Skip to main content
SpringerLink
Log in

n-3 LC-PUFA deposition efficiency and appetite-regulating hormones are modulated by the dietary lipid source during rainbow trout grow-out and finishing periods

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

Abstract

Largely attributable to concerns surrounding sustainability, the utilisation of omega-3 long-chain polyunsaturated fatty acid-rich (n-3 LC-PUFA) fish oils in aquafeeds for farmed fish species is an increasingly concerning issue. Therefore, strategies to maximise the deposition efficiency of these key health beneficial fatty acids are being investigated. The present study examined the effects of four vegetable-based dietary lipid sources (linseed, olive, palm and sunflower oil) on the deposition efficiency of n-3 LC-PUFA and the circulating blood plasma concentrations of the appetite-regulating hormones, leptin and ghrelin, during the grow-out and finishing phases in rainbow trout culture. Minimal detrimental effects were noted in fish performance; however, major modifications were apparent in tissue fatty acid compositions, which generally reflected that of the diet. These modifications diminished somewhat following the fish oil finishing phase, but longer-lasting effects remained evident. The fatty acid composition of the alternative oils was demonstrated to have a modulatory effect on the deposition efficiency of n-3 LC-PUFA and on the key endocrine hormones involved in appetite regulation, growth and feed intake during both the grow-out and finishing phases. In particular, n-6 PUFA (sunflower oil diet) appeared to ‘spare’ the catabolism of n-3 LC-PUFA and, as such, resulted in the highest retention of these fatty acids, ultimately highlighting new nutritional approaches to maximise the maintenance of the qualitative benefits of fish oils when they are used in feeds for aquaculture species.

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

  • Brown TD, Francis DS, Turchini GM (2010) Can dietary lipid source circadian alternation improve omega-3 deposition in rainbow trout? Aquaculture 300:148–155

    Article  CAS  Google Scholar 

  • Codabaccus BM, Carter CG, Bridle AR, Nichols PD (2012) The “n-3 LC-PUFA sparing effect” of modified dietary n-3 LC-PUFA content and DHA to EPA ratio in Atlantic salmon smolt. Aquaculture 356–357:125–140

    Google Scholar 

  • De Silva SS, Gunasekera RM, Ingram BA (2004) Performance of intensively farmed Murray cod Maccullochella peelii peelii (Mitchell) fed newly formulated vs. currently used commercial diets, and a comparison of fillet composition of farmed and wild fish. Aquac Res 35:1039–1052

    Article  Google Scholar 

  • Emery JA, Hermon K, Hamid NKA, Donald JA, Turchini GM (2013) Δ-6 desaturase substrate competition: dietary linoleic acid (18:2n-6) has only trivial effects on α-linolenic acid (18:3n-3) bioconversion in the teleost rainbow trout. PLoS One 8:e57463

    Google Scholar 

  • Eroldoğan TO, Yilmaz AH, Turchini GM, Arslan M, Sirkecioğlu NA, Engin K, Özşahinoğlu I, Mumoğullarinda P (2013) Fatty acid metabolism in European sea bass (Dicentrarchus labrax): effects of n-6 PUFA and MUFA in fish oil replaced diets. Fish Physiol Biochem 39:941–955

    Article  PubMed  Google Scholar 

  • Feltrin KL, Patterson M, Ghatei MA, Bloom SR, Meyer JH, Horowitz M, Feinle-Bisset C (2006) Effect of fatty acid chain length on suppression of ghrelin and stimulation of PYY, GLP-2 and PP secretion in healthy men. Peptides 27:1638–1643

    Article  CAS  PubMed  Google Scholar 

  • Folch JM, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Francis DS, Turchini GM, Jones PL, De Silva SS (2007) Dietary lipid source modulates in vivo fatty acid metabolism in the freshwater fish, Murray cod (Maccullochella peelii peelii). J Agric Food Chem 55:1582–1591

    Article  CAS  PubMed  Google Scholar 

  • Ganga R, Bell JG, Montero D, Robaina L, Caballero MJ, Izquierdo MS (2005) Effect of dietary lipids on plasma fatty acid profiles and prostaglandin and leptin production in gilthead seabream (Sparus aurata). Comp Biochem Physiol Biochem Mol Biol 142:410–418

    Article  CAS  Google Scholar 

  • Geurden I, Cuvier A, Gondouin E, Olsen RE, Ruohonen K, Kaushik S, Boujard T (2005) Rainbow trout can discriminate between feeds with different oil sources. Physiol Behav 85:107–114

    Article  CAS  PubMed  Google Scholar 

  • Geurden I, Corraze G, Boujard T (2007) Self-feeding behaviour of rainbow trout, Oncorhynchus mykiss, offered diets with distinct feed oils. Appl Anim Behav Sci 108:313–326

    Article  Google Scholar 

  • Glencross B, Hawkins W, Curnow J (2003) Evaluation of canola oils as alternative lipid resources in diets for juvenile red seabream, Pagrus auratus. Aquac Nutr 9:305–315

