Skip to main content

Advertisement

SpringerLink
Log in

Minimizing marine ingredients in diets of farmed Atlantic salmon (Salmo salar): effects on liver and head kidney lipid class and fatty acid composition

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

Abstract

Limited fish meal and fish oil supplies have necessitated research on alternatives for aquafeeds. Seven dietary treatments with different protein and lipid sources were formulated for farmed Atlantic salmon, and their effects on liver and head kidney lipid class, fatty acid, and elemental composition were studied. Fish meal, fish oil, and EPA + DHA content ranged from 5–35%, 0–12%, and 0.1–3%, respectively. Elemental analysis showed that the C to N ratio was higher in the head kidney than in the liver, which is consistent with higher content of total lipids in the head kidney compared with the liver. There was a greater susceptibility to dietary lipid alterations in the liver compared with the head kidney despite liver having a greater proportion of phospholipid and a much lower proportion of triacylglycerol. So long as fish oil levels were 5% or more of the diet, arachidonic acid (ARA) and docosahexaenoic acid (DHA) proportions were the same for each tissue as with feeding the marine diet with 12% fish oil; however, livers and head kidneys from fish fed the lowest amount of fish meal and fish oil had the lowest levels of eicosapentaenoic (EPA) and DHA and the highest ARA levels. Removal of fish oil and reduction of fish meal to 5% in diets of farmed Atlantic salmon affected elemental and lipid compositions of the liver and head kidney tissues potentially increasing susceptibility to inflammation. However, with 10% of the diet comprising fish meal and fish oil, lipid contents were comparable with fish fed marine-based diets.

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

Similar content being viewed by others

References

  • Beheshti Foroutani M, Parrish CC, Wells J, Taylor RG, Rise ML, Shahidi F (2018) Minimizing marine ingredients in diets of farmed Atlantic salmon (Salmo salar): effects on growth performance and muscle lipid class and fatty acid composition. PLoS One 13:e0198538

    Article  Google Scholar 

  • Bell JG, Ashton I, Secombes CJ, Weitzel BR, Dick JR, Sargent JR (1996) Dietary lipid affects phospholipid fatty acid compositions, eicosanoid production and immune function in Atlantic salmon (Salmo salar). Prostaglandins Leukot Essent Fat Acids 54:173–182

    Article  CAS  Google Scholar 

  • Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR (2001) Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr 131:1535–1543

    Article  CAS  Google Scholar 

  • Betancor MB, Howarth FJ, Glencross BD, Tocher DR (2014) Influence of dietary docosahexaenoic acid in combination with other long-chain polyunsaturated fatty acids on expression of biosynthesis genes and phospholipid fatty acid compositions in tissues of post-smolt Atlantic salmon (Salmo salar). Comp Biochem Physiol B 172:74–89

    Article  Google Scholar 

  • Bodin N, Le Loc'h F, Hily C (2007) Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. J Exp Mar Bio Ecol 341:168–175

    Article  CAS  Google Scholar 

  • Bou M, Berge GM, Baeverfjord G, Sigholt T, Østbye T-K, Romarheim OH, Hatlen B, Leeuwis R, Venegas C, Ruyter B (2017) Requirements of n-3 very long-chain PUFA in Atlantic salmon (Salmo salar L): effects of different dietary levels of EPA and DHA on fish performance and tissue composition and integrity. Br J Nutr 117:30–47

    Article  CAS  Google Scholar 

  • Bozza PT, Magalhães KG, Weller PF (2009) Leukocyte lipid bodies—biogenesis and functions in inflammation. Biochim Biophys Acta Mol Cell Biol Lipids 1791:540–551

    Article  CAS  Google Scholar 

  • Caballero-Solares A, Hall JR, Xue X, Eslamloo K, Taylor RG, Parrish CC, Rise ML (2017) The dietary replacement of marine ingredients by terrestrial animal and plant alternatives modulates the antiviral immune response of Atlantic salmon (Salmo salar). Fish Shellfish Immunol 64:24–38

    Article  CAS  Google Scholar 

  • Caballero-Solares A, Xue X, Parrish CC, Foroutani MB, Taylor RG, Rise ML (2018) Changes in the liver transcriptome of farmed Atlantic salmon (Salmo salar) fed experimental diets based on terrestrial alternatives to fish meal and fish oil. BMC Genomics 19:796

