Skip to main content
SpringerLink
Log in

Interactive effects of a high-quality protein diet and high stocking density on the stress response and some innate immune parameters of Senegalese sole Solea senegalensis

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Amino acids (AA) regulate key metabolic pathways, including some immune responses. Therefore, this study aimed to assess whether an increased availability of dietary AA can mitigate the expected increase in plasma cortisol and metabolites levels due to high stocking density and its subsequent immunosuppression. Senegalese sole (Solea senegalensis) were maintained at low stocking density (LSD; 3.5 kg m−2) or high stocking density (HSD; 12 kg m−2) for 18 days. Additionally, both treatments were fed a control or a high protein (HP) diet (LSD, LSD HP, HSD and HSD HP). The HP diet slightly increased the levels of digestible indispensable AA, together with tyrosine and cysteine. HSD was effective in inducing a chronic stress response after 18 days of treatment since fish held at HSD presented higher plasma cortisol, glucose and lactate levels. Moreover, this increase in stress indicators translated in a decrease in plasma lysozyme, alternative complement pathway (ACP) and peroxidase activities, suggesting some degree of immunosuppression. Interestingly, while plasma glucose and lactate levels in HSD HP specimens decreased to similar values than LSD fish, plasma lysozyme, ACP and peroxidase activities increased, with even higher values than LSD groups for ACP activity. It is suggested that the HP diet may be used as functional feed since it may represent a metabolic advantage during stressful events and may counteract immunosuppression in sole.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 1758. Amino Acids 34:143–148

    Article  PubMed  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  Google Scholar 

  • Arends RJ, Mancera JM, Muñoz JL, Wendelaar Bonga SE, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocr 163:149–157

    Article  PubMed  CAS  Google Scholar 

  • Caipang CMA, Berg I, Brinchmann MF, Kiron V (2009) Short-term crowding stress in Atlantic cod, Gadus morhua L. modulates the humoral immune response. Aquaculture 295:110–115

    Article  CAS  Google Scholar 

  • Cerezuela R, Cuesta A, Meseguer J, Esteban MA (2009) Effects of dietary vitamin D3 administration on innate immune parameters of seabream (Sparus aurata L.). Fish Shellfish Immunol 26:243–248

    Article  PubMed  CAS  Google Scholar 

  • Cohen SA, Meys M, Tarvin TL (1989) The pico-tag method—a manual of advanced techniques for amino acids analysis. Waters, Division of Milipore, Bedford

    Google Scholar 

  • Conceição LEC, Aragão C, Dias J, Costas B, Terova G, Martins C, Tort L (2012) Dietary nitrogen and fish welfare. Fish Physiol Biochem 38:119–141

    Article  PubMed  Google Scholar 

  • Conde-Sieira M, Aguilar AJ, López-Patiño MA, Míguez JM, Soengas JL (2010) Stress alters food intake and glucosensing response in hypothalamus, hindbrain, liver, and Brockmann bodies of rainbow trout. Physiol Behav 101:483–493

    Article  PubMed  CAS  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. Aquac Res 39:1–9

    Article  CAS  Google Scholar 

  • Costas B, Conceição LEC, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011a) 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, Conceição LEC, Dias J, Novoa B, Figueras A, Afonso A (2011b) Dietary arginine and repeated handling increase disease resistance and modulate innate immune mechanisms of Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol 31:838–847

    Article  PubMed  CAS  Google Scholar 

  • Costas B, Aragão C, Soengas JL, Míguez JM, Rema P, Dias J, Afonso A, Conceição LEC (2012a) Effects of dietary amino acids and repeated handling on stress response and brain monoaminergic neurotransmitters in Senegalese sole (Solea senegalensis) juveniles. Comp Biochem Physiol A 161:18–26

    Article  CAS  Google Scholar 

  • Costas B, Rêgo PCNP, Simões I, Marques JF, Castro-Cunha M, Afonso A (2012b) Cellular and humoral immune responses of Senegalese sole (Solea senegalensis Kaup, 1858) following challenge with two Photobacterium damselae subsp. piscicida strains from different geographical origins. J Fish Dis (in press). doi:10.1111/jfd12033

  • Cuesta A, Laiz-Carrión R, Martín del Río MP, Meseguer J, Mancera JM, Esteban MA (2005) Salinity influences the humoral immune parameters of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 18:255–261

    Article  PubMed  CAS  Google Scholar 

  • Demers NE, Bayne CJ (1997) The immediate effects of stress on hormones and plasma lysozyme in rainbow trout. Dev Comp Immunol 21:363–373

    Article  PubMed  CAS  Google Scholar 

  • Dhabhar FS (2009) A hassle a day may keep the pathogens away: the fight-or-flight stress response and the augmentation of immune function. Integr Comp Biol 49:215–236

