Skip to main content
Log in

Effects of stocking density on stress response, innate immune parameters, and welfare of turbot (Scophthalmus maximus)

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

This experiment was conducted to investigate the growth performance, stress and immune responses, and welfare of juvenile turbot (Scophthalmus maximus) under three different densities (initial density 9.3, 13.6, and 19.1 kg m−2) for 120 days in a recirculating aquaculture system. Turbot were measured every 20 days to evaluate growth biometrically and sampled every month to measure biochemical parameters and mRNA levels of some stress-related genes. No significant differences were detected in the parameters and gene expression among density groups until the final sampling, except Fulton’s condition factor, lysozyme, immunoglobulin M, and complement C3. At the end of the experiment (final density 26.11, 38.22, and 52.25 kg m−2), turbot reared in the high-density (HD) group had lower body mass increase, specific growth rate, and Fulton’s condition factor, as well as higher feed conversion ratio and coefficient of variation for weight than those reared in the low-density (LD) group (P < 0.05). Fish in the HD group had higher serum cortisol, glucose, lactate, and cholesterol levels than fish in the other groups, whereas they had lower lysozyme, immunoglobulin M, and complement C3 and C4 contents (P < 0.05). Fish reared in the HD group also had higher serum chloride and osmolality levels and higher sodium-potassium adenosine triphosphatase (Na+,K+-ATPase) activity and higher Na+,K+-ATPase gene expression levels in gills compared to the other groups (P < 0.05). The mRNA levels of cytochrome P450 1A (CYP1A) and heat-shock proteins 70 and 90 (HSP70 and HSP90) were significantly upregulated, whereas glutathione S-transferase (GST) mRNA levels were significantly downregulated in the head kidney of fish in the HD group relative to fish in the other groups at the end of this trial (P < 0.05). These results indicated that overly high stocking (~50 kg m−2) density can negatively affect the growth performance, serum biochemical parameters, osmolality levels, stress-related gene expression, and overall welfare of turbot.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aksungur N, Aksungur M, Akbulut B, Kutlu I (2007) Effects of stocking density on growth performance survival and food conversion ratio of turbot (Psetta maxima) in the net cages on the southeastern coast of the Black Sea. Turk J Fish Aquat Sci 7:147–152

    Google Scholar 

  • Alak G, Yeltekin AÇ, Taş IH, Ucar A, Parlak V, Topal A, Kocaman EM, Atamanalp M (2017) Investigation of 8-OHdG, CYP1A, HSP70 and transcriptional analyses of antioxidant defence system in liver tissues of rainbow trout exposed to eprinomectin. Fish Shellfish Immunol 65:136–144

    CAS  PubMed  Google Scholar 

  • Arockiaraj J, Gnanam AJ, Palanisamy R, Bhatt P, Kumaresan V, Chaurasia MK, Pasupuleti M, Ramaswamy H, Arasu A, Sathyamoorthi A (2014) A cytosolic glutathione s-transferase, GST-theta from freshwater prawn Macrobrachium rosenbergii: molecular and biochemical properties. Gene 546:437–442

    CAS  PubMed  Google Scholar 

  • Baer A, Schulz C, Traulsen I, Krieter J (2011) Analysing the growth of turbot (Psetta maxima) in a commercial recirculation system with the use of three different growth models. Aquacult Int 19:497–511

    Google Scholar 

  • Björnsson B, Steinarsson A, Oddgeirsson M, Ólafsdóttir SR (2012) Optimal stocking density of juvenile Atlantic cod (Gadus morhua L.) reared in a land-based farm. Aquaculture s356-357:342–350

    Google Scholar 

  • Conte FS (2004) Stress and the welfare of cultured fish. Appl Anim Behav Sci 86:205–223

    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

    CAS  Google Scholar 

  • Costas B, Aragão C, Dias J, Afonso A, Conceição LEC (2013) 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

    CAS  PubMed  Google Scholar 

  • Dennis TE, Bulger AJ (1995) Condition factor and whole-body sodium concentrations in a freshwater fish: evidence for acidification stress and possible ionoregulatory over-compensation. Water Air Soil Pollut 85:377–382

    CAS  Google Scholar 

  • Di Marco P, Priori A, Finoia MG, Massari A, Mandich A, Marino G (2008) Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquaculture 275:319–328

    Google Scholar 

  • Diesen Hosfeld C, Hammer J, Handeland SO, Fivelstad S, Stefansson SO (2009) Effects of fish density on growth and smoltification in intensive production of Atlantic salmon (Salmo salar L.). Aquaculture 294:236–241

    Google Scholar 

  • Ellis T, North B, Scott AP, Bromage NR, Porter M, Gadd D (2010) The relationships between stocking density and welfare in farmed rainbow trout. J Fish Biol 61:493–531

    Google Scholar 

  • European Food Safety Authority (EFSA) (2008) Scientific Opinion of the Panel on Animal Health and Animal Welfare on a request from the European Commission on the Animal welfare aspects of husbandry systems for farmed trout. EFSA J 796:1–22