    Article  CAS  Google Scholar 

  • Gormsen LC, Gjedsted J, Gjedde S, Vestergaard ET, Christiansen JS, Jorgensen JO, Nielsen S, Moller N (2006) Free fatty acids decrease circulating ghrelin concentrations in humans. Eur J Endocrinol 154:667–673

    Article  CAS  PubMed  Google Scholar 

  • Karakatsouli N (2012) An overview of the use of fatty acids in fish farming research during the last decade, with particular emphasis on fish quality. J World Aquac Soc 43:291–320

    Article  Google Scholar 

  • Ng WK, Chong CY, Wang Y, Romano N (2013) Effects of dietary fish and vegetable oils on the growth, tissue fatty acid composition, oxidative stability and vitamin E content of red hybrid tilapia and efficacy of using fish oil finishing diets. Aquaculture 372–375:97–110

    Article  Google Scholar 

  • Nishi Y, Hiejima H, Hosoda H, Kaiya H, Mori K, Fukue Y, Yanase T, Nawata H, Kangawa K, Kojima M (2005) Ingested medium-chain fatty acids are directly utilized for the acyl modification of ghrelin. Endocrinology 146:2255–2264

    Article  CAS  PubMed  Google Scholar 

  • Olsen Y (2011) Resources for fish feed in future mariculture. Aquac Environ Interact 1:187–200

    Article  Google Scholar 

  • Palmeri G, Turchini GM, De Silva SS (2007) Lipid characterisation and distribution in the fillet of the farmed Australian native fish, Murray cod (Maccullochella peelii peelii). Food Chem 102:796–807

    Article  CAS  Google Scholar 

  • Pasman WJ, Heimerikx J, Rubingh CM, van den Berg R, O’Shea M, Gambelli L, Hendriks HFJ, Einerhand AWC, Scott C, Keizer HG, Mennen LI (2008) The effect of Korean pine nut oil on in vitro CCK release, on appetite sensations and on gut hormones in post-menopausal overweight women. Lipids Health Dis 7:10. doi:10.1186/1476-511X-7-10

  • Pettersson A, Johnsson L, Brannas E, Pickova J (2009) Effects of rapeseed oil replacement in fish feed on lipid composition and self-selection by rainbow trout (Oncorhynchus mykiss). Aquac Nutr 15:577–586

    Article  CAS  Google Scholar 

  • Rosenlund G, Corraze G, Izquierdo M, Torstensen BE (2011) The effects of fish oil replacement on nutritional and organoleptic qualities of farmed fish. In: Turchini GM, Ng WK, Tocher DR (eds) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press; Taylor & Francis group, Boca Raton, FL, pp 487–522

    Google Scholar 

  • Tacon AGJ, Metian M (2009) Fishing for feed or fishing for food: increasing global competition for small pelagic forage fish. AMBIO 38:294–302

    Article  PubMed  Google Scholar 

  • Thanuthong T, Francis DS, Senadheera SD, Jones PL, Turchini GM (2011a) LC-PUFA biosynthesis in rainbow trout is substrate limited: use of the whole body fatty acid balance method and different 18:3n-3/18:2n-6 ratios. Lipids 46:1111–1127

    Article  CAS  PubMed  Google Scholar 

  • Thanuthong T, Francis DS, Senadheera SD, Jones PL, Turchini GM (2011b) Fish oil replacement in rainbow trout diets and total dietary PUFA content: I) effects on feed efficiency, fat deposition and the efficiency of a finishing strategy. Aquaculture 320:82–90

    Article  CAS  Google Scholar 

  • Thanuthong T, Francis DS, Senadheera SPSD, Jones PL, Turchini GM (2012) Short-term food deprivation before a fish oil finishing strategy improves the deposition of n-3 LC-PUFA, but not the washing-out of C18 PUFA in rainbow trout. Aquac Nutr 18:441–456

    Article  CAS  Google Scholar 

  • Tocher DR, Bell JG, McGhee F, Dick JR, Fonseca-Madrigal J (2003) Effects of dietary lipid level and vegetable oil on fatty acid metabolism in Atlantic salmon (Salmo salar L.) over the whole production cycle. Fish Physiol Biochem 29:193–209

    Article  CAS  Google Scholar 

  • Torstensen BE, Tocher DR (2011) The effects of fish oil replacement on lipid metabolism of fish. In: Turchini GM, Ng WK, Tocher DR (eds) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Taylor & Francis group, Boca Raton, FL, pp 405–438

    Google Scholar 

  • Torstensen BE, Froyland L, Ornsrud R, Lie O (2004) Tailoring of a cardioprotective muscle fatty acid composition of Atlantic salmon (Salmo salar) fed vegetable oils. Food Chem 87:567–580

    Article  CAS  Google Scholar 

  • Trushenski JT (2009) Saturated lipid sources in feeds for sunshine bass: alterations in production performance and tissue fatty acid composition. N Am J Aquac 71:363–373

    Article  Google Scholar 

  • Trushenski JT, Boesenberg J (2009) Influence of dietary fish oil concentration and finishing duration on beneficial fatty acid profile restoration in sunshine bass Morone chrysops female × M. saxatilis male. Aquaculture 296:277–283

