Abstract
Two fish species reared in aquaculture (pink salmon Oncorhynchus gorbuscha and whitefish Coregonus lavaretus) and ten fish species from natural habitats (whitefish C. lavaretus, tugun Coregonus tugun, broad whitefish Coregonus nasus, least cisco Coregonus sardinella, vendace Coregonus albula, boganid charr Salvelinus boganidae, charr Salvelinus alpinus complex, northern pike Esox lucius, sharp-snouted lenok Brachymystax lenok, and taimen Hucho taimen) have been studied. The content of two long-chain polyunsaturated omega-3 fatty acids (PUFAs), eicosapentaenoic acid (20:5n-3, EPA) and docosahexaenoic acid (22:6n-3, DHA), in the muscle tissue of the fish and in their food (intestine contents) are compared. In the aquacultures of whitefish and pink salmon, the total content of EPA and DHA is significantly higher in feed than in the muscle tissue of the fish, which indicates losses of PUFA in the two-link food chain of the aquaculture during their transfer to the upper trophic level. EPA and DHA losses in aquaculture, which are confirmed by numerous literature data, mean an inefficient usage of the available sources of PUFAs and the aggravation of the global deficit of these biochemicals in the human diet. A study of natural fish populations reveals the accumulation of EPA and DHA in their biomass compared to food in many cases, although opposite phenomena are also observed. An assumption on the presence of an optimal, physiologically adequate species-specific level of PUFA in the fish muscle tissue has been made based on our data and literature data. If the level of PUFAs in the muscles is lower than optimal, their accumulation (bioaccumulation) from food and/or de novo synthesis are observed. When the optimal level is exceeded, the content of EPA and DHA in biomass approaches maximum species-specific values; however, part of these PUFAs entering from food is not digested or is catabolized. According to the obtained data, the species of the order Salmoniformes have an optimal level of 2 to 6 mg/g of wet weight. It has been found that in aquaculture approaching to maximum values of EPA + DHA content was accompanied by their losses (scattering) in the food chains, while in natural ecosystems the maximum values of PUFA content in the fish biomass are achieved by their accumulation from the lower trophic level. Boganid charr S. boganidae had the highest content of EPA + DHA in the muscle tissue among all known fish species (32.78 mg/g of wet weight).
Similar content being viewed by others
References
Adkins, Y. and Kelley, D.S., Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids, J. Nutr. Biochem., 2010, vol. 21, pp. 781–792.
Ahlgren, G., Sonesten, L., Boberg, M., and Gustafsson, I.-B., Fatty acid content of some freshwater fish in lakes of different trophic levels—a bottom-up effect? Ecol. Freshwater Fish., 1996, vol. 5, pp. 15–27.
Albert, B.B., Derraik, J.G.B., Cameron-Smith, D., Hofman, P.L., Tumanov, S., Villas-Boas, S.G., Garg, M.L., and Cutfield, W.S., Fish oil supplements in New Zealand are highly oxidized and do not meet label content of n-3 PUFA, Sci. Rep., 2015, vol. 5, p. 7928.
Amira, M.B., Hanene, J.H., Madiha, D., Imen, B., Mohamed, H., and Abdelhamid, C., Effects of frying on the fatty acid composition in farmed and wild gilthead sea bream (Sparus aurata), Int. J. Food Sci. Technol., 2010, vol. 45, pp. 113–123.
Bazan, N.G., Cellular and molecular events mediated by docosahexaenoic acid-derived neuroprotectin D1 signaling in photoreceptor cell survival and brain protection, Prostaglandins, Leukotrienes Essent. Fatty Acids, 2009, vol. 81, pp. 205–211.
Beloe more i ego vodosbor pod vliyaniem klimaticheskikh i antropogennykh faktorov (The White Sea and Its Watershed Affected by Climate and Anthropogenic Factors), Filatov, N.N. and Terzhevik, A.Yu., Eds., Petrozavodsk: Karel. Nauch. Tsentr, Ross. Akad. Nauk, 2007.
Benedito-Palos, L., Calduch-Giner, J.A., Ballester-Lozano, G.F. and Perez-Sanchez, J., Effect of ration size on fillet fatty acid composition, phospholipid allostasis and mRNA expression patterns of lipid regulatory genes in gilthead seabream (Sparus aurata), Br. J. Nutr., 2013, vol. 109, pp. 1175–1187.
