival and growth in juvenile grouper, Epinephelus coioides. Aquaculture 218:251–263

    Article  CAS  Google Scholar 

  • Ip YK, Chew SF, Randall DJ (2001) Ammonia toxicity, tolerance, and excretion. In: Wright PA, Anderson AJ (eds) Nitrogen excretion. Fish physiology, vol 20. Academic Press Inc., San Diego, pp 109–148

    Chapter  Google Scholar 

  • Israf DA, Coop RL, Stevenson LM, Jones DG, Jackson F, Jackson E, MacKellar A, Huntley JF (1996) Dietary protein influences upon immunity to Nematodirus battus infection in lambs. Vet Parasitol 61:273–286

    Article  PubMed  CAS  Google Scholar 

  • Johnston W, Atkinson JL, Hilton JW, Were KE (1990) Effect of dietary tryptophan on plasma and brain tryptophan, brain serotonin and brain 5-hydroxyindoleacetic acid in rainbow trout. J Nut Biochem 1:49–54

    Article  CAS  Google Scholar 

  • Jørgensen ALW, Juul-Madsen HR, Stagsted J (2010) Colostrum and bioactive, colostral peptides differentially modulate the innate immune response of intestinal epithelial cells. J Pept Sci 16:21–30. doi:10.1002/psc.1190

    Google Scholar 

  • Kiessling AH, Johansson L, Kiessling JH (1990) Effect of starvation on rainbow trout muscle. Acta Agr Scand 40:309–324

    Article  CAS  Google Scholar 

  • Kim SK, Takeuchi T, Yokoyama M, Murata Y (2003) Effect of dietary supplementation with taurine, β-alanine, and GABA on the growth of juvenile and fingerling Japanese flounder Paralichthys olivaceus. Fish Sci 69:242–248

    Article  CAS  Google Scholar 

  • Kim SK, Matsunari H, Takeuchi T, Yokoyama M, Furuita H, Murata Y, Goto T (2008) Comparison of taurine biosynthesis ability between juveniles of Japanese flounder and common carp. Amino Acids 35:161–168

    Article  PubMed  CAS  Google Scholar 

  • Kiørboe T, Munk P, Richardson K (1987) Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Mar Ecol Prog Ser 40:1–10

    Article  Google Scholar 

  • Kirchner S, McDaniel NK, Sugiura SH, Soteropoulos P, Tian B, Fletcher J, Ferraris RP (2007) Salmonid microarrays identify intestinal genes that reliably monitor P deficiency in rainbow trout aquaculture. Anim Genet 38:319–331

    Article  PubMed  CAS  Google Scholar 

  • Kitts DD, Weiler K (2003) Bioactive proteins and peptides from food sources. Applications of bioprocesses used in isolation and recovery. Curr Pharm Des 9:1309–1323

    Article  PubMed  CAS  Google Scholar 

  • Korhonen H, Pihlanto A (2006) Bioactive peptides: production and functionality. Int Dairy J 16:945–960. doi:10.1016/j.idairyj.2005.10.015

    Article  CAS  Google Scholar 

  • Krogdahl A, Lee TB, Olli JJ (1994) Soybean protease inhibitors affect intestinal trypsin activities and amino acid digestibilities in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A 107:215–219

    Article  Google Scholar 

  • Langar H, Guillaume J, Metailler R, Fauconneau B (1993) Augmentation of protein-synthesis and degradation by poor dietary amino-acid balance in European sea bass (Dicentrarchus labrax). J Nutr 123:1754–1761

    PubMed  CAS  Google Scholar 

  • Leenhouwers JI, Ortega RC, Verreth JAJ, Schrama JW (2007) Digesta characteristics in relation to nutrient digestibility and mineral absorption in Nile tilapia (Oreochromis niloticus L.) fed cereal grains of increasing viscosity. Aquaculture 273:556–565

    Article  CAS  Google Scholar 

  • Lefèvre F, Bugeon J, Aupérin B, Aubin J (2008) Rearing oxygen level and slaughter stress effects on rainbow trout flesh quality. Aquaculture 284:81–89

    Article  CAS  Google Scholar 

  • Lepage O, Tottmar O, Winberg S (2002) Elevated dietary intake of l-tryptophan counteracts the stress-induced elevation of plasma cortisol in rainbow trout (Oncorhynchus mykiss). J Exp Biol 205:3679–3687

    PubMed  CAS  Google Scholar 

  • Lepage O, Vílchez IM, Pottinger TG, Winberg S (2003) Time-course of the effect of dietary l-tryptophan on plasma cortisol levels in rainbow trout Oncorhynchus mykiss. J Exp Biol 206:3589–3599