    Article  PubMed  CAS  Google Scholar 

  • Dias J, Yúfera M, Valente LMP, Rema P (2010) Feed transit and apparent protein, phosphorus and energy digestibility of practical feed ingredients by Senegalese sole (Solea senegalensis). Aquaculture 302:94–99

    Article  CAS  Google Scholar 

  • Dinis MT, Ribeiro L, Soares F, Sarasquete C (1999) A review on the cultivation potential of Solea senegalensis in Portugal and Spain. Aquaculture 176:27–38

    Article  Google Scholar 

  • Ellis AE (1999) Immunity to bacteria in fish. Fish Shellfish Immunol 9:291–308

    Article  Google Scholar 

  • Fast MD, Hosoya S, Johnson SC, Afonso LOB (2008) Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immunol 24:194–204

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Herrera M, Vargas-Chacoff L, Hachero I, Ruíz-Jarabo I, Rodiles A, Navas JI, Mancera JM (2009) Physiological responses of juvenile wedge sole Dicologoglossa cuneata (Moreau) to high stocking density. Aquac Res 40:790–797

    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  Google Scholar 

  • Holland MCH, Lambris JD (2002) The complement system in teleosts. Fish Shellfish Immunol 12:399–420

    Article  PubMed  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 

  • Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture potential of Solea solea and Solea senegalensis. Rev Fish Biol Fish 13:379–407

    Article  Google Scholar 

  • Kaushik SJ (1998) Whole body amino acid composition of European seabass (Dicentrarchus labrax), gilthead seabream (Sparus aurata) and turbot (Psetta maxima) with an estimation of their IAA requirement profiles. Aquat Living Resour 11:355–358

    Article  Google Scholar 

  • Lepage O, Tottmar O, Winberg S (2002) Time-course of the effect of dietary l-tryptophan on plasma cortisol levels in rainbow trout Oncorhynchus mykiss. J Exp Biol 206:3679–3687

    Google Scholar 

  • Lepage O, Vílchez IM, Pottinger TG, Winberg S (2003) Elevated dietary intake of l-tryptophan counteracts the stress-induced elevation of plasma cortisol in rainbow trout (Oncorhynchus mykiss). J Exp Biol 205:3589–3599

    Article  Google Scholar 

  • Li P, Yin Y-L, Li D, Kim SW, 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  Google Scholar 

  • Ma X, Lin Y, Jiang Z, Zheng C, Zhou G, Yu D, Cao T, Wang J, Chen F (2010) Dietary arginine supplementation enhances antioxidative capacity and improves meat quality of finishing pigs. Amino Acids 38:95–102

    Article  PubMed  CAS  Google Scholar 

  • Mauri I, Romero A, Acerete L, MacKenzie S, Roher N, Callol A, Cano I, Alvarez MC, Tort L (2011) Changes in complement responses in Gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax) under crowding stress, plus viral and bacterial challenges. Fish Shellfish Immunol 30:182–188

    Article  PubMed  CAS  Google Scholar 

  • Melchior D, Seve B, Le Floc’h N (2004) Chronic lung inflammation affects plasma amino acid concentrations in pigs. J Anim Sci 82:1091–1099

    PubMed  CAS  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 16:119–128

    Article  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 

  • Montero D, Izquierdo MS, Tort L, Robaina L, Vergara JM (1999) High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata L, juveniles. Fish Physiol Biochem 20:53–60

    Article  CAS  Google Scholar 

  • Murray CK, Fletcher TC (1976) The immunohistochemical localization of lysozyme in plaice (Pleuronectes platessa L.) tissues. J Fish Biol 9:329–334

    Article  CAS  Google Scholar 

  • Neumann NF, Fagan D, Belosevic M (1995) Macrophage activating factor(s) secreted by mitogen stimulated goldfish kidney leucocytes synergize with bacterial lipopolysaccharide to induce nitric oxide production in teleost macrophages. Dev Comp Immunol 19:473–482

    Article  PubMed  CAS  Google Scholar 

  • NRC (1993) Nutrient requirements of fish. National Academy Press, Washington

    Google Scholar 

  • Perianayagam MC, Oxenkrug GF, Jaber BL (2005) Immune-modulating effects of melatonin, N-acetylserotonin, and N-acetyldopomine. Ann N Y Acad Sci 1053:386–393

    Article  PubMed  CAS  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. Aquac Res 38:1198–1204

    Article  CAS  Google Scholar 

  • Pottinger TG (2008) The stress response in fish-mechanisms, effects and measurement. In: Branson EJ (ed) Fish welfare. Blackwell Publishing, Oxford, pp 32–48

    Chapter  Google Scholar 

  • Prunet P, Øverli Ø, Douxfils J, Bernardini G, Kestemont P, Baron D (2012) Fish welfare and genomics. Fish Physiol Biochem 38:43–60