Bioresursy Onezhskogo ozera (Biological Resources of the Onega Lake), Petrozavodsk: Karel. Nauch. Tsentr, Ross. Akad. Nauk, 2008.
Broadhurst, C.L., Wang, Y., Crawford, M.A., Cunnane, S.C., Parkington, J.E., and Schmidt, W.F., Brain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2002, vol. 131, pp. 653–673.
Broughton, K.S., Johnson, C.S., Pace, B.K., Liebman, M., and Kleppinger, K.M., Reduced asthma symptoms with n-3 fatty acid ingestion are related to 5-series leukotriene production, Am. J. Clin. Nutr., 1997, vol. 65, pp. 1011–1017.
Codabaccus, B.M., Carter, C.G., Bridle, A.R., and Nichols, P.D., 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, 2012, vols. 356–357, pp. 135–140.
Davis, B.C. and Kris-Etherton, P.M., Achieving optimal essential fatty acid status in vegetarians: current knowledge and practical implications, Am. J. Clin. Nutr., 2003, vol. 78, suppl., pp. 640S–646S.
De Caterina, R., n–3 Fatty acids in cardiovascular disease, N. Engl. J. Med., 2011, vol. 364, pp. 2439–2450.
Elvevoll, E.O., Barstad, H., Breimo, E.S., Brox, J., Eilertsen, K.-E., Lund, T., Olsen, J.O., and Østerud, B., Enhanced incorporation of n-3 fatty acids from fish compared with fish oils, Lipids, 2006, vol. 41, pp. 1109–1114.
Emery, A.F., Norambuena, F., Trushenski, J., and Turchini, G.M., Uncoupling of EPA and DHA in fish nutrition: dietary demand is limited in Atlantic salmon and effectively met by DHA alone, Lipids, 2016, vol. 51, pp. 399–412.
Fasolato, L., Novelli, E., Salmaso, L., Corain, L., Camin, F., Perini, M., Antonetti, P., and Balzan, S., Application of nonparametric multivariate analyses to the authentication of wild and farmed European sea bass (Dicentrarchus labrax): results of a survey on fish sampled in the retail trade, J. Agric. Food Chem., 2010, vol. 58, pp. 10979–10988.
Garg, M.L., Wood, L.G., Singh, H., and Moughan, P.J., Means of delivering recommended levels of long chain n-3 polyunsaturated fatty acids in human diets, J. Food Sci., 2006, vol. 71, pp. 66–71.
Gladyshev, M.I., Gribovskaya, I.V., and Adamovich, V.V., Disappearance of phenol in water samples taken from the Yenisei River and the Krasnoyarsk reservoir, Water Res., 1993, vol. 27, pp. 1063–1070.
Gladyshev, M.I., Arts, M.T., and Sushchik, N.N., Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terrestrial ecosystems, in Lipids in Aquatic Ecosystems, Arts,M.T., Kainz, M., and Brett, M.T., Eds., New York: Springer-Verlag, 2009, pp. 179–209.
Gladyshev, M.I., Sushchik, N.N., Anishchenko, O.V., Makhutova, O.N., Kolmakov, V.I., Kalachova, G.S., Kolmakova, A.A., and Dubovskaya, O.P., Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir, Oecologia, 2011, vol. 165, pp. 521–531.
Gladyshev, M.I., Sushchik, N.N., Makhutova, O.N., Kalachova, G.S., and Malyshevskaya, K.K., Differences in fatty acid composition of food and tissues of grayling from the Yenisei River, Dokl. Biochem. Biophys., 2012, vol. 445, no. 1, pp. 194–196.
Gladyshev, M.I., Sushchik, N.N., and Makhutova, O.N., Production of EPA and DHA in aquatic ecosystems and their transfer to the land, Prostaglandins Other Lipid Mediators, 2013, vol. 107, pp. 117–126.
Gladyshev, M.I., Sushchik, N.N., Gubanenko, G.A., Makhutova, O.N., Kalachova, G.S., Rechkina, E.A., and Malyshevskaya, K.K., Effect of the way of cooking on contents of essential polyunsaturated fatty acids in filets of zander, Czech J. Food Sci., 2014, vol. 32, pp. 226–231.