    Google Scholar 

  • FAO (2018) FAO yearbook. Fishery and aquaculture statistics 2016. Rome

  • Garcia F, Romera DM, Gozi KS, Onaka EM, Fonseca FS, Schalch SHC, Candeira PG, Guerra LOM, Carmo FJ, Carneiro DJ, Martins MIEG, Portella MC (2013) Stocking density of Nile tilapia in cages placed in a hydroelectric reservoir. Aquaculture 410-411:51–56

    Google Scholar 

  • Gornati R, Papis E, Rimoldi S, Terova G, Saroglia M, Bernardini G (2004) Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax, L.). Gene 341:111–118

    CAS  PubMed  Google Scholar 

  • Herrera M, Vargas-Chacoff L, Hachero I, Ruiz-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

    CAS  Google Scholar 

  • Hwang HK, Son MH, Myeong JI, Kim CW, Min BH (2014) Effects of stocking density on the cage culture of Korean rockfish (Sebastes schlegeli). Aquaculture 434:303–306

    Google Scholar 

  • Iguchi K, Ogawa K, Nagae M, Ito F (2003) The influence of rearing density on stress response and disease susceptibility of ayu (Plecoglossus altivelis). Aquaculture 220:515–523

    Google Scholar 

  • Irwin S, O'Halloran J, FitzGerald RD (1999) Stocking density, growth and growth variation in juvenile turbot, Scophthalmus maximus (Rafinesque). Aquaculture 178:77–88

    Google Scholar 

  • Iwama GK (2007) The welfare of fish. Dis Aquat Org 75:155–158

    Google Scholar 

  • Jia R, Liu BL, Han C, Huang B, Lei JL (2016) Influence of stocking density on growth performance, antioxidant status, and physiological response of juvenile turbot, Scophthalmus maximu, reared in land-based recirculating aquaculture system. J World Aquacult Soc 47:587–599

    CAS  Google Scholar 

  • Larsen BK, Skov PV, McKenzie DJ, Jokumsen A (2012) The effects of stocking density and low level sustained exercise on the energetic efficiency of rainbow trout (Oncorhynchus mykiss) reared at 19 °C. Aquaculture 324-325:226–233

    Google Scholar 

  • Lei JL, Liu XF (2010) Culture of turbot: chinese perspective. In: Daniels HV, Watanabe WO (eds) Practical flatfish culture and stock enhancement. Wiley-Blackwell, Iowa, pp 185–202

    Google Scholar 

  • Li X, Liu Y, Blancheton JP (2013) Effect of stocking density on performances of juvenile turbot (Scophthalmus maximus) in recirculating aquaculture systems. Chin J Oceanol Limnol 31:514–522

    CAS  Google Scholar 

  • Liu B, Liu Y, Wang X (2015) The effect of stocking density on growth and seven physiological parameters with assessment of their potential as stress response indicators for the Atlantic salmon (Salmo salar). Mar Freshw Behav Physiol 48:177–192

    CAS  Google Scholar 

  • Liu B, Jia R, Zhao K, Wang G, Lei J, Huang B (2017a) Stocking density effects on growth and stress response of juvenile turbot (Scophthalmus maximus) reared in land-based recirculating aquaculture system. Acta Oceanol Sin 36:31–38

    CAS  Google Scholar 

  • Liu B, Liu Y, Sun G (2017b) Effects of stocking density on growth performance and welfare-related physiological parameters of Atlantic salmon Salmo salar L. in recirculating aquaculture system. Aquac Res 48:2133–2144

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Lupatsch I, Santos GA, Schrama JW, Verreth JAJ (2010) Effect of stocking density and feeding level on energy expenditure and stress responsiveness in European sea bass Dicentrarchus labrax. Aquaculture 298:245–250

    Google Scholar 

  • Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151

    PubMed  Google Scholar 

  • Magnadóttir B (2010) Immunological control of fish diseases. Mar Biotechnol 12:361–379

    Google Scholar 

  • Mazur CF, Iwama GK (1993) Handling and crowding stress reduces number of plaque-forming cells in Atlantic salmon. J Aquat Anim Health 5:98–101

    Google Scholar 

  • McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794

    CAS  Google Scholar 

  • Merino GE, Piedrahita RH, Conklin DE (2007) The effect of fish stocking density on the growth of California halibut (Paralichthys californicus) juveniles. Aquaculture 265:176–186

    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, juveniles. Fish Physiol Biochem 20:53–60

    CAS  Google Scholar 

  • Ni M, Wen H, Li J, Chi M, Bu Y, Ren Y, Zhang M, Song Z, Ding H (2014) The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenckii) to stocking density and hypoxia stress. Fish Shellfish Immunol 36:325–335

    CAS  PubMed  Google Scholar 

  • North BP, Turnbull JF, Ellis T, Porter MJ, Migaud H, Bron J, Bromage NR (2006) The impact of stocking density on the welfare of rainbow trout (Oncorhynchus mykiss). Aquaculture 255:466–479