    Article  PubMed  Google Scholar 

  • Lepage O, Larson ET, Mayer I, Winberg S (2005) Tryptophan affects both gastrointestinal melatonin production and interrenal activity in stressed and nonstressed rainbow trout. J Pineal Res 38:264–271

    Article  PubMed  CAS  Google Scholar 

  • Leroith D, Bondy C, Yakar S, Liu JL, Butler A (2001) The somatomedin hypothesis. Endocr Rev 22:53–74

    Article  CAS  Google Scholar 

  • Li P, Yin Y, Li D, Kim WK, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237–252

    Article  PubMed  CAS  Google Scholar 

  • Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53

    Article  PubMed  CAS  Google Scholar 

  • Lin TH, Yang RS, Tang CH, Wu MY, Fu WM (2008) Regulation of the maturation of osteoblasts and osteoclastogenesis by glutamate. Eur J Pharmacol 589:37–44

    Article  PubMed  CAS  Google Scholar 

  • Madureira AR, Tavares T, Gomes AMP, Pintado ME, Malcata FX (2010) Invited review: physiological properties of bioactive peptides obtained from whey proteins. J Dairy Sci 93:437–455

    Article  PubMed  CAS  Google Scholar 

  • Martin SAM, Vilhelmsson O, Médale F, Watt P, Kaushik S, Houlihan DF (2003) Proteomic sensitivity to dietary manipulations in rainbow trout. Biochim Biophys Acta 1651:17–29

    PubMed  CAS  Google Scholar 

  • Melcion JP, Van der Poel AFB (1993) Process technology and antinutritional factors: principles, adequacy and process optimization. In: Van der Poel AFB, Huisman J, Saini HS (eds) Recent advances in antinutritional factors in legume seeds. EAAP Publication, Wageningen, The Netherlands, pp 419–434

    Google Scholar 

  • Miczek KA, Fish EW (2005) Monoamines, GABA, glutamate and aggression. In: Nelson RJ (ed) Biology of aggression. Oxford University Press, Oxford

    Google Scholar 

  • Milligan CL (1997) The role of cortisol in amino acid mobilization and metabolism following exhaustive exercise in rainbow trout (Oncorhynchus mykiss Walbaum). Fish Physiol Biochem 16:1119–1128

    Article  Google Scholar 

  • Mommsen TP (2001) Paradigms of growth in fish. Comp Biochem Physiol B 129:207–219

    Article  PubMed  CAS  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

    Article  Google Scholar 

  • Mommsen TP, Busby ER, von Schalburg KR, Evans JC, Osachoff HL, Elliott ME (2003) Glutamine synthetase in tilapia gastrointestinal tract: zonation, cDNA and induction by cortisol. J Comp Physiol B 173:419–427

    Article  PubMed  CAS  Google Scholar 

  • Montero D, Tort L, Izquierdo MS, Robaina L, Vergara JM (1998) Depletion of serum alternative complement pathway activity in gilthead seabream caused by alpha-tocopherol and n-3 HUFA dietary deficiencies. Fish Physiol Biochem 18:399–407

    Article  CAS  Google Scholar 

  • Morales AE, Cardenete G, Abellán E, García-Rejón L (2005) Stress-related physiological responses to handling in common dentex (Dentex dentex Linnaeus, 1758). Aquacult Res 36:33–40

    Article  Google Scholar 

  • Musaro A, McCullagh KJ, Naya FJ, Olson EN, Rosenthal N (1999) IGF-I induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATcl. Nature 400:81–585

    Article  CAS  Google Scholar 

  • Neji H, Naimi N, Lallier R, de la Noue J (1993) Relationships between feeding, hypoxia, digestibility and experimentally induced furunculosis in rainbow trout. In: Kaushik SJ, Luquet P (eds) Fish nutrition in practice. Institut National de la Recherche Agronomique, Paris, pp 187–197

    Google Scholar 

  • Norton WH, Folchert A, Bally-Cuif L (2008) Comparative analysis of serotonin receptor (HTR1A/HTR1B families) and transporter (slc6a4a/b) gene expression in the zebrafish brain. J Comp Neurol 511:521–542

    Article  PubMed  CAS  Google Scholar 

  • Øverli Ø, Pottinger TG, Carrick TR, Øverli E, Winberg S (2001) Brain monoaminergic activity in rainbow trout selected for high and low stress responsiveness. Brain Behav Evol 57:214–224

