Abstract
In several Russian northern lakes and rivers, Arctic cisco Coregonus autumnalis, least cisco C. sardinella, peled C. peled, tugun C. tugun, broad whitefish C. nasus, whitefish C. lavaretus and vendace C. albula were sampled in periods of officially permitted commercial fishery. Special attention was paid to contents (mg g−1 of wet weight) of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) in muscle tissues (filets), which are essential for human nutrition. The highest values of EPA + DHA content in semi-anadromous fish and freshwater fish were recorded for C. autumnalis from the Yenisei River, 17.60 mg g−1 wet weight, and for C. lavaretus from the Sobachye Lake, 16.61 mg g−1 wet weight, respectively. Intra-genus variations of EPA + DHA contents of Coregonus species were from 1.87 to 17.60 mg g−1 wet weight. Since the congeneric species were genetically close to each other, the variations in EPA and DHA contents were thought to be caused primarily by ecological factors: migrational capability, type of feeding and trophic status of aquatic ecosystems. In general, the majority of studied species appeared to be of a high nutritive value for humans, although unfavorable environmental conditions could considerably diminish this value.
Similar content being viewed by others
Abbreviations
- BFA:
-
Branched fatty acid(s)
- CCA:
-
Canonical correspondence analysis
- DHA:
-
Docosahexaenoic acid (22:6n-3)
- EPA:
-
Eicosapentaenoic acid (20:5n-3)
- FA:
-
Fatty acid(s)
- FAME:
-
Fatty acid methyl ester(s)
- GC–MS:
-
Gas chromatography–mass spectrometry
- PL:
-
Phospholipids
- PUFA:
-
Polyunsaturated fatty acid(s)
- TAG:
-
Triacylglycerol(s)
References
Hibbeln JR, Nieminen LRG, Blasbalg TL, Riggs JA, Lands WEM (2006) Healthy intakes of n-3 and n-6 fatty acids: estimations considering worldwide diversity. Am J Clin Nutr 83:1483S–1493S
McNamara RK, Carlson SE (2006) Role of omega-3 fatty acids in brain development and function: potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids 75:329–349
Adkins Y, Kelley DS (2010) Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. J Nutr Biochem 21:781–792
De Caterina R (2011) n–3 Fatty acids in cardiovascular disease. N Engl J Med 364:2439–2450
Harris WS, Mozaffarian D, Lefevre M, Toner CD, Colombo J, Cunnane SC, Holden JM, Klurfeld DM, Morris MC, Whelan J (2009) Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids. J Nutr 139:804S–819S
Kris-Etherton PM, Grieger JA, Etherton TD (2009) Dietary reference intakes for DHA and EPA. Prostaglandins Leukot Essent Fatty Acids 81:99–104
Casula M, Soranna D, Catapano AL, Corrao G (2013) Long-term effect of high dose omega-3 fatty acid supplementation for secondary prevention of cardiovascular outcomes: a meta-analysis of randomized, double blind, placebo controlled trials. Atheroscler Suppl 14:243–251
Nagasaka R, Gagnon C, Swist E, Rondeau I, Massarelli I, Cheung W, Ratnayake WMN (2014) EPA and DHA status of South Asian and White Canadians living in the National Capital Region of Canada. Lipids 49:1057–1069
Robert SS (2006) Production of eicosapentaenoic and docosahexaenoic acid-containing oils in transgenic land plants for human and aquaculture nutrition. Mar Biotechnol 8:103–109
Gladyshev MI, Sushchik NN, Makhutova ON (2013) Production of EPA and DHA in aquatic ecosystems and their transfer to the land. Prostaglandins Other Lipid Mediat 107:117–126
Gladyshev MI, Makhutova ON, Gubanenko GA, Rechkina EA, Kalachova GS, Sushchik NN (2015) 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 117:17–1421
Tacon AGJ, Metian M (2013) Fish matters: importance of aquatic foods in human nutrition and global food supply. Rev Fish Sci 21:22–38
Kwetegyeka J, Mpango G, Grahl-Nielsen O (2008) Variation in fatty acid composition in muscle and heart tissues among species and populations of tropical fish in lakes Victoria and Kyoga. Lipids 43:1017–1029
