Skip to main content
SpringerLink
Log in

High dietary lipids elevate carbon loss without sparing protein in adequate protein-fed juvenile turbot (Psetta maxima)

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

This study was undertaken to determine the effects of dietary lipid levels on growth and nutrient utilization, and carbon (C), nitrogen (N) and phosphorus (P) balances in juvenile turbot (Psetta maxima) in brackish water. Four isonitrogenous diets (50 % protein) differing in dietary lipid levels from 10 to 19 by 3 % increments (named 10L, 13L, 16L and 19L, respectively) were fed to four replicate groups of fish with an initial weight of 54.4 ± 0.2 g for 9 weeks. Significantly better growth and feed conversion ratio were observed in fish fed 13L than those fed 16L and 19L. The whole body, fillet, viscera and liver dry matter and lipid levels were increased as dietary lipid was increased. Liver protein levels were lower in 16L and 19L than 10L. There was an ascending pattern in the whole-body C levels and C/N ratios with the increase in dietary lipids. No significant effect of dietary lipids on either protein efficiency ratio or N and P retentions was detected. Dietary lipids led to an increase in C losses to the environment. Overall, high dietary lipids when introduced at an adequate protein level did reduce growth and feed utilization without a protein-sparing effect and resulted in higher C losses in juvenile turbot reared, and a dietary lipid level of about 13 % seemed to be optimum.

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

Similar content being viewed by others

References

  • Adron JW, Blair A, Cowey CB, Shanks AM (1976) Effects of dietary energy level and dietary energy source on growth, feed conversion and body composition of turbot (Scophthalmus maximus L.). Aquaculture 7:125–132

    Article  CAS  Google Scholar 

  • Akpınar Z, Sevgili H, Demir A, Özgen T, Emre Y, Eroldoğan OT (2012) Effects of dietary lipid levels on growth, nutrient utilization, and nitrogen and carbon balances in shi drum (Umbrina cirrosa L.). Aquac Int 20:131–143

    Article  Google Scholar 

  • Alam MS, Teshima S-I, Koshio S, Uyan O, Ishikawa M (2004) Effects of dietary protein and lipid levels on growth and body composition of juvenile Japanese flounder, Paralichthys olivaceus, fed diets containing intact proteins or crystalline amino acids. J Appl Aquac 14:115–131

    Article  Google Scholar 

  • Alam MS, Watanabe WO, Daniels HV (2009) Effect of different dietary protein and lipid levels on growth performance and body composition of juvenile southern flounder, Paralichthys lethostigma, reared in a recirculating aquaculture system. J World Aquac Soc 40:513–521

    Article  Google Scholar 

  • Andersen NG, Alsted NS (1993) Growth and body composition of turbot (Scophthalmus maximus (L.) in relation to different lipid/protein ratios in the diet. In: Kaushik SJ, Luquet P (eds) Fish nutrition in practice. France, INRA, pp 479–491

    Google Scholar 

  • AOAC (1990) Official methods of analysis. Association of official analytical chemists, Arlington

    Google Scholar 

  • Apostolaki ET, Holmer M, Marba N, Karakassis I (2011) Reduced carbon sequestration in a Mediterranean seagrass (Posidonia oceanica) ecosystem impacted by fish farming. Aquac Env Interac 2:49–59

    Article  Google Scholar 

  • Bailey J, Alanärä A (2006) Digestible energy need (DEN) of selected farmed fish species. Aquaculture 251:438–455

    Article  Google Scholar 

  • Booth MA, Allan GL, Pirozzi I (2010) Estimation of digestible protein and energy requirements of yellowtail kingfish Seriola lalandi using a factorial approach. Aquaculture 307:247–259

    Article  Google Scholar 

  • Borba MR, Fracalossi DM, Pezzato LE (2006) Dietary energy requirement of piracanjuba fingerlings, Brycon orbignyanus, and relative utilization of dietary carbohydrate and lipid. Aquac Nutr 12:183–191

    Article  CAS  Google Scholar 

  • Borges P, Oliveira B, Casal S, Dias J, Conceição L, Valente LMP (2009) Dietary lipid level affects growth performance and nutrient utilisation of Senegalese sole (Solea senegalensis) juveniles. Br J Nutr 102:1007–1014

    Article  CAS  PubMed  Google Scholar 

  • Brendel O, Iannetta PPM, Stewart D (2000) A rapid and simple method to isolate pure alpha-cellulose. Phytochem Anal 11:7–10

    Google Scholar 

  • Bromley PJ (1980) Effect of dietary protein, lipid and energy content on the growth of turbot (Scophthalmus maximus L.). Aquaculture 19:359–369

    Article  CAS  Google Scholar 

  • Bureau DP, Hua K (2010) Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquac Res 41:777–792