    Article  CAS  Google Scholar 

  • Cleland LG, Gibson RA, Hawkes JS, James MJ (1990) Comparison of cell membrane phospholipid fatty acids in five rat strains fed four test diets. Lipids 25:559–564

    Article  CAS  Google Scholar 

  • Codabaccus BM, Bridle AR, Nichols PD, Carter CG (2011) An extended feeding history with a stearidonic acid enriched diet from parr to smolt increases n-3 long-chain polyunsaturated fatty acids biosynthesis in white muscle and liver of Atlantic salmon (Salmo salar L.). Aquaculture 322:65–73

    Article  Google Scholar 

  • Cottin SC, Sanders TA, Hall WL (2011) The differential effects of EPA and DHA on cardiovascular risk factors. Proc Nutr Soc 70:215–231

    Article  CAS  Google Scholar 

  • de Jonge HW, Dekkers DH, Bastiaanse LE, Bezstarosti K, van der Laarse A, Lamers JM (1996) Eicosapentaenoic acid incorporation in membrane phospholipids modulates receptor-mediated phospholipase C and membrane fluidity in rat ventricular myocytes in culture. J Mol Cell Cardiol 28:1097–1108

    Article  Google Scholar 

  • Emery JA, Norambuena F, Trushenski J, Turchini GM (2016) Uncoupling EPA and DHA in fish nutrition: dietary demand is limited in Atlantic salmon and effectively met by DHA alone. Lipids 51:399–412

    Article  CAS  Google Scholar 

  • Eslamloo K, Xue X, Hall JR, Smith NC, Caballero-Solares A, Parrish CC, Rise ML (2017) Transcriptome profiling of antiviral immune and dietary fatty acid dependent responses of Atlantic salmon macrophage-like cells. BMC Genomics 18:706

    Article  Google Scholar 

  • Folmes CD, Park S, Terzic A (2013) Lipid metabolism greases the stem cell engine. Cell Metab 17:153–155

    Article  CAS  Google Scholar 

  • Gasco L, Gai F, Maricchiolo G, Genovese L, Ragonese S, Bottari T, Caruso G (2018a) Fishmeal alternative protein sources for aquaculture feeds. pp. 1-28 in Gasco L, Gai F, Maricchiolo G, Genovese L, Ragonese S, Bottari T, Caruso, G Chemistry of foods: feeds for the aquaculture sector—current situation and alternative sources, SpringerBriefs in Chemistry of Foods 103pp

  • Gasco L, Gai F, Maricchiolo G, Genovese L, Ragonese S, Bottari T, Caruso G (2018b) Sustainable alternatives for dietary fish oil in aquafeeds: actual situation and future perspectives. pp. 49-61 in Gasco L, Gai F, Maricchiolo G, Genovese L, Ragonese S, Bottari T, Caruso, G Chemistry of foods: feeds for the aquaculture sector—current situation and alternative sources, SpringerBriefs in Chemistry of Foods 103pp

  • Hasan M, Halwart M (2009) Fish as feed input for aquaculture: practices sustainability and implications. FAO Fisheries and Aquaculture Technical Paper, Rome, p 518

    Google Scholar 

  • Huntington TC, Hasan MR (2009) Fish as feed inputs for aquaculture: practices, sustainability and implications: a global synthesis. FAO Fisheries and Aquaculture Technical Paper, Rome, pp 209–268

    Google Scholar 

  • IFOMA (2001) Advantages of using fishmeal in animal feeds. Sociedad nacional de pesqueria, http://fis.com/snp/. Accessed 16 November 2017

  • Isseroff RR, Ziboh VA, Chapkin RS, Martinez DT (1987) Conversion of linoleic acid into arachidonic acid by cultured murine and human keratinocytes. J Lipid Res 28:1342–1349

    CAS  PubMed  Google Scholar 

  • Jobling M (2012) National Research Council (NRC): nutrient requirements of fish and shrimp. Aquacult Int 20:601–602

    Article  Google Scholar 

  • Jordal A-EO, Lie Ø, Torstensen BE (2007) Complete replacement of dietary fish oil with a vegetable oil blend affect liver lipid and plasma lipoprotein levels in Atlantic salmon (Salmo salar L.). Aquac Nutr 13:114–130

