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Dietary inclusion of Antarctic krill meal during the finishing feed period improves health and fillet quality of Atlantic salmon (Salmo salar L.)

  • Turid Mørkøre (a1) (a2), Helena M. Moreno (a3), Javier Borderías (a3), Thomas Larsson (a1), Hege Hellberg (a4), Bjarne Hatlen (a1), Odd Helge Romarheim (a1), Bente Ruyter (a1), Carlo C. Lazado (a5), Raúl Jiménez-Guerrero (a1), Målfrid T. Bjerke (a1), Tibiabin Benitez-Santana (a6) and Aleksei Krasnov (a5)...

Abstract

There is an urgent need to find alternative feed resources that can further substitute fishmeal in Atlantic salmon diets without compromising health and food quality, in particular during the finishing feeding period when the feed demand is highest and flesh quality effects are most significant. This study investigates efficacy of substituting a isoprotein (35 %) and isolipid (35 %) low fishmeal diet (FM, 15 %) with Antarctic krill meal (KM, 12 %) during 3 months with growing finishing 2·3 kg salmon (quadruplicate sea cages/diet). Final body weight (3·9 (se 0·04) kg) was similar in the dietary groups, but the KM group had more voluminous body shape, leaner hearts and improved fillet integrity, firmness and colour. Ectopic epithelial cells and focal Ca deposits in intestine were only detected in the FM group. Transcriptome profiling by microarray of livers showed dietary effects on several immune genes, and a panel of structural genes were up-regulated in the KM group, including cadherin and connexin. Up-regulation of genes encoding myosin heavy chain proteins was the main finding in skeletal muscle. Morphology examination by scanning electron microscopy and secondary structure by Fourier transform IR spectroscopy revealed more ordered and stable collagen architecture of the KM group. NEFA composition of skeletal muscle indicated altered metabolism of n-3, n-6 and SFA of the KM group. The results demonstrated that improved health and meat quality in Atlantic salmon fed krill meal were associated with up-regulation of immune genes, proteins defining muscle properties and genes involved in cell contacts and adhesion, altered fatty acid metabolism and fat deposition, and improved gut health and collagen structure.

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Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

*Corresponding author: Turid Mørkøre, fax +47 64965101, email turid.morkore@nmbu.no

References

Hide All
1.Green, K (2016) Fishmeal and fish oil facts and figures. https://www.seafish.org/media/publications/SeafishFishmealandFishOilFactsandFigures_201612.pdf (accessed September 2019)
2.New, MB & Wijkström, UN (2002) Use of Fishmeal and Fish Oil in Aquafeeds: Further Thoughts on the Fishmeal Trap. Rome: Food and Agriculture Organization of the United Nations.
3.Ytrestøyl, T, Aas, TS & Åsgård, T (2015) Utilisation of feed resources in production of Atlantic salmon (Salmo salar) in Norway. Aquaculture 448, 365374.
4.Norwegian Seafood Federation (2019) Akvafakta. https://akvafakta.no/wp-content/uploads/Maned/siste.pdf (accessed September 2019)
5.Xie, D, Gong, M, Wei, W, et al. (2019) Antarctic krill (Euphausia superba) oil: a comprehensive review of chemical composition, extraction technologies, health benefits, and current applications. Compr Rev Food Sci Food Saf 18, 514534.
6.Hertrampf, JW & Piedad-Pascual, F (2012) Handbook on Ingredients for Aquaculture Feeds. Berlin: Springer Science & Business Media.
7.Tou, JC, Jaczynski, J & Chen, Y-C (2007) Krill for human consumption: nutritional value and potential health benefits. Nutr Rev 65, 6377.
8.Köhler, A, Sarkkinen, E, Tapola, N, et al. (2015) Bioavailability of fatty acids from krill oil, krill meal and fish oil in healthy subjects – a randomized, single-dose, cross-over trial. Lipids Health Dis 14, 19.
9.Everson, I (2008) Krill: Biology, Ecology and Fisheries. Hoboken, NJ: John Wiley & Sons.
10.Burri, L & Nunes, A (2016) Benefits of including krill meal in shrimp diets. World Aquacult 1923.
11.Storebakken, T (1988) Krill as a potential feed source for salmonids. Aquaculture 70, 193205.
12.Anderson, JS (1997) The Evaluation of Air-dried Whole Krill Meal as a Dietary Protein Supplement for Juvenile Chinook Salmon (Oncorhynchus Tshawytscha). Canadian Technical Report of Fisheries and Aquatic Sciences no. 2148. Science Branch, Pacific Region, West Vancouver, B.C.: Department of Fisheries & Oceans.
13.Kubitza, F & Lovshin, LL (1997) Effects of initial weight and genetic strain on feed training largemouth bass Micropterus salmoides using ground fish flesh and freeze dried krill as starter diets. Aquaculture 148, 179190.
14.Olsen, RE, Suontama, J, Langmyhr, E, et al. (2006) The replacement of fish meal with Antarctic krill, Euphausia superba in diets for Atlantic salmon, Salmo salar. Aquacult Nutr 12, 280290.
15.Suontama, J, Kiessling, A, Melle, W, et al. (2007) Protein from Northern krill (Thysanoessa inermis), Antarctic krill (Euphausia superba) and the Arctic amphipod (Themisto libellula) can partially replace fish meal in diets to Atlantic salmon (Salmo salar) without affecting product quality. Aquacult Nutr 13, 5058.
16.Hatlen, B, Berge, K, Nordrum, S, et al. (2017) The effect of low inclusion levels of Antarctic krill (Euphausia superba) meal on growth performance, apparent digestibility and slaughter quality of Atlantic salmon (Salmo salar). Aquacult Nutr 23, 721729.
17.Aas, TS, Ytrestøyl, T & Åsgård, T (2019) Utilization of feed resources in the production of Atlantic salmon (Salmo salar) in Norway: an update for 2016. Aquacult Rep 15, 100216.
18.Thomassen, M, Gudding, R, Norberg, B, et al. (2007) Aquaculture Research: From Cage to Consumption. Oslo: Research Council of Norway.
19.Rasmussen, RS (2001) Quality of farmed salmonids with emphasis on proximate composition, yield and sensory characteristics. Aquacult Res 32, 767786.
20.Mørkøre, T & Rørvik, K-A (2001) Seasonal variations in growth, feed utilisation and product quality of farmed Atlantic salmon (Salmo salar) transferred to seawater as 0+ smolts or 1+ smolts. Aquaculture 199, 145157.
21.Folkestad, A, Rørvik, KA, Kolstad, K, et al. (2008) Growth rates of individual farmed Atlantic salmon Salmo salar L. influence the texture of raw and smoked fillets. Aquacult Res 39, 329332.
22.Koteng, DF (1992) Markedsundersøkelse norsk laks (Market Investigation Norwegian salmon). Prosjekt God Fisk. Bergen: Fiskerinæringens Landsforening (FHL) (In Norwegian).
23.Michie, I (2001) Causes of downgrading in the salmon industry. In Farmed Fish Quality, pp. 129136 [Kestin, SC and Warris, P, editors]. Oxford: Blackwell Science.
24.National Research Council (2011) Nutrient Requirements of Fish and Shrimp. Washington, DC: The National Academies Press. https://doi.org/10.17226/13039
25.Thivend, P, Mercier, C & Guilbot, A (1972) Determination of starch with glucoamylase. In General Carbohydrate Method, pp. 100105 [Whistler, R and Bemiller, J, editors]. New York: Academic Press.
26.Ytrestøyl, T, Struksnæs, G, Rørvik, K-A, et al. (2006) Astaxanthin digestibility as affected by ration levels for Atlantic salmon, Salmo salar. Aquaculture 261, 215224.
27.Kousoulaki, K, Mørkøre, T, Nengas, I, et al. (2016) Microalgae and organic minerals enhance lipid retention efficiency and fillet quality in Atlantic salmon (Salmo salar L.). Aquaculture 451, 4757.
28.Wall, T & Bjerkas, E (1999) A simplified method of scoring cataracts in fish. Bull Eur Ass Fish Pathol 19, 162165.
29.Tietz, NW (1995) Clinical Guide to Laboratory Tests, 3rd ed. Philadelphia, PA: WB Saunders Company.
30.Krasnov, A, Timmerhaus, G, Afanasyev, S, et al. (2011) Development and assessment of oligonucleotide microarrays for Atlantic salmon (Salmo salar L.). Comp Biochem Physiol D Genomics Proteomics 6, 3138.
31.Erikson, U, Bye, G & Oppedal, K (2009) Fastere filet–industritest og opplæring (Firmer fillet - industry test and training). SINTEF rapport no. SFH80. Trondheim: SINTEF (In Norwegian).
32.Mørkøre, T & Einen, O (2003) Relating sensory and instrumental texture analyses of Atlantic salmon. J Food Sci 68, 14921497.
33.Norges Standardiseringsforbund (1994) Atlantic salmon – Reference sampling for quality measurements. In NS9401. Oslo: Norges Standardiseringsforbund.
34.Folch, J, Lees, M & Sloane Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497509.
35.Mason, ME, Eager, ME & Waller, GR (1964) A procedure for the simultaneous quantitative determination of glycerol and fatty acid contents of fats and oils. Anal Chem 36, 587590.
36.Bou, M, Berge, GM, Baeverfjord, G, et al. (2017) Low levels of very-long-chain n-3 PUFA in Atlantic salmon (Salmo salar) diet reduce fish robustness under challenging conditions in sea cages. J Nutr Sci 6, e32.
37.Borderias, AJ & Montero, P (1985) Changes in fish muscle collagen during frozen storage. In Storage Lives of Chilled and Frozen Products, Proceedings of Meetings of Commissions C2 and D3 of IIR, pp. 6571 [International Institute of Refrigeration, editors]. Paris: International Institute of Refrigeration.
38.Moreno, H, Montero, M, Gómez-Guillén, M, et al. (2012) Collagen characteristics of farmed Atlantic salmon with firm and soft fillet texture. Food Chem 134, 678685.
39.Sigurgisladottir, S, Hafsteinsson, H, Jonsson, A, et al. (1999) Textural properties of raw salmon fillets as related to sampling method. J Food Sci 64, 99104.
40.Nortvedt, R (1996) Anvendelse av kjemometri innen forskning og industri (Application of Chemometrics in Research and Industry). Oslo: Tidsskriftforlaget Kjemi.
41.Eckhoff, KM, Aidos, I, Hemre, G-I, et al. (1998) Collagen content in farmed Atlantic salmon (Salmo salar, L.) and subsequent changes in solubility during storage on ice. Food Chem 62, 197200.
42.Kirschner, C, Ofstad, R, Skarpeid, H-J, et al. (2004) Monitoring of denaturation processes in aged beef loin by Fourier transform infrared microspectroscopy. J Agric Food Chem 52, 39203929.
43.Iversen, A & Kosmo, J (2004) Kan vekstindeksene sammenlignes (Can growth indices be compared). Norsk Fiskeoppdrett no. 4/2004. Bergen.
44.Iversen, A, Hermansen, Ø, Nystøyl, R, et al. (2017) Kostnadsutvikling i lakseoppdrett–med fokus på fôr-og lusekostnader (Cost development in salmon farming - focusing on feed and lice costs). Nofima rapportserie no. 37/2018. Tromsø: Nofima.
45.Mørkøre, T, Vallet, J, Cardinal, M, et al. (2001) Fat content and fillet shape of Atlantic salmon: relevance for processing yield and quality of raw and smoked products. J Food Sci 66, 13481354.
46.Alne, H, Oehme, M, Thomassen, M, et al. (2011) Reduced growth, condition factor and body energy levels in Atlantic salmon Salmo salar L. during their first spring in the sea. Aquacult Res 42, 248259.
47.Dessen, J-E, Weihe, R, Hatlen, B, et al. (2017) Different growth performance, lipid deposition, and nutrient utilization in in-season (S1) Atlantic salmon post-smolt fed isoenergetic diets differing in protein-to-lipid ratio. Aquaculture 473, 345354.
48.Rørvik, KA, Dessen, JE, Åsli, M, et al. (2018) Low body fat content prior to declining day length in the autumn significantly increased growth and reduced weight dispersion in farmed Atlantic salmon Salmo salar L. Aquacult Res 49, 19441956.
49.De Pitta, C, Biscontin, A, Albiero, A, et al. (2013) The Antarctic krill Euphausia superba shows diurnal cycles of transcription under natural conditions. PLOS ONE 8, e68652.
50.Lumeij, J & Westerhof, I (1987) Blood chemistry for the diagnosis of hepatobiliary disease in birds. A review. Vet Quart 9, 255261.
51.Hansen, , Penn, M, Øverland, M, et al. (2010) High inclusion of partially deshelled and whole krill meals in diets for Atlantic salmon (Salmo salar). Aquaculture 310, 164172.
52.Sandnes, K, Lie, Ø & Waagbø, R (1988) Normal ranges of some blood chemistry parameters in adult farmed Atlantic salmon, Salmo salar. J Fish Biol 32, 129136.
53.Marchesini, G, Moscatiello, S, Di Domizio, S, et al. (2008) Obesity-associated liver disease. J Clin Endocrinol Metab 93, 7480.
54.Tacon, AGJ (1992) Nutritional Fish Pathology. Morphological Signs of Nutrient Deficiency and Toxicity in Farmed Fish. FAO Fish Technical Paper 330, 75.
55.Feingold, KR & Grunfeld, C (2018) Introduction to lipids and lipoproteins. In Endotext [Internet]. MDText. com, Inc.
56.Burri, L, Berge, K, Wibrand, K, et al. (2011) Differential effects of krill oil and fish oil on the hepatic transcriptome in mice. Front Genet 2, 45.
57.Nicolas, A, Aubert, R, Bellili-Munoz, N, et al. (2017) T-cadherin gene variants are associated with type 2 diabetes and the fatty liver index in the French population. Diabetes Metab 43, 3339.
58.Willebrords, J, Cogliati, B, Pereira, IVA, et al. (2017) Inhibition of connexin hemichannels alleviates non-alcoholic steatohepatitis in mice. Sci Rep 7, 8268.
59.Reid, A, Young, K & Lumsden, J (2011) Rainbow trout Oncorhynchus mykiss ladderlectin, but not intelectin, binds viral hemorrhagic septicemia virus IVb. Dis Aquat Organ 95, 137143.
60.Young, KM, Russell, S, Smith, M, et al. (2007) Bacterial-binding activity and plasma concentration of ladderlectin in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 23, 305315.
61.Russell, S, Young, K, Smith, M, et al. (2008) Cloning, binding properties, and tissue localization of rainbow trout (Oncorhynchus mykiss) ladderlectin. Fish Shellfish Immunol 24, 669683.
62.Waagbø, R, Berntssen, M, Danielsen, T, et al. (2013) Feeding Atlantic salmon diets with plant ingredients during the seawater phase – a full-scale net production of marine protein with focus on biological performance, welfare, product quality and safety. Aquacult Nutr 19, 598618.
63.Bjørgen, H, Koppang, EO, Gunnes, G, et al. (2018) Ectopic epithelial cell clusters in salmonid intestine are associated with inflammation. J Fish Dis 41, 10311040.
64.Dale, OB, Tørud, B, Kvellestad, A, et al. (2009) From chronic feed-induced intestinal inflammation to adenocarcinoma with metastases in salmonid fish. Cancer Research 69, 43554362.
65.Simpson, K, Katayama, T, Chichester, C, et al. (1981) Carotenoids as Colorants and Vitamin A Precursors. New York: Academic Press.
66.Torgersen, JS, Koppang, EO, Stien, LH, et al. (2014) Soft texture of Atlantic salmon fillets is associated with glycogen accumulation. PLOS ONE 9, e85551.
67.Nordberg, M (2018) Seasonal variation in fillet quality of Atlantic salmon (Salmo salar). Master Thesis, Norwegian University of Life Sciences, Ås.
68.Anderson, S (2000) Salmon color and the consumer. Microbehavior and Macroresults: Proceedings of the Tenth Biennial Conference of the International Institute of Fisheries Economics and Trade, 10-14 July 2000, Corvallis, OR, USA. https://ir.library.oregonstate.edu/concern/conference_proceedings_or_journals/9s1616848
69.Torrissen, O, Hardy, R & Shearer, K (1989) Pigmentation of salmonids-carotenoid deposition and metabolism. CRC Crit Rev Aquat Sci 1, 209225.
70.Johnston, IA, Alderson, R, Sandham, C, et al. (2000) Muscle fibre density in relation to the colour and texture of smoked Atlantic salmon (Salmo salar L.). Aquaculture 189, 335349.
71.Mørkøre, T, Larsson, T, Kvellestad, AS, et al. (2015) Mørke flekker i laksefilet. Kunnskapsstatus og tiltak for å begrense omfanget (Dark spots in salmon fillets. Knowledge status and measures to reduce prevalence). Nofima rapportserie no. 34/2015. Tromsø: Nofima.
72.Moreno, H, Jacq, C, Montero, M, et al. (2016) Effect of selective breeding on collagen properties of Atlantic salmon (Salmo salar L.). Food Chem 190, 856863.
73.Priego-Capote, F, Scherl, A, Müller, M, et al. (2010) Glycation isotopic labeling with 13C-reducing sugars for quantitative analysis of glycated proteins in human plasma. Mol Cell Proteomics 9, 579592.
74.Tskhovrebova, L & Trinick, J (2012) Making muscle elastic: the structural basis of myomesin stretching. PLoS Biol 10, e1001264.

Keywords

Dietary inclusion of Antarctic krill meal during the finishing feed period improves health and fillet quality of Atlantic salmon (Salmo salar L.)

  • Turid Mørkøre (a1) (a2), Helena M. Moreno (a3), Javier Borderías (a3), Thomas Larsson (a1), Hege Hellberg (a4), Bjarne Hatlen (a1), Odd Helge Romarheim (a1), Bente Ruyter (a1), Carlo C. Lazado (a5), Raúl Jiménez-Guerrero (a1), Målfrid T. Bjerke (a1), Tibiabin Benitez-Santana (a6) and Aleksei Krasnov (a5)...

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