    Article  Google Scholar 

  • Bureau DP, Kaushik SJ, Cho CY (2002) Bioenergetics. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic Press, San Diego

    Google Scholar 

  • Caceres-Martinez C, Cadena-Roa M, Métailler R (1984) Nutritional requirements of turbot (Scophthalmus maximus): i. a preliminary study of protein and lipid utilization. J World Maric Soc 15:191–202

    Article  Google Scholar 

  • Campos C, Valente LMP, Borges P, Bizuayehu T, Fernandes JMO (2010) Dietary lipid levels have a remarkable impact on the expression of growth-related genes in Senegalese sole (Solea senegalensis Kaup). J Exp Biol 213:200–209

    Article  CAS  PubMed  Google Scholar 

  • Cho CY, Bureau DP (2001) A review of diet formulation strategies and feeding systems to reduce excretory and feed wastes in aquaculture. Aquac Res 32:349–360

    CAS  Google Scholar 

  • Cho SH, Lee SM, Lee JH (2005) Effect of dietary protein and lipid levels on growth and body composition of juvenile turbot (Scophthalmus maximus L) reared under optimum salinity and temperature conditions. Aquac Nutr 11:235–240

    Article  CAS  Google Scholar 

  • Chun Y, Yin ZD (1998) Glycogen assay for diagnosis of female genital chlamydia trachomatis infection. J Clin Microbiol 36:1081–1082

    CAS  PubMed Central  PubMed  Google Scholar 

  • Company R, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J (1999) Growth performance and adiposity in gilthead sea bream (Sparus aurata): risks and benefits of high energy diets. Aquaculture 171:279–292

    Article  CAS  Google Scholar 

  • Czamanski M, Nugraha A, Pondaven P, Lasbleiz M, Masson A, Caroff N, Bellail R, Tréguer P (2011) Carbon, nitrogen and phosphorus elemental stoichiometry in aquacultured and wild-caught fish and consequences for pelagic nutrient dynamics. Mar Biol 158:2847–2862

    Article  CAS  Google Scholar 

  • Danancher D, Garcia-Vazquez E (2007) Turbot–Scophthalmus maximus Biology, ecology and genetics. Genimpact Final Scientific Report Oviedo, Spain, pp 55–61

  • Danielssen DS, Hjertnes T (1993) Effect of dietary protein levels in diets for turbot (Scophthalmus maximus L.) to market size. In: Kaushik SJ, Luquet P (eds) Fish nutrition in practice. France, INRA, pp 89–96

    Google Scholar 

  • Davies SJ, Gouveia A, Laporte J, Woodgate SL, Nates S (2009) Nutrient digestibility profile of premium (category III grade) animal protein by-products for temperate marine fish species (European sea bass, gilthead sea bream and turbot). Aquac Res 40:1759–1769

    Article  CAS  Google Scholar 

  • Dias J, Huelvan C, Dinis MT, Métailler R (1998) Influence of dietary bulk agents (silica, cellulose and a natural zeolite) on protein digestibility, growth, feed intake and feed transit time in European seabass (Dicentrarchus labrax) juveniles. Aquat Living Resour 11:219–226

    Article  Google Scholar 

  • Dias J, Rueda-Jasso R, Panserat S, Conceição LECd, Gomes EF, Dinis MT (2004) Effect of dietary carbohydrate-to-lipid ratios on growth, lipid deposition and metabolic hepatic enzymes in juvenile Senegalese sole (Solea senegalensis, Kaup). Aquac Res 35:1122–1130

    Article  CAS  Google Scholar 

  • Dixon WJ (1950) Analysis of extreme values. Ann Math Stat 21:488–506

    Article  Google Scholar 

  • Dumas A, de Lange CFM, France J, Bureau DP (2007) Quantitative description of body composition and rates of nutrient deposition in rainbow trout (Oncorhynchus mykiss). Aquaculture 273:165–181

    Article  CAS  Google Scholar 

  • Enes P, Panserat S, Kaushik S, Oliva-Teles A (2009) Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 35:519–539

    Article  CAS  PubMed  Google Scholar 

  • Glencross B, Michael R, Austen K, Hauler R (2008) Productivity, carcass composition, waste output and sensory characteristics of large barramundi Lates calcarifer fed high-nutrient density diets. Aquaculture 284:167–173

    Article  CAS  Google Scholar 

  • Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298

    Article  Google Scholar 

  • Gondwe MJS, Guildford SJ, Hecky RE (2011) Carbon, nitrogen and phosphorus loadings from tilapia fish cages in Lake Malawi and factors influencing their magnitude. J Gt Lakes Res 37:93–101