Gladyshev, M.I., Kolmakova, O.V., Tolomeev, A.P., Anishchenko, O.V., Makhutova, O.N., Kolmakova, A.A., Kravchuk, E.S., Glushchenko, L.A., Kolmakov, V.I., and Sushchik, N.N. Differences in organic matter and bacterioplankton between sections of the largest Arctic river: Mosaic or continuum? Limnol. Oceanogr., 2015a, vol. 60, pp. 1314–1331.
Gladyshev, M.I., Makhutova, O.N., Gubanenko, G.A., Rechkina, E.A., Kalachova, G.S., and Sushchik, N.N., Livers of terrestrial production animals as a source of long-chain polyunsaturated fatty acids for humans: An alternative to fish? Eur. J. Lipid Sci. Technol., 2015b, vol. 117, pp. 417–1421.
Goulden, C.E. and Place, A.R., Fatty acid synthesis and accumulation rates in daphniids, J. Exp. Zool., 1990, vol. 256, pp. 168–178.
Gritsevskaya, G.L., Kyabileva, G.K., Nikolaeva, L.A., and Semenov, V.N., Hydrology and hydrochemistry of the Solovetsky lakes, Tr. Sev. Otd. Gos. Nauchno-Issled. Inst. Ozern. Rechn. Rybn. Khoz., 1972, vol. 6, pp. 5–44.
Guler, G.O., Aktumsek, A., Cakmak, Y.S., Zengin, G., and Citil, O.B., Effect of season on fatty acid composition and n-3/n-6 ratios of zander and carp muscle lipids in Altinapa Dam Lake, J. Food Sci., 2011, vol. 76, pp. C594–C597.
Hansen, J.Ø., Berge, G.M., Hillestad, M., Krogdahl, Å., Galloway, T.F., Holm, H., Holm, J., and Ruyter, B., Apparent digestion and apparent retention of lipid and fatty acids in Atlantic cod (Gadus morhua) fed increasing dietary lipid levels, Aquaculture, 2008, vol. 284, pp. 159–166.
Harris, W.S., Mozaffarian, D., Lefevre, M., Toner, C.D., Colombo, J., Cunnane, S.C., Holden, J.M., Klurfeld, D.M., Morris, M.C., and Whelan, J., Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids, J. Nutr., 2009, vol. 139, pp. 804S–819S.
Hartwich, M., Martin-Creuzburg, D., and Wacker, A., Seasonal changes in the accumulation of polyunsaturated fatty acids in zooplankton, J. Plankton Res., 2013, vol. 35, pp. 121–134.
Henriques, J., Dick, J.R., Tocher, D.R., and Bell, J.G., Nutritional quality of salmon products available from major retailers in the UK: content and composition of n-3 long-chain PUFA, Br. J. Nutr., 2014, vol. 112, pp. 964–975.
Hibbeln, J.R., Nieminen, L.R.G., Blasbalg, T.L., Riggs, J.A., and Lands, W.E.M., Healthy intakes of n-3 and n-6 fatty acids: estimations considering worldwide diversity, Am. J. Clin. Nutr., 2006, vol. 83, pp. 1483S–1493S.
Hightower, J.M. and Moore, D., Mercury levels in highend consumers of fish, Environ. Health Perspect., 2003, vol. 111, pp. 604–608. doi doi 10.1289/ehp.5837available
Hixson, S.M., Sharma, B., Kainz, M.J., Wacker, A., and Arts, M.T., Production, distribution, and abundance of long-chain omega-3 polyunsaturated fatty acids: a fundamental dichotomy between freshwater and terrestrial ecosystems, Environ. Rev., 2015, vol. 23, pp. 414–424.
Hulbert, A.J., Membrane fatty acids as pacemakers of animal metabolism, Lipids, 2007, vol. 42, pp. 811–819.
Hulbert, A.J., Faulks, S., Buttemer, W.A., and Else, P.L., Acyl composition of muscle membranes varies with body size in birds, J. Exp. Biol., 2002, vol. 205, pp. 3561–3569.
Huynh, M.D. and Kitts, D.D., Evaluating nutritional quality of pacific fish species from fatty acid signatures, Food Chem., 2009, vol. 114, pp. 912–918.