    Article  CAS  Google Scholar 

  • Kobayashi M, Msangi S, Batka M, Vannuccini S, Dey MM, Anderson JL (2015) Fish to 2030: the role and opportunity for aquaculture. Aquac Econ Manag 19:282–300. https://doi.org/10.1080/13657305.2015.994240

    Article  Google Scholar 

  • Koletzko B, Lien E, Agostoni C, Böhles H, Campoy C, Cetin I, Decsi T, Dudenhausen JW, Dupont C, Forsyth S, Hoesli I, Holzgreve W, Lapillonne A, Putet G, Secher NJ, Symonds M, Szajewska H, Willatts P, Uauy R (2008) The roles of long-chain polyunsaturated fatty acids in pregnancy, lactation and infancy: review of current knowledge and consensus recommendations. J Perinat Med 36(1):5–14

    Article  CAS  Google Scholar 

  • Lund EK, Harvey LJ, Ladha S, Clark DC, Johnson IT (1999) Effects of dietary fish oil supplementation on the phospholipid composition and fluidity of cell membranes from human volunteers. Ann Nutr Metab 43:290–300

    Article  CAS  Google Scholar 

  • Nuez-Ortín WG, Carter CG, Wilson R, Cooke I, Nichols PD (2016) Preliminary validation of a high docosahexaenoic acid (DHA) and α-linolenic acid (ALA) dietary oil blend: tissue fatty acid composition and liver proteome response in Atlantic salmon (Salmo salar) Smolts. PloS One 11:e0161513

    Article  Google Scholar 

  • Oliveira-Goumas B (2004) European parliament directorate general for research working paper: the fish meal and fish oil industry its role in the common fisheries policy (FISH 113 EN) vol FISH 113 EN. European Parliament Luxemburg

  • Parrish CC (1987) Separation of aquatic lipid classes by Chromarod thin-layer chromatography with measurement by Iatroscan flame ionization detection. Can J Fish Aquat Sci 44:722–731

    Article  CAS  Google Scholar 

  • Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. Lipids in Freshwater Ecosystems, Springer-Verlag New York, pp 4-20

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    Article  Google Scholar 

  • Sargent JR, Tocher DR, Bell JG (2002) The lipids. In Fish nutrition, pp181–257

  • Shepherd CJ, Jackson AJ (2013) Global fishmeal and fish-oil supply: inputs, outputs and markets. J Fish Biol 83:1046–1066

    CAS  PubMed  Google Scholar 

  • Siriwardhana N, Kalupahana NS, Moustaid-Moussa N (2012) Health benefits of n-3 polyunsaturated fatty acids: eicosapentaenoic acid and docosahexaenoic acid. Adv Food Nutr Res 65:211–222

    Article  Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184

    Article  CAS  Google Scholar 

  • Torstensen BE, Frøyland L, Lie Ø (2004) Replacing dietary fish oil with increasing levels of rapeseed oil and olive oil–effects on Atlantic salmon (Salmo salar L.) tissue and lipoprotein lipid composition and lipogenic enzyme activities. Aquac Nutr 10:175–192

    Article  CAS  Google Scholar 

  • Torstensen BE, Espe M, Stubhaug I, Lie Ø (2011) Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.). Br J Nutr 106:633–647

    Article  CAS  Google Scholar 

  • Tort L, Balasch JC, Mackenzie S (2003) Fish immune system. A crossroads between innate and adaptive responses. Inmunología 22:277–286

    Google Scholar 

  • Turchini GM, Torstensen BE, Ng WK (2009) Fish oil replacement in finfish nutrition. Rev Aquac 1:10–57

    Article  Google Scholar 

  • Turchini GM, Ng WK, Tocher DR (2010) Fish oil replacement and alternative lipid sources in aquaculture feeds, CRC Press

  • Wall R, Ross RP, Fitzgerald GF, Stanton C (2010) Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 68(5):280–289

    Article  Google Scholar 

  • Xue X, Hall JR, Caballero-Solares A, Eslamloo K, Taylor RG, Parrish CC, Rise ML (2020) Liver transcriptome profiling reveals that dietary DHA and EPA levels influence suites of genes involved in metabolism, redox homeostasis, and immune function in Atlantic salmon (Salmo salar). Mar Biotechnol 22:263–284. https://doi.org/10.1007/s10126-020-09950-x