    Article  PubMed  Google Scholar 

  • Panserat S, Kolditz C, Richard N, Plagnes-Juan E, Piumi F, Esquerré D, Médale F, Corraze G, Kaushik S (2008) Hepatic gene expression profiles in juvenile rainbow trout (Oncorhynchus mykiss) fed fishmeal or fish oil-free diets. Br J Nutr 28:1–15

    Google Scholar 

  • Papoutsoglou SE, Karakatsouli N, Chiras G (2005) Dietary l-tryptophan and tank colour effects on growth performance of rainbow trout (Oncorhynchus mykiss) juveniles reared in a recirculating water system. Aquac Eng 32:277–284

    Article  Google Scholar 

  • Peremans K, Audenaert K, Blanckart P, Jacobs F, Coopman F, Verschooten F, Van Bree H, Van Heeringen C, Mertens J, Slegers G, Dierckx R (2002) Effects of aging on brain perfusion and serotonin-2A receptor binding in the normal canine brain measured with single photon emission tomography. Prog Neuropsychopharmacol Biol Psychiatry 26:1393–1404

    Article  PubMed  CAS  Google Scholar 

  • Phang JM, Donald SP, Pandhare J, Liu Y (2008) The metabolism of proline, as a stress substrate, modulates carcinogenic pathways. Amino Acids 35:681–690

    Article  PubMed  CAS  Google Scholar 

  • Pickering AD (1998) Stress responses of farmed fish. In: Black K, Pickering A (eds) Biology of farmed fish. Sheffield Academic Press, Sheffield, pp 222–238

    Google Scholar 

  • Pinto W, Aragão C, Soares F, Dinis MT, Conceição LEC (2007) Growth, stress response and free amino acid levels in Senegalese sole (Solea senegalensis Kaup 1858) chronically exposed to exogenous ammonia. Aquacult Res 38:1198–1204

    Article  CAS  Google Scholar 

  • Prunet P, Cairns MT, Winberg S, Pottinger TG (2008) Functional genomics of stress responses in fish. Rev Fish Sci 16:157–166

    Article  CAS  Google Scholar 

  • Refstie S, Svihus B, Shearer KD, Storebakken T (1999) Nutrient digestibility in Atlantic salmon and broiler chickens related to viscosity and non-starch polysaccharide content in different soybean products. Anim Feed Sci Technol 79:331–345

    Article  CAS  Google Scholar 

  • Refstie S, Landsverk T, Bakke-McKellep AM, Ringø E, Sundby A, Shearer CD, Krogdahl Å (2006) Digestive capacity, intestinal morphology, and microflora of 1-year and 2-year old Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. Aquaculture 261:269–284

    Article  Google Scholar 

  • Reyes-Becerril M, Ascencio-Valle F, Tovar-Ramírez D, Meseguer J, Esteban MA (2011) Effects of polyamines on cellular innate immune response and the expression of immune-relevant genes in gilthead seabream leucocytes. Fish Shellfish Immunol 30:248–254

    Article  PubMed  CAS  Google Scholar 

  • Romarheim OH, Aslaksen MA, Storebakken T, Krogdahl A, Skrede A (2005) Effect of extrusion on trypsin inhibitor activity and nutrient digestibility of diets based on fish meal, soybean meal and white flakes. Arch Anim Nutr 59:365–375

    Article  PubMed  CAS  Google Scholar 

  • Romeo J, Warnberg J, Gomez-Martinez S, Diaz LE, Marcos A (2008) Neuroimmunomodulation by nutrition in stress situations. Neuroimmunomodulation 15:165–169

    Article  PubMed  CAS  Google Scholar 

  • Rumsey GL, Siwicki AK, Anderson DP, Bowser PR (1994) Effect of soybean protein on serological response, non-specific defense mechanisms, growth, and protein utilization in rainbow trout. Vet Immunol Immunopathol 41:323–339

    Article  PubMed  CAS  Google Scholar 

  • Saeij JPJ, van Muiswinkel WB, van de Meent M, Amaral C, Wiegertjes GF (2003) Different capacities of carp leukocytes to encounter nitric oxide-mediated stress: a role for the intracellular reduced glutathione pool. Dev Comp Immunol 27:555–568

    Article  PubMed  CAS  Google Scholar 

  • Saha N, Dutta S, Bhattacharjee A (2002) Role of amino acid metabolism in an air-breathing catfish, Clarias batrachus in response to exposure to a high concentration of exogenous ammonia. Comp Biochem Physiol B 133:235–250

    Article  PubMed  Google Scholar 

  • Santigosa E, Sánchez J, Médale F, Kaushik S, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282:68–74