Vasconi M, Caprino F, Bellagamba F, Busetto ML, Bernardi C, Puzzi C, Moretti VM (2015) Fatty acid composition of freshwater wild fish in subalpine lakes: a comparative study. Lipids 50:283–302
Chuang L-T, Bulbul U, Wen P-C, Glew RH, Ayaz FA (2012) Fatty acid composition of 12 fish species from the Black Sea. J Food Sci 77:C512–C518
Makhutova ON, Sushchik NN, Gladyshev MI, Ageev AV, Pryanichnikova EG, Kalachova GS (2011) Is the fatty acid composition of freshwater zoobenthic invertebrates controlled by phylogenetic or trophic factors? Lipids 46:709–721
Lau DCP, Vrede T, Pickova J, Goedkoop W (2012) Fatty acid composition of consumers in boreal lakes—variation across species, space and time. Freshw Biol 57:24–38
Litzow MA, Bailey KM, Prahl FG, Heintz R (2006) Climate regime shifts and reorganization of fish communities: the essential fatty acid limitation hypothesis. Mar Ecol Prog Ser 315:1–11
Sushchik NN, Gladyshev MI, Kalachova GS (2007) Seasonal dynamics of fatty acid content of a common food fish from the Yenisei River, Siberian grayling, Thymallus arcticus. Food Chem 104:1353–1358
Garg ML, Wood LG, Singh H, Moughan PJ (2006) Means of delivering recommended levels of long chain n-3 polyunsaturated fatty acids in human diets. J Food Sci 71:R66–R71
Rubio-Rodriguez N, Beltran S, Jaime I, de Diego SM, Sanz M, Carballido JR (2010) Production of omega-3 polyunsaturated fatty acid concentrates: a review. Innov Food Sci Emerg Technol 11:1–12
Taipale SJ, Vuorioc K, Strandberg U, Kahilainen KK, Jarvinen M, Hiltunen M, Peltomaa E, Kankaala P (2016) Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption. Environ Int 96:156–166
Ahlgren G, Vrede T, Goedkoop W (2009) Fatty acid ratios in freshwater fish, zooplankton and zoobenthos—are their specific optima? In: Arts MT, Kainz M, Brett MT (eds) Lipids in aquatic ecosystems. Springer, New York
Gladyshev MI, Lepskaya EV, Sushchik NN, Makhutova ON, Kalachova GS, Malyshevskaya KK, Markevich GN (2012) Comparison of polyunsaturated fatty acids content in filets of anadromous and landlocked sockeye salmon Oncorhynchus nerka. J Food Sci 77:C1306–C1310
Hixson SM, Sharma B, Kainz MJ, Wacker A, Arts MT (2015) Production, distribution, and abundance of long-chain omega-3 polyunsaturated fatty acids: a fundamental dichotomy between freshwater and terrestrial ecosystems. Environ Rev 23:414–424
Gladyshev MI, Sushchik NN, Gubanenko GA, Demirchieva SM, Kalachova GS (2007) Effect of boiling and frying on the content of essential polyunsaturated fatty acids in muscle tissue of four fish species. Food Chem 101:1694–1700
Gladyshev MI, Artamonova VS, Makhrov AA, Sushchik NN, Kalachova GS, Dgebuadze YY (2017) Triploidy does not decrease contents of eicosapentaenoic and docosahexaenoic acids in filets of pink salmon Oncorhynchus gorbuscha. Food Chem 216:66–69
Huynh MD, Kitts DD (2009) Evaluating nutritional quality of pacific fish species from fatty acid signatures. Food Chem 114:912–918
Popova ON, Haritonov AY, Sushchik NN, Makhutova ON, Kalachova GS, Kolmakova AA, Gladyshev MI (2017) Export of aquatic productivity, including highly unsaturated fatty acids, to terrestrial ecosystems via Odonata. Sci Total Environ 581–582:40–48
Gladyshev MI, Gribovskaya IV, Adamovich VV (1993) Disappearance of phenol in water samples taken from the Yenisei River and the Krasnoyarsk reservoir. Water Res 27:1063–1070. doi:10.1016/0043-1354(93)90071-O
Gladyshev MI, Kolmakova OV, Tolomeev AP, Anishchenko OV, Makhutova ON, Kolmakova AA, Kravchuk ES, Glushchenko LA, Kolmakov VI, Sushchik NN (2015) Differences in organic matter and bacterioplankton between sections of the largest Arctic river: mosaic or continuum? Limnol Oceanogr 60:1314–1331
Pichugin MY (2009) 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 49:236–248