Infante, J.P., Kirwan, R.C., and Brenna, J.T., High levels of docosahexaenoic acid (22:6n-3)-containing phospholipids in high-frequency contraction muscles of hummingbirds and rattlesnakes, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2001, vol. 130, pp. 291–298.
Kainz, M., Telmer, K., and Mazumder, A., Bioaccumulation patterns of methyl mercury and essential fatty acids in lacustrine planktonic food webs and fish, Sci. Total Environ., 2006, vol. 368, pp. 271–282.
Kainz, M., Arts, M.T., and Mazumder, A., Essential versus potentially toxic dietary substances: a seasonal comparison of essential fatty acids and methyl mercury concentrations in the planktonic food web, Environ. Pollut., 2008, vol. 155, pp. 262–270.
Kainz, M.J., Hager, H.H., Rasconi, S., Kahilainen, K.K., Amundsen, P.-A., and Hayden, B., Polyunsaturated fatty acids in fishes increase with total lipids irrespective of feeding sources and trophic position, Ecosphere, 2017, vol. 8, no. 4, p. e01753. doi 10.1002/ecs2.1753
Kiessling, A., Pickova, J., Johansson, L., Åsgård, T., Storebakken, T., and Kiessling, K-H., Changes in fatty acid composition in muscle and adipose tissue of farmed rainbow trout (Oncorhynchus mykiss) in relation to ration and age, Food Chem., 2001, vol. 73, pp. 271–284.
Kolanowski, W., Omega-3 LC PUFA contents and oxidative stability of encapsulated fish oil dietary supplements, Int. J. Food Prop., 2010, vol. 13, pp. 498–511.
Kousoulaki, K., Mørkøre, T., Nengas, I., Berge, R.K., and Sweetman, J., Microalgae and organic minerals enhance lipid retention efficiency and fillet quality in Atlantic salmon (Salmo salar L.), Aquaculture, 2016, vol. 451, pp. 47–57.
Kris-Etherton, P.M., Grieger, J.A., and Etherton, T.D., Dietary reference intakes for DHA and EPA, Prostaglandins, Leukotrienes Essent. Fatty Acids, 2009, vol. 81, pp. 99–104.
Kris-Etherton, P.M., Harris, W.S., and Appel, L.J., Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease, Circulation, 2002, vol. 106, pp. 2747–2757.
Larsen, D., Quek, S.Y., and Eyres, L., Effect of cooking method on the fatty acid profile of New Zealand king salmon (Oncorhynchus tshawytscha), Food Chem., 2010, vol. 119, pp. 785–790.
Lauritzen, L., Hansen, H.S., Jorgensen, M.H., and Michaelsen, K.F., The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina, Progr. Lipid Res., 2001, vol. 40, pp. 1–94.
Leaver, M.J., Taggart, J.B., Villeneuve, L., Bron, J.E., Guy, D.R., Bishop, S.C., Houston, R.D., Matika, O., and Tocher, D.R., Heritability and mechanisms of n-3 long chain polyunsaturated fatty acid deposition in the flesh of Atlantic salmon, Comp. Biochem. Physiol., Part D: Genomics Proteomics, 2011, vol. 6, pp. 62–69.
Leonov, A.V., Filatov, N.N., Zdorovennov, R.E., and Zdorovennova, G.E., Mathematical modeling of the ecosystem functioning conditions in the Chupa estuary of the White Sea: transformation of organogenic substances and bioproductivity of the marine environment, Water Resour., 2006, vol. 33, no. 5, pp. 543–567.
Litzow, M.A., Bailey, K.M., Prahl, F.G., and Heintz, R., Climate regime shifts and reorganization of fish communities: the essential fatty acid limitation hypothesis, Mar. Ecol.: Progr. Ser., 2006, vol. 315, pp. 1–11.
Mairesse, G., Thomas, M., Gardeur, J.-N., and Brun-Bellut, J., Effects of geographic source rearing system, and season on the nutritional quality of wild and farmed Perca fluviatilis, Lipids, 2006, vol. 41, pp. 221–229.
McNamara, R.K. and Carlson, S.E., Role of omega-3 fatty acids in brain development and function: Potential implications for the pathogenesis and prevention of psychopathology, Prostaglandins, Leukotrienes Essent. Fatty Acids, 2006, vol. 75, pp. 329–349.