    Article  PubMed  CAS  Google Scholar 

  • Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248

    Article  PubMed  CAS  Google Scholar 

  • Rotllant J, Pavlidis M, Kentouri M, Abad ME, Tort L (1997) Non-specific immune responses in the red porgy, Pagrus pagrus after crowding stress. Aquaculture 156:279–290

    Article  Google Scholar 

  • Rotllant J, Ruane NM, Dinis MT, Canário AVM, Power DM (2006) Intra-adrenal interactions in fish: catecholamine stimulated cortisol release in sea bass (Dicentrarchus labrax L.). Comp Biochem Physiol A 143:375–381

    Article  Google Scholar 

  • Saeij JPJ, Verburg-van Kemenade LBM, van Muiswinkel WB, Wiegertjes GF (2003) Daily hangling stress reduces resistance of carp to Trypanoplasma borreli: in vitro modulatory effects of cortisol on leukocyte function and apoptosis. Dev Comp Immunol 27:233–245

    Article  PubMed  CAS  Google Scholar 

  • Salas-Leiton E, Anguis V, Martín-Antonio B, Crespo D, Planas JV, Infante C, Cañavate JP, Manchado M (2010) Effects of stocking density and feed ration on growth and gene expression in the Senegalese sole (Solea senegalensis): potential effects on the immune response. Fish Shellfish Immunol 28:296–302

    Article  PubMed  CAS  Google Scholar 

  • Segner H, Sundh H, Buchmann K, Douxfils J, Sundell KS, Mathieu C, Ruane N, Jutfelt F, Toften H, Vaughan L (2012) Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiol Biochem 38:85–105

    Article  PubMed  CAS  Google Scholar 

  • Stolte EH, Nabuurs SB, Bury NR, Sturm A, Flik G, Savelkoul HFJ, Verburg-van Kemenade BML (2008) Stress and innate immunity in carp: corticosteroid receptors and pro-inflammatory cytokines. Mol Immunol 46:70–79

    Article  PubMed  CAS  Google Scholar 

  • Suenaga R, Tomonaga S, Yamane H, Kurauchi I, Tsuneyoshi Y, Sato H, Denbow DM, Furuse M (2008) Intracerebroventricular injection of l-arginine induces sedative and hypnotic effects under an acute stress in neonatal chicks. Amino Acids 35:139–146

    Article  PubMed  CAS  Google Scholar 

  • Sunyer JO, Tort L (1995) Natural hemolitic and bactericidal activities of seabream Sparus aurata serum are affected by the alternative complement pathway. Vet Immunol Immunopathol 45:333–345

    Article  PubMed  CAS  Google Scholar 

  • Tafalla C, Novoa B (2000) Requirements for nitric oxide production by turbot (Scophthalmus maximus) head kidney macrophages. Dev Comp Immunol 24:623–631

    Article  PubMed  CAS  Google Scholar 

  • Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375

    Article  PubMed  CAS  Google Scholar 

  • Verburg-van Kemenade LBM, 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 physiology, vol 28. Academic Press Inc., San Diego, pp 313–364

    Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 7:591–625

    Google Scholar 

  • Weyts FAA, Cohen N, Flik G, Verburg-van Kemenade BML (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 9:1–20

    Article  Google Scholar 

  • Wilson RP (2002) Amino acids and proteins. In: Halver JE, Hardy RW (eds) Fish nutrition. Elsevier Science, San Diego, pp 144–179

    Google Scholar 

  • Yao K, Guan S, Li T, Huang R, Wu G, Ruan Z, Yin Y (2011) Dietary l-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. Br J Nutr 105:703–709

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by project STRESSAA-POCTI/CVT/49324/2002 (FCT, Portugal and FEDER). Benjamín Costas and Cláudia Aragão were supported by Fundação para a Ciência e a Tecnologia, Portugal (SFRH/BD/38697/2007 and SFRH/BPD/37197/2007, respectively).

Author information

Authors and Affiliations

  1. CCMAR-CIMAR LA, Centro de Ciências do Mar do Algarve, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Cláudia Aragão, Jorge Dias & Luís E. C. Conceição

  2. CIIMAR-CIMAR LA, Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Rua dos Bragas 289, 4050-123, Porto, Portugal

    Benjamín Costas & António Afonso

  3. ICBAS, Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Largo Prof. Abel Salazar 2, 4099-003, Porto, Portugal

    António Afonso

Authors
  1. Benjamín Costas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cláudia Aragão
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. António Afonso
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luís E. C. Conceição
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamín Costas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Costas, B., Aragão, C., Dias, J. et al. Interactive effects of a high-quality protein diet and high stocking density on the stress response and some innate immune parameters of Senegalese sole Solea senegalensis . Fish Physiol Biochem 39, 1141–1151 (2013). https://doi.org/10.1007/s10695-013-9770-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-013-9770-1

Keywords

Search

Navigation