    Article  CAS  Google Scholar 

  • Sauvant D, Perez J-M, Tran G (2004) Tables of composition and nutritive value of feed materials. Pigs, poultry, cattle, sheep, goats, rabbits, horses, fish. INRA Editions Versailles

  • Shamblott MJ, Chen TT (1992) Identification of a second insulin-like growth factor in a fish species. PNAS 89:8913–8917

    Article  PubMed  CAS  Google Scholar 

  • Sitjà-Bobadilla A, Peña-Llopis S, Gómez-Requeni P, Médale F, Kaushik S, Pérez-Sánchez J (2005) Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture 249:387–400

    Article  CAS  Google Scholar 

  • Siwicki AK, Morand M, Fuller J Jr, Nissen S, Goryczko K, Ostaszewski P, Kazun K, Glombski E (2003) Influence of feeding the leucine metabolite β-hydroxy-β-methylbutyrate (HMB) on the non-specific cellular and humoral defence mechanisms of rainbow trout (Oncorhynchus mykiss). J Appl Ichthyol 19:44–48

    Article  CAS  Google Scholar 

  • Siwicki AK, Zakes Z, Fuller JC Jr, Nissen S, Trapkowska S, Glabski E, Kazun K, Kowalska A, Terech-Majewska E (2005) The effect of feeding the leucine metabolite β-hydroxy-β-methylbutyrate (HMB) on cell-mediated immunity and protection against Yersinia ruckeri in pikeperch (Sander lucioperca). Aquacult Res 36:16–21

    Article  CAS  Google Scholar 

  • Siwicki AK, Zakes Z, Fuller JC Jr, Nissen S, Kazun K, Glabski E (2006) The influence of β-hydroxy-β-methylbutyrate (HMB) on cell-mediated immunity in tench Tinca tinca (L.): in vitro and in vivo study. Aquacult Int 14:153–161

    Article  Google Scholar 

  • Snyder GS, Gaylord TG, Barrows FT, Hardy RW (2008) Carnosine supplementation on an all-plant protein diet for rainbow trout Oncorhynchus mykiss. Book of Abstracts of Aquaculture America 08, February 9–12, Orlando, Florida, USA, p 369

  • Storebakken T, Shearer KD, Baeverfjord G, Nielsen BG, Åsgård T, Scott T, De Laporte A (2000) Digestibility of macronutrients, energy and amino acids, absorption of elements and absence of intestinal enteritis in Atlantic salmon, Salmo salar, fed diets with wheat gluten. Aquaculture 184:115–132

    Article  CAS  Google Scholar 

  • Subhadra B, Lochmann R, Rawles S, Chen R (2006) Effect of dietary lipid source on the growth, tissue composition and hematological parameters of largemouth bass (Micropterus salmoides). Aquaculture 255:210–222

    Article  CAS  Google Scholar 

  • Summers CH, Winberg S (2006) Interactions between the neural regulation of stress and aggression. J Exp Biol 209:4581–4589

    Article  PubMed  CAS  Google Scholar 

  • Tacon AGJ, Jackson AJ (1985) Utilization of conventional and unconventional protein sources in practical fish feeds. In: Cowey CB, Mackie AMM, Bell JG (eds) Nutrition and feeding in fish. Academic Press, London, pp 119–145

    Google Scholar 

  • 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 285:146–158

    Article  CAS  Google Scholar 

  • Tang HG, Wu TX, Zhao ZY, Pan XD (2008) Effects of fish protein hydrolysate on growth performance and humoral immune response in large yellow croaker (Pseudosciaena crocea R.). J Zhejiang Univ Sci B 9:684–690

    Article  PubMed  CAS  Google Scholar 

  • Taylor JR, Cooper CA, Mommsen TP (2011) Implications of GI function for gas exchange, acid-base balance and nitrogen metabolism. In: Grosell M, Farrell AP, Brauner CJ (eds) The multifunctional gut of fish. Fish physiology, vol 30. Elsevier Science, San Diego, pp 213–259

    Chapter  Google Scholar 

  • Terova G, Bernardini G, Binelli G, Gornati R, Saroglia M (2006) cDNA encoding sequences for myostatin and FGF6 in sea bass (Dicentrarchus labrax L.) and the effect of fasting and refeeding on their expression levels. Domest Anim Endocrin 30:304–319

    Article  CAS  Google Scholar 

  • Terova G, Rimoldi S, Chini V, Gornati R, Bernardini G, Saroglia M (2007) Cloning and expression analysis of insulin-like growth factor I and II in liver and muscle of sea bass (Dicentrarchus labrax L.) during long-term fasting and refeeding. J Fish Biol 70(SB):219–233