    Article  CAS  Google Scholar 

  • Trushenski JT, Kasper CS, Kohler CC (2006) Challenges and opportunities in finfish nutrition. N Am J Aquac 68:122–140

    Article  Google Scholar 

  • Trushenski JT, Lewis HA, Kohler CC (2008) Fatty acid profile of sunshine bass: I. Profile change is affected by initial composition and differs among tissues. Lipids 43:629–641

    Article  CAS  PubMed  Google Scholar 

  • Trushenski JT, Boesenberg J, Kohler CC (2009) Influence of grow-out feed fatty acid composition on finishing success in Nile tilapia. N Am J Aquac 71:242–251

    Article  Google Scholar 

  • Turchini GM, Francis DS (2009) Fatty acid metabolism (desaturation, elongation and beta-oxidation) in rainbow trout fed fish oil- or linseed oil-based diets. Br J Nutr 102:69–81

    Article  CAS  PubMed  Google Scholar 

  • Turchini GM, Paolucci M (2010) Leptin and lipid metabolism in fish. In: Paolucci M (ed) Leptin in non mammalian vertebrates. Transworld Research Network, Kerala, pp 151–172

    Google Scholar 

  • Turchini GM, Francis DS, De Silva SS (2006) Fatty acid metabolism in the freshwater fish Murray cod (Maccullochella peelii peelii) deduced by the whole-body fatty acid balance method. Comp Biochem Physiol B Biochem Mol Biol 144:110–118

    Article  PubMed  Google Scholar 

  • Turchini GM, Francis DS, De Silva SS (2007a) Finishing diets stimulate compensatory growth: results of a study on Murray cod, Maccullochella peelii peelii. Aquac Nutr 13:351–360

    Article  CAS  Google Scholar 

  • Turchini GM, Francis DS, De Silva SS (2007b) A whole body, in vivo, fatty acid balance method to quantify PUFA metabolism (desaturation, elongation and beta-oxidation). Lipids 42:1065–1071

    Article  CAS  PubMed  Google Scholar 

  • Turchini GM, Francis DS, De Silva SS (2008) A whole body, in vivo, fatty acid balance method to quantify PUFA metabolism (desaturation, elongation and beta-oxidation) (vol 42, pg 1065, 2007). Lipids 43:977

    Article  CAS  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, Francis DS, Senadheera SPSD, Thanuthong T, De Silva SS (2011) Fish oil replacement with different vegetable oils in Murray cod: evidence of an “omega-3 sparing effect” by other dietary fatty acids. Aquaculture 315:250–259

    Article  CAS  Google Scholar 

  • Unniappan S, Canosa LF, Peter RE (2004) Orexigenic actions of ghrelin in goldfish: feeding-induced changes in brain and gut mRNA expression and serum levels, and responses to central and peripheral injections. Neuroendocrinology 79:100–108

    Article  CAS  PubMed  Google Scholar 

  • Varricchio E, Russo F, Coccia E, Turchini G, Francis D, De Girolamo P, Paolucci M (2012) Immunohistochemical and immunological detection of ghrelin and leptin in rainbow trout Oncorhynchus mykiss and Murray cod Maccullochella peelii peelii as affected by different dietary fatty acids. Microsc Res Tech 75:771–780

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported under the Australian Research Council’s Discovery Projects funding scheme (Projects DP0772271 and DP1093570). The views expressed herein are those of the authors and are not necessarily those of the Australian Research Council. The authors also express their gratitude to Dr. Richard Smullen (Ridley Aquafeed) for kindly donating the raw materials used for experimental feed preparation.

Author information

Authors and Affiliations

  1. Australian Institute of Marine Science, PMB No 3, Townsville, QLD, 4810, Australia

    D. S. Francis

  2. School of Life and Environmental Sciences, Deakin University, PO Box 423, Warrnambool, VIC, 3280, Australia

    D. S. Francis, T. Thanuthong, S. P. S. D. Senadheera, S. S. De Silva & G. M. Turchini

  3. Faculty of Agricultural Technology, Songkhla Rajabhat University, Songkhla, 90000, Thailand

    T. Thanuthong

  4. Ocean University (National Institute of Fisheries and Nautical Engineering), Colombo 15, Sri Lanka

    S. P. S. D. Senadheera

  5. Department of Sciences and Technologies, University of Sannio, Via Port’Arsa, 11, 82100, Benevento, Italy

    M. Paolucci & E. Coccia

Authors
  1. D. S. Francis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Thanuthong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. P. S. D. Senadheera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Paolucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Coccia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. S. De Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. M. Turchini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. S. Francis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Francis, D.S., Thanuthong, T., Senadheera, S.P.S.D. et al. n-3 LC-PUFA deposition efficiency and appetite-regulating hormones are modulated by the dietary lipid source during rainbow trout grow-out and finishing periods. Fish Physiol Biochem 40, 577–593 (2014). https://doi.org/10.1007/s10695-013-9868-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-013-9868-5

Keywords

Search

Navigation