    Article  CAS  Google Scholar 

  • Guerreiro I, Peres H, Castro-Cunha M, Oliva-Teles A (2012) Effect of temperature and dietary protein/lipid ratio on growth performance and nutrient utilization of juvenile Senegalese sole (Solea senegalensis). Aquac Nutr 18:98–106

    Article  CAS  Google Scholar 

  • Hall POJ, Anderson LG, Holby O, Kollberg S, Samuelsson M (1990) Chemical fluxes and mass balances in a marine fish cage farm I: carbon. Mar Ecol Prog Ser 61:61–73

    Article  CAS  Google Scholar 

  • Hamre K, Mangor-Jensen A (2006) A multivariate approach to optimization of macronutrient composition in weaning diets for cod (Gadus morhua). Aquac Nutr 12:15–24

    Article  CAS  Google Scholar 

  • Hebb CD, Castell JD, Anderson DM, Batt J (2003) Growth and feed conversion of juvenile winter flounder (Pleuronectes americanus) in relation to different protein-to-lipid levels in isocaloric diets. Aquaculture 221:439–449

    Article  CAS  Google Scholar 

  • Hendrixson HA, Sterner RW, Kay AD (2007) Elemental stoichiometry of freshwater fishes in relation to phylogeny, allometry and ecology. J Fish Biol 70:121–140

    Article  Google Scholar 

  • Hessen DO, Anderson TR (2008) Excess carbon in aquatic organisms and ecosystems: physiological, ecological, and evolutionary implications. Limnol Oceanogr 53:1685–1696

    Article  CAS  Google Scholar 

  • Holmer M, Marbá N, Terrados J, Duarte CM, Fortes MD (2002) Impacts of milkfish (Chanos chanos) aquaculture on carbon and nutrient fluxes in the Bolinao area, Philippines. Mar Pollut Bull 44:685–696

    Article  CAS  PubMed  Google Scholar 

  • Jobling M (2001) Nutrient partitioning and the influence of feed composition on body composition. In: Houlihan D, Jobling M, Boujard T (eds) Food intake in fish. Blackwell Science, Oxford, pp 354–375

    Chapter  Google Scholar 

  • Koven W, Henderson R, Sargent J (1994) Lipid digestion in turbot (Scophthalmus maximus). I: lipid class and fatty acid composition of digesta from different segments of the digestive tract. Fish Physiol Biochem 13:69–79

    Article  CAS  PubMed  Google Scholar 

  • Lee S-M, Cho SH, Kim K-D (2000) Effects of dietary protein and energy levels on growth and body composition of juvenile flounder Paralichthys olivaceus. J World Aquac Soc 31:306–315

    Article  Google Scholar 

  • Lee JK, Cho SH, Park SU, Kim KD, Lee SM (2003) Dietary protein requirement for young turbot (Scophthalmus maximus L.). Aquac Nutr 9:283–286

    Article  CAS  Google Scholar 

  • Leknes E, Imsland AK, Gústavsson A, Gunnarsson S, Thorarensen H, Árnason J (2012) Optimum feed formulation for turbot, Scophthalmus maximus (Rafinesque, 1810) in the grow-out phase. Aquaculture 344–349:114–119

    Article  Google Scholar 

  • Lupatsch I, Kissil GW (2005) Feed formulations based on energy and protein demands in white grouper (Epinephelus aeneus). Aquaculture 248:83–95

    Article  CAS  Google Scholar 

  • Lupatsch I, Kissil GW, Sklan D (2003) Comparison of energy and protein efficiency among three fish species gilthead sea bream (Sparus aurata), European sea bass (Dicentrarchus labrax) and white grouper (Epinephelus aeneus): energy expenditure for protein and lipid deposition. Aquaculture 225:175–189

    Article  Google Scholar 

  • Mallekh R, Boujard T, Lagardère JP (1999) Evaluation of retention and environmental discharge of nitrogen and phosphorus by farmed turbot (Scophthalmus maximus). N Am J Aquac 61:141–145

    Article  Google Scholar 

  • Mandrioli L, Sirri R, Gatta PP, Morandi F, Sarli G, Parma L, Fontanillas R, Bonaldo A (2012) Histomorphologic hepatic features and growth performances of juvenile Senegalese sole (Solea senegalensis) fed isogenertic practical diets with variable protein/lipid levels. J Appl Ichthyol 28:628–632

    Article  CAS  Google Scholar 

  • Norði G, Glud RN, Gaard E, Simonsen K (2011) Environmental impacts of coastal fish farming: carbon and nitrogen budgets for trout farming in Kaldbaksfjørður (Faroe Islands). Mar Ecol Prog Ser 431:223–241

    Article  Google Scholar 

  • NRC (2011) Nutrient requirement of fish and shrimp. National Academic Press, Washington, DC