    Google Scholar 

  • Terova G, Corà S, Verri T, Rimoldi S, Bernardini G, Saroglia M (2009) Impact of feed availability on PepT1 mRNA expression levels in sea bass (Dicentrarchus labrax). Aquaculture 294:288–299

    Article  CAS  Google Scholar 

  • Trenzado CE, Carrick TR, Pottinger TG (2003) Divergence of endocrine and metabolic responses to stress in two rainbow trout lines selected for differing cortisol responsiveness to stress. Gen Comp Endocrinol 133:332–340

    Article  PubMed  CAS  Google Scholar 

  • Urán PA, Gonçalves AA, Taverne-Thiele JJ, Schrama JW, Verreth JAJ, Rombout JHWM (2008) Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 25:751–760

    Article  PubMed  CAS  Google Scholar 

  • Verburg-van Kemenade BML, Stolte EH, Metz JR, Chadzinska M (2009) Neuroendocrine-immune interactions in teleost fish. In: Bernier NJ, Van Der Kraak G, Farrell AP, Brauner CJ (eds) Fish Neuroendocrinology. Fish physiology, vol 28. Academic Press Inc., San Diego, pp 313–364

    Chapter  Google Scholar 

  • Verri T, Terova G, Dabrowski K, Saroglia M (2011) Peptide transport and animal growth: the fish paradigm. Biol Lett 7:597–600

    Article  PubMed  CAS  Google Scholar 

  • Vielma J, Ruohonen K, Gabaudan J, Vogel K (2004) Top- spraying soybean meal-based diets with phytase improves protein and mineral digestibilities but not lysine utilization in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 35:955–964

    Google Scholar 

  • Vijayan MM, Pereira C, Gordon Grau E, Iwama GK (1997) Metabolic response associated with confinement stress in tilapia: the role of cortisol. Comp Biochem Physiol C 116:89–95

    Article  Google Scholar 

  • Vilhelmsson OT, Martin SAM, Médale F, Kaushik SJ, Houlihan DF (2004) Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92:71–80

    Article  PubMed  CAS  Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    PubMed  CAS  Google Scholar 

  • Wilson RW, Wood CM, Houlihan DF (1996) Growth and protein turnover during acclimation to acid and aluminium in juvenile rainbow trout Oncorhynchus mykiss. Can J Fish Aquat Sci 53:802–811

    Article  CAS  Google Scholar 

  • Winberg S, Lepage O (1998) Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. Am J Physiol Regul Integr Comp Physiol 274:R645–R654

    CAS  Google Scholar 

  • Winberg S, Nilsson A, Hylland P, Söderstöm V, Nilsson GE (1997) Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish. Neurosci Lett 230:113–116

    Google Scholar 

  • Winberg S, Øverli Ø, Lepage O (2001) Suppression of aggression in rainbow trout (Oncorhynchus mykiss) by dietary l-tryptophan. J Exp Biol 204:3867–3876

    PubMed  CAS  Google Scholar 

  • Wiseman S, Osachoff H, Bassett E, Malhotra J, Bruno J, VanAggelen G, Mommsen TP, Vijayan MM (2007) Gene expression pattern in the liver during recovery from an acute stressor in rainbow trout. Comp Biochem Physiol D 2:234–244

    Google Scholar 

  • Wood AW, Duan CM, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol Surv Cell Biol 243:215–285

    CAS  Google Scholar 

  • Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Davis TA, Jaeger LA, Johnson GA, Kim SW, Knabe DA, Meininger CJ, Spencer TE, Yin YL (2007) Important roles of the arginine family amino acids in swine nutrition and production. Livest Sci 112:8–22

    Article  Google Scholar 

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Acknowledgments

This publication benefits from participation of authors in COST action 867 “Welfare of fish in European aquaculture.” LC participated in this review in the framework of project HYDRAA-PTDC/MAR/71685/2006, granted by Fundação para a Ciência e a Tecnologia (FCT), Portugal, with the support of FEDER. LT is a member of the XRAq and was founded by SGR2009-554 (Generalitat de Catalunya). C. Aragão, B. Costas and C. Martins acknowledge financial support by Fundação para a Ciência e Tecnologia, Portugal, through grants SFRH/BPD/37197/2007, SFRH/BD/38697/2007 and SFRH/BPD/42015/2007.

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Conceição, L.E.C., Aragão, C., Dias, J. et al. Dietary nitrogen and fish welfare. Fish Physiol Biochem 38, 119–141 (2012). https://doi.org/10.1007/s10695-011-9592-y

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