Leonov AV, Filatov NN, Zdorovennov RE, Zdorovennova GE (2006) 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 33:543–567
Ivanov VV, Brizgalo VA (2007) Hydrology and hydrochemistry of watershed. In: Filatov N, Terzhevik A (eds) The White Sea and its watershed under influences of climate and anthropogenic impacts. Karelian Research Center of the RAS, Petrozavodsk (in Russian)
Gritsevskaya GL, Kyabeleva GK, Nikolayeva LA, Semenov VN (1972) Hydrology and hydrochemistry of Solovetsky lakes. Proc SevNIORH 6:5–44 (in Russian)
Savina EA (1991) Evaluation of degree of water pollution of surface waterbodies of the Solovetsky archipelago. In: Boyarsky PV (ed) Unknown Solovkee. Russian Scientific Research Institute of Cultural and Natural Heritage, Moscow (in Russian)
Domanitsky AP, Dubrovina RG, Isaeva AI (1971) Rivers and lakes of Soviet Union. Gidrometeoizdat, Leningrad (in Russian)
Timakova TM (2010) General description of the lake. In: Filatov NN (ed) Lake Onega. Atlas. Karelian Research Centre of the RAS, Petrozavodsk (in Russian)
Glushchenko LA (2016) Hydrobiological study of Lake Sobachye. Annals of nature recorded by Federal Institution “Nature Reserves of Taimyr”, issue 3. Norilsk (in Russian)
Vyshegorodcev AA (2000) Fishes of the Yenisei. Nauka, Novosibirsk (in Russian)
Berger VY (1995) Biological resources and problems of their rational exploitation. In: Scarlato OA (ed) White Sea Part II. Zoological Institute of the RAS, St.-Petersburg (in Russian)
Reshetnikov YS, Lukin AA (2008) Coregonids. In: Kukharev VI, Lukin AA (eds) Bioresources of Lake Onego. Karelian Research Centre of the RAS, Petrozavodsk (in Russian)
Sterligova OP, Ilmast NV, Savosin DS (2016) Cyclostomata and fish of freshwater of Karelia. Karelian Scientific Center of RAS, Petrozavodsk (in Russian)
Rusakova SA (1972) Feeding of vendace of the Goreloye Lake and the Bolshoie Krasnoie Lake. Proc SevNIORH 6:85–89 (in Russian)
Borovikova EA, YaI Alekseeva, Schreider MJ, Artamonova VS, Makhrov AA (2013) Morphology and genetics of the ciscoes (Actinopterygii: Salmoniformes: Salmonidae: Coregoninae: Coregonus) from the Solovetsky Archipelago (White Sea) as a key to determination of the taxonomic position of ciscoes in Northeastern Europe. Acta Ichthyol Piscat 43:183–194
Gladyshev MI, Sushchik NN, Gubanenko GA, Makhutova ON, Kalachova GS, Rechkina EA, Malyshevskaya KK (2014) Effect of the way of cooking on contents of essential polyunsaturated fatty acids in filets of zander. Czech J Food Sci 32:226–231
Legendre P, Legendre L (1998) Numerical ecology. Elsevier Science, Amsterdam
Wagner T, Jones ML, Ebener MP, Arts MT, Brenden TO, Honeyfield DC, Wright GM, Faisal M (2010) Spatial and temporal dynamics of lake whitefish (Coregonus clupeaformis) health indicators: linking individual-based indicators to a management-relevant endpoint. J Great Lakes Res 36:121–134
Cladis DP, Kleiner AC, Freiser HH, Santerre CR (2014) Fatty acid profiles of commercially available finfish fillets in the United States. Lipids 49:1005–1101
Neff MR, Bhavsar SP, Braekevelt E, Arts MT (2014) Effects of different cooking methods on fatty acid profiles in four freshwater fishes from the Laurentian Great Lakes region. Food Chem 164:544–550
Guler GO, Aktumsek A, Cakmak YS, Zengin G, Citil OB (2011) 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 76:C594–C597
Philibert A, Vanier C, Abdelouahab N, Chan HM, Mergler D (2006) Fish intake and serum fatty acid profiles from freshwater fish. Am J Clin Nutr 84:1299–1307
Arts MT, Kohler CC (2009) Health and condition in fish: the influence of lipids on membrane competency and immune response? In: Arts MT, Kainz M, Brett MT (eds) Lipids in aquatic ecosystems. Springer, New York