    Google Scholar 

  • Oppedal F, Vågseth T, Dempster T, Juell JE, Johansson D (2011) Fluctuating sea-cage environments modify the effects of stocking densities on production and welfare parameters of Atlantic salmon (Salmo salar L.). Aquaculture 315:361–368

    Google Scholar 

  • Ortuno J, Esteban MA, Meseguer J (2001) Effects of short-term crowding stress on the gilthead seabream (Sparus aurata L) innate immune response. Fish Shellfish Immunol 11:187–197

    CAS  PubMed  Google Scholar 

  • Person-Le Ruyet J, Baudin-Laurencin F, Devauchelle N, Me’tailler R, Nicolas JL, Robin J, Guillaume J (1991) Culture of turbot (Scophthalmus maximus). In: McVey JP (ed) CRC Handbook of mariculture, Vol. II: Finfish aquaculture. CRC Press, Boca Raton, pp 21–41

    Google Scholar 

  • Pottinger TG (2010) Changes in blood cortisol, glucose and lactate in carp retained in anglers’ keepnets. J Fish Biol 53:728–742

    Google Scholar 

  • Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801

    CAS  PubMed  Google Scholar 

  • Ruane NM, Carballo EC, Komen J (2002) Increased stocking density influences the acute physiological stress response of common carp Cyprinus carpio (L.). Aquac Res 33:777–784

    Google Scholar 

  • Sadhu N, Sharma SK, Joseph S, Dube P, Philipose K (2014) Chronic stress due to high stocking density in open sea cage farming induces variation in biochemical and immunological functions in Asian seabass (Lates calcarifer, Bloch). Fish Physiol Biochem 40:1105–1113

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Sánchez P, Ambrosio PP, Flos R (2013) Stocking density affects Senegalese sole (Solea senegalensis, Kaup) growth independently of size dispersion, evaluated using an individual photo-identification technique. Aquac Res 44:231–241

    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

    CAS  PubMed  Google Scholar 

  • van de Nieuwegiessen PG, Olwo J, Khong S, Verreth JAJ, Schrama JW (2009) Effects of age and stocking density on the welfare of African catfish, Clarias gariepinus Burchell. Aquaculture 288:69–75

    Google Scholar 

  • Vargas-Chacoff L, Calvo Á, Ruiz-Jarabo I, Villarroel F, Muñoz JL, Tinoco AB, Cárdenas S, Mancera JM (2011) Growth performance, osmoregulatory and metabolic modifications in red porgy fry, Pagrus pagrus, under different environmental salinities and stocking densities. Aquac Res 42:1269–1278

    CAS  Google Scholar 

  • Vargas-Chacoff L, Martínez D, Oyarzún R, Nualart D, Olavarría V, Yáñez A, Bertrán C, Ruiz-Jarabo I, Mancera JM (2014) Combined effects of high stocking density and Piscirickettsia salmonis treatment on the immune system, metabolism and osmoregulatory responses of the sub-Antarctic Notothenioid fish Eleginops maclovinus. Fish Shellfish Immunol 40:424–434

    CAS  PubMed  Google Scholar 

  • Wagner EJ, Intelmann SS, Routledge MD (2010) The effects of fry rearing density on hatchery performance, fin condition, and agonistic behavior of rainbow trout Oncorhynchus mykiss fry. J World Aquacult Soc 27:264–274

    Google Scholar 

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

    Google Scholar 

  • Yarahmadi P, Miandare HK, Hoseinifar SH, Gheysvandi N, Akbarzadeh A (2014) The effects of stocking density on hemato-immunological and serum biochemical parameters of rainbow trout (Oncorhynchus mykiss). Aquac Int 23:55–63

    Google Scholar 

  • Yarahmadi P, Miandare HK, Fayaz S, Caipang CMA (2016) Increased stocking density causes changes in expression of selected stress- and immune-related genes, humoral innate immune parameters and stress responses of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 48:43–53

    CAS  PubMed  Google Scholar 

  • Zapata A, Diez B, Cejalvo T, Gutierrez-de Frias C, Cortes A (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136

    CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Key R&D Program of China (grant number 2017YFD0701701), the Central Public-Interest Scientific Institution Basal Research Fund, CAFS (2017HYZD04), and the Modern Agriculture Industry System Construction of Special Funds (CARS-47-G24).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Baoliang Liu or Bin Huang.

Ethics declarations

All procedures performed in studies involving animals were in accordance with the guidelines and ethical standards of Chinese Academy of Fishery Sciences and its later amendments or comparable ethical standards.

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, B., Fei, F., Li, X. et al. Effects of stocking density on stress response, innate immune parameters, and welfare of turbot (Scophthalmus maximus). Aquacult Int 27, 1599–1612 (2019). https://doi.org/10.1007/s10499-019-00413-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-019-00413-2

Keywords

Navigation