    Article  CAS  Google Scholar 

  • Ytrestøyl T, Aas TS, Åsgård T (2015) Utilisation of feed resources in production of Atlantic salmon (Salmo salar) in Norway. Aquaculture 448:365–374

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Cara Kirkpatrick for managing the project; Dr. Dominic Nanton for feed formulations; and Dr. Albert Caballero-Solares, Dr. Khalil Eslamloo, Xi Xue, Danny Boyce, and the Joe Brown Aquaculture Research Building staff for their valuable help with fish rearing and sampling. We also thank Dr. Fereidoon Shahidi and three anonymous reviewers for carefully reading the manuscript.

Funding

This study was conducted within the Biomarker Platform for Commercial Aquaculture Feed Development project, a Genomic Applications Partnership Program (GAPP # 6604), funded by the Government of Canada through Genome Canada, Genome Atlantic, Innovate NL (# 211219) and the Atlantic Canada Opportunities Agency (ACOA # 206200). Financial assistance was also provided by the Natural Sciences and Engineering Research Council of Canada (NSERC).

Author information

Authors and Affiliations

  1. Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Maryam Beheshti Foroutani, Christopher C. Parrish, Jeanette Wells & Matthew L. Rise

  2. Cargill Animal Nutrition, Elk River, MN, 55330, USA

    Richard G. Taylor

Authors
  1. Maryam Beheshti Foroutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher C. Parrish
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeanette Wells
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard G. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matthew L. Rise
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher C. Parrish.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Appendix

Appendix

Table 10 Correlation analysis r values among diet ingredients, elemental composition at week 14, diet (D) lipid classes, diet fatty acid composition, lipid classes of liver (L) and head kidney (HK), and fatty acid composition of liver and head kidney (data with*, **, and *** represent P ≤ 0.05, P ≤ 0.01, and P ≤ 0.001, respectively)
Full size table
Table 11 Correlation analysis r values among diet ingredients, elemental composition at week 14, diet (D) lipid classes, diet fatty acid composition, lipid classes of liver (L) and head kidney (HK), and fatty acid composition of liver and head kidney (data with*, **, and *** represent P ≤ 0.05, P ≤ 0.01, and P ≤ 0.001, respectively)
Full size table
Table 12 Correlation analysis r values among lipid classes of head kidney (HK) and fatty acid composition of head kidney (data with*, **, and *** represent P ≤ 0.05, P ≤ 0.01, and P ≤ 0.001, respectively)
Full size table
Table 13 Lipid classes of liver tissue before and after 14 week of feeding trial (mg g−1 wet weight)
Full size table
Table 14 Fatty acid composition of liver tissue before and after 14 weeks of feeding trial (mg g−1 wet weight)
Full size table
Table 15 Lipid classes of head kidney tissue before and after 14 weeks of feeding trial (mg g−1 wet weight)
Full size table
Table 16 Fatty acid composition of head kidney tissue before and after 14 weeks of feeding trial (mg g−1 wet weight)
Full size table
Fig. 3
figure 3

Principal components analysis of lipid and fatty acid contents (mg g−1 wet weight) in liver tissue (bacterial is the sum of all the bacterial fatty acids, including i15:0, ai15:0, 15:0, 15:1, i16:0, ai16:0, i17:0, ai17:0, 17:0, 17:1, and 18:1ω6)

Full size image
Fig. 4
figure 4

Principal components analysis of lipid and fatty acid contents (mg g−1 wet weight) in head kidney tissue (bacterial is the sum of all the bacterial fatty acids, including i15:0, ai15:0, 15:0, 15:1, i16:0, ai16:0, i17:0, ai17:0, 17:0, 17:1, and 18:1ω6)

Full size image

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Foroutani, M.B., Parrish, C.C., Wells, J. et al. Minimizing marine ingredients in diets of farmed Atlantic salmon (Salmo salar): effects on liver and head kidney lipid class and fatty acid composition. Fish Physiol Biochem 46, 2331–2353 (2020). https://doi.org/10.1007/s10695-020-00862-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00862-0

Keywords

Search

Navigation