Moths, M.D., Dellinger, J.A., Holub, B., Ripley, M.P., McGraw, J.E. and Kinnunen, R.E., Omega-3 fatty acids in fish from the Laurentian Great Lakes tribal fisheries, Hum. Ecol. Risk Assess., 2013, vol. 19, pp. 1628–1643.
Nagasaka, R., Gagnon, C., Swist, E., Rondeau, I., Massarelli, I., Cheung, W., and Ratnayake, W.M.N., EPA and DHA status of South Asian and white Canadians living in the national capital region of Canada, Lipids, 2014, vol. 49, pp. 1057–1069.
Norris, P.C and Dennis, E.A., Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signaling, Proc. Natl. Acad. Sci. U.S.A., 2012, vol. 109, pp. 8517–8522.
Onezhskoe ozero. Atlas (Atlas of the Onega Lake), Filatov, N.N., Ed., Petrozavodsk: Karel. Nauch. Tsentr, Ross. Akad. Nauk, 2010.
Pichugin, M.Yu., The development of an artificial hybrid and revealing elements of reproductive isolation between sympatric forms of Dryagin’s char and Salvelinus alpinus complex (Salmonidae) from Sobachye Mountain Lake (Taimyr), J. Ichthyol., 2009, vol. 49, no. 3, pp. 236–248.
Plourde, M. and Cunnane, S.C., Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements, Appl. Physiol. Nutr. Metab., 2007, vol. 32, pp. 619–634.
Robert, S.S., Production of eicosapentaenoic and docosahexaenoic acid-containing oils in transgenic land plants for human and aquaculture nutrition, Mar. Biotechnol., 2006, vol. 8, pp. 103–109.
Rossi, S., Sabates, A., Latasa, M., and Reyes, E., Lipid biomarkers and trophic linkages between phytoplankton, zooplankton and anchovy (Engraulis encrasicolus) larvae in the NW Mediterranean, J. Plankton Res., 2006, vol. 28, pp. 551–562.
Rubio-Rodriguez, N., Beltran, S., Jaime, I., de Diego, S.M., Sanz, M., and Carballido, J.R., Production of omega-3 polyunsaturated fatty acid concentrates: a review, Innovative Food Sci. Emerging Technol., 2010, vol. 11, pp. 1–12.
Ruffle, B., Burmaster, D.E., Anderson, P.D., and Gordon, H.D., Lognormal distributions for fish consumption by the general U.S. population, Risk Anal., 1994, vol. 14, pp. 395–404.
Ruiz-Lopez, N., Sayanova, O., Napier, J.A., and Haslam, R.P., Metabolic engineering of the omega-3 long chain polyunsaturated fatty acid biosynthetic pathway into transgenic plants, J. Exp. Bot., 2012, vol. 63, pp. 2397–2410.
Rusakova, S.A., Feeding of the vendace from Goreloe and Krasnoe Bol’shoe lakes, Tr. Sev. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 1972, vol. 6, pp. 85–89.
Sanden, M., Stubhaug, I., Berntssen, M.H.G., Lie, O., and Torstensen, B.E., Atlantic salmon (Salmo salar L.) as a net producer of long-chain marine ω-3 fatty acids, J. Agric. Food Chem., 2011, vol. 59, pp. 12697–12706.
SanGiovanni, J.P. and Chew, E.Y., The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina, Prog. Retinal Eye Res., 2005, vol. 24, pp. 87–138.
Sayanova, O.V. and Napier, J.A., Eicosapentaenoic acid: biosynthetic routes and the potential for synthesis in transgenic plants, Phytochemistry, 2004, vol. 65, pp. 147–158.
Stone, D.A.J., Oliveira, A.C.M., Plante, S., Smiley, S., Bechtel, P., and Hardy, R.W., Enhancing highly unsaturated omega-3 fatty acids in phase-fed rainbow trout (Oncorhynchus mykiss) using Alaskan fish oils, Aquacult. Nutr., 2011, vol. 17, pp. E501–E510.
Strandberg, U., Hiltunena, M., Jelkanen, E., Taipale, S.J., Kainz, M.J., Brett, M.T., and Kankaala, P., Selective transfer of polyunsaturated fatty acids from phytoplankton to planktivorous fish in large boreal lakes, Sci. Total Environ., 2015, vol. 536, pp. 858–865.