Arts MT, Palmer ME, Skiftesvik AB, Jokinen IE, Browman HI (2012) UVB radiation variably affects n-3 fatty acids but elevated temperature reduces n-3 fatty acids in juvenile Atlantic salmon (Salmo salar). Lipids 47:1181–1192
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 68:280–289
Pethybridge HR, Parrish CC, Morrongiello J, Young JW, Farley JH, Gunasekera RM, Nichols PD (2015) Spatial patterns and temperature predictions of tuna fatty acids: tracing essential nutrients and changes in primary producers. PLoS One 10(7):e0131598
Gokce MA, Tasbozan O, Celik M, Tabakoglu SS (2004) Seasonal variations in proximate and fatty acid compositions of female common sole (Solea solea). Food Chem 88:419–423
Laurel BJ, Copeman LA, Parrish CC (2012) Role of temperature on lipid/fatty acid composition in Pacific cod (Gadus macrocephalus) eggs and unfed larvae. Mar Biol 159:2025–2034
Murzina SA, Nefedova ZA, Falk-Petersen S, Ripatti PO, Ruokolainen TR, Pekkoeva SN, Nemova NN (2013) Lipid status of the two high latitude fish species, Leptoclinus maculatus and Lumpenus fabricii. Int J Mol Sci 14:7048–7060
Wijekoon MPA, Parrish CC, Mansour A (2014) Effect of dietary substitution of fish oil with flaxseed or sunflower oil on muscle fatty acid composition in juvenile steelhead trout (Oncorhynchus mykiss) reared at varying temperatures. Aquaculture 433:74–81
Gribble MO, Karimi R, Feingold BJ, Nyland JF, O’Hara TM, Gladyshev MI, Chen CY (2016) Mercury, selenium and fish oils in marine food webs and implications for human health. J Mar Biol Assoc UK 96:43–59
Stillwell W, Wassall SR (2003) Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids 126:1–27
Dymond MK (2015) Mammalian phospholipid homeostasis: homeoviscous adaptation deconstructed by lipidomic data driven modelling. Chem Phys Lipids 191:136–146
Dymond MK (2016) Mammalian phospholipid homeostasis: evidence that membrane curvature elastic stress drives homeoviscous adaptation in vivo. J R Soc Interface 13:20160228
Ahlgren G, Sonesten L, Boberg M, Gustafsson I-B (1996) Fatty acid content of some freshwater fish in lakes of different trophic levels—a bottom-up effect? Ecol Freshw Fish 5:15–27
Graeve M, Albers C, Kattner G (2005) Assimilation and biosynthesis of lipids in Arctic Calanus species based on feeding experiments with a 13C labelled diatom. J Exp Mar Biol Ecol 317:109–125
Kattner G, Hagen W (2009) Lipids in marine copepods: latitudinal characteristics and perspectives to global warming. In: Arts MT, Kainz M, Brett MT (eds) Lipids in aquatic ecosystems. Springer, New York
Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306
Ozawa A, Satake M, Fujita T (1993) Comparison of muscle lipid composition between marine and landlocked forms of sockeye salmon (Oncorhynchus nerka). Comp Biochem Physiol B 106:513–516
Makhutova ON, Protasov AA, Gladyshev MI, Sylaieva AA, Sushchik NN, Morozovskaya IA, Kalachova GS (2013) Feeding spectra of bivalve mollusks Unio and Dreissena from Kanevskoe Reservoir, Ukraine: are they food competitors or not? Zool Stud 52:56
Rollin X, Peng J, Pham D, Ackman RG, Yvan Larondelle (2003) The effects of dietary lipid and strain difference on polyunsaturated fatty acid composition and conversion in anadromous and landlocked salmon (Salmo salar L.) parr. Comp Biochem Physiol B 134:349–366
Betancor MB, Olsen RE, Solstorm D, Skulstad OF, Tocher DR (2016) Assessment of a land-locked Atlantic salmon (Salmo salar L.) population as a potential genetic resource with a focus on long-chain polyunsaturated fatty acid biosynthesis. Biochim Biophys Acta 1861:227–238
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
Stone DAJ, Oliveira ACM, Plante S, Smiley S, Bechtel P, Hardy RW (2011) Enhancing highly unsaturated omega-3 fatty acids in phase-fed rainbow trout (Oncorhynchus mykiss) using Alaskan fish oils. Aquacult Nutr 17:E501–E510
Sushchik NN, Rudchenko AE, Gladyshev