    Google Scholar 

  • Pearson-Le Ruyet J (2002) Turbot (Scophtalmus maximus) grow-out in Europe: practices, results and prospects. Turk J Fish Aquac Sci 2:29–39

    Google Scholar 

  • Regost C, Arzel J, Kaushik SJ (1999) Partial or total replacement of fish meal by corn gluten meal in diet for turbot (Psetta maxima). Aquaculture 180:99–117

    Article  Google Scholar 

  • Regost C, Arzel J, Cardinal M, Robin J, Laroche M, Kaushik SJ (2001) Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 193:291–309

    Article  CAS  Google Scholar 

  • Sæther BS, Jobling M (2001) Fat content in turbot feed: influence on feed intake, growth and body composition. Aquac Res 32:451–458

    Article  Google Scholar 

  • SAS Institute Inc (2008) JMP 8 introductory guide. Cary, NC

    Google Scholar 

  • Satoh S, Sarker MSA, Satoh S, Kiron V (2004) Effects of dietary lipid and phosphorus levels on nitrogen and phosphorus excretion in young yellowtail Seriola quinqueradiata: a preliminary observation. Fish Sci 70:1082–1088

    Article  CAS  Google Scholar 

  • Seo J-Y, Lee S-M (2008) Effects of dietary macronutrient level and feeding frequency on growth and body composition of juvenile rockfish (Sebastes schlegeli). Aquac Int 16:551–560

    Article  CAS  Google Scholar 

  • Sevgili H, Kurtoğlu A, Oikawa M, Mefut A, Süyek R (2012) The Use of farmed salmon oil to replace anchovy oil in diet of turbot, Psetta maxima, reared in brackish water. J World Aquacult Soc 43:560–570

    Article  Google Scholar 

  • Shi C-Y, Wang Y-G, Yang S-L, Huang J, Wang Q-Y (2004) The first report of an iridovirus-like agent infection in farmed turbot, Scophthalmus maximus, in China. Aquaculture 236:11–25

    Article  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 

  • Tanner D, Leonard EN, Brazner JC (1999) Microwave digestion method for phosphorus determination of fish tissue. Limnol Oceanogr 44:708–709

    Article  CAS  Google Scholar 

  • Tibbetts SM, Lall SP, Milley JE (2005) Effects of dietary protein and lipid levels and DP DE−1 ratio on growth, feed utilization and hepatosomatic index of juvenile haddock, Melanogrammus aeglefinus L. Aquac Nutr 11:67–75

    Article  CAS  Google Scholar 

  • Turchini GM, Torstensen BE, Ng W-K (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1:10–57

    Article  Google Scholar 

  • Wang X, Olsen LM, Reitan KI, Olsen Y (2012) Discharge of nutrient wastes from salmon farms: environmental effects, and potential for integrated multi-trophic aquaculture. Aquac Env Interact 2:267–283

    Article  Google Scholar 

  • Weimin M, Mengqing L (2007) Analysis of feeds and fertilizers for sustainable aquaculture development in China. In: Hecht T, De Silva SS, Tacon AGJ (eds) Hasan MR. Study and Analysis of Feeds and Fertilizers for Sustainable Aquaculture Development, Rome, pp 141–190

    Google Scholar 

  • Yokoyama H, Takashi T, Ishihi Y, Abo K (2009) Effects of restricted feeding on growth of red sea bream and sedimentation of aquaculture wastes. Aquaculture 286:80–88

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by Japan International Cooperation Agency and General Directorate of Agricultural Production, Turkey. Senior scientists, G. Nezaki, N. Takeno and other project members are greatly acknowledged for their valuable contributions during the study. Ramazan Uysal and Gül Tunç are very much appreciated for their contributions during the carbon analysis.

Author information

Authors and Affiliations

  1. Kepez Unit, Mediterranean Fisheries Research and Production and Training Institute, 07192, Döşemealtı, Antalya, Turkey

    Hüseyin Sevgili, Nesrin Emre & Faruk Pak

  2. Beymelek Unit, Mediterranean Fisheries Research Production and Training Institute, Demre, Antalya, Turkey

    Adem Kurtoğlu, Masahiko Oikawa, Erol Öztürk & Nurgül Dedebali

Authors
  1. Hüseyin Sevgili
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adem Kurtoğlu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masahiko Oikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erol Öztürk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nurgül Dedebali
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nesrin Emre
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Faruk Pak
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hüseyin Sevgili.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 47 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sevgili, H., Kurtoğlu, A., Oikawa, M. et al. High dietary lipids elevate carbon loss without sparing protein in adequate protein-fed juvenile turbot (Psetta maxima). Aquacult Int 22, 797–810 (2014). https://doi.org/10.1007/s10499-013-9708-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-013-9708-8

Keywords

Search

Navigation