Sushchik, N.N., Gladyshev, M.I., Kalachova, G.S., Makhutova, O.N., and Ageev, A.V., Comparison of seasonal dynamics of the essential PUFA contents in benthic invertebrates and grayling Thymallus arcticus in the Yenisei River, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2006, vol. 145, pp. 278–287.
Sushchik, N.N., Rudchenko, A.E., and Gladyshev, M.I., Effect of season and trophic level on fatty acid composition and content of four commercial fish species from Krasnoyarsk reservoir (Siberia, Russia), Fish. Res., 2017, vol. 187, pp. 178–187.
Teoh, C.Y. and Ng, W.K., The implications of substituting dietary fish oil with vegetable oils on the growth performance, fillet fatty acid profile and modulation of the fatty acid elongase, desaturase and oxidation activities of red hybrid tilapia, Oreochromis sp., Aquaculture, 2016, vol. 465, pp. 311–322.
Teoh, C.Y., Turchini, G.M., and Ng, W.K., Genetically improved farmed Nile tilapia and red hybrid tilapia showed differences in fatty acid metabolism when fed diets with added fish oil or a vegetable oil blend, Aquaculture, 2011, vol. 312, pp. 126–136.
Thanuthong, T., Francis, D.S., Senadheera, S.D., Jones, P.L., and Turchini, G.M., 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, 2011, vol. 320, pp. 82–90.
Tocher, D.R., Metabolism and functions of lipids and fatty acids in teleost fish, Rev. Fish. Sci., 2003, vol. 11, pp. 107–184.
Tocher, D.R., Omega-3 long-chain polyunsaturated fatty acids and aquaculture in perspective, Aquaculture, 2015, vol. 449, pp. 94–107.
Torstensen, B.E., Froyland, L., Ornsrud, R., and Lie, O., Tailoring of a cardioprotective muscle fatty acid composition of Atlantic salmon (Salmo salar) fed vegetable oils, Food Chem., 2004, vol. 87, 567–580.
Turchini, G.M., Francis, D.S., Keast, R.S.J., and Sinclair, A.J., Transforming salmonid aquaculture from a consumer to a producer of long chain omega-3 fatty acids, Food Chem., 2011, vol. 124, pp. 609–614.
Turner, N., Else, P.L., and Hulbert, A.J., Docosahexaenoic acid (DHA) content of membranes determines molecular activity of the sodium pump: implications for disease states and metabolism, Naturwissenschaften, 2003, vol. 90, pp. 521–523.
Turner, N., Else, P.L., and Hulbert, A.J., An allometric comparison of microsomal membrane lipid composition and sodium pump molecular activity in the brain of mammals and birds, J. Exp. Biol., 2005, vol. 208, pp. 371–381.
Wall, R., Ross, R.P., Fitzgerald, G.F., and Stanton, C., Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids, Nutr. Rev., 2010, vol. 68, pp. 280–289.
Ward, O.P. and Singh, A., Omega-3/6 fatty acids: alternative sources of production, Process Biochem., 2005, vol. 40, pp. 3627–3652.
Weber, J.-M., Metabolic fuels: regulating fluxes to select mix, J. Exp. Biol., 2011, vol. 214, pp. 286–294.
Young, L.R. and Nestle, M., Portion sizes in dietary assessment, Nutr. Rev., 1995, vol. 53, pp. 149–158.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © M.I. Gladyshev, L.A. Glushchenko, O.N. Makhutova, A.E. Rudchenko, S.P. Shulepina, O.P. Dubovskaya, I.V. Zuev, V.I. Kolmakov, N.N. Sushchik, 2018, published in Sibirskii Ekologicheskii Zhurnal, 2018, No. 3, pp. 325–339.
Rights and permissions
About this article
Cite this article
Gladyshev, M.I., Glushchenko, L.A., Makhutova, O.N. et al. Comparative Analysis of Content of Omega-3 Polyunsaturated Fatty Acids in Food and Muscle Tissue of Fish from Aquaculture and Natural Habitats. Contemp. Probl. Ecol. 11, 297–308 (2018). https://doi.org/10.1134/S199542551803006X
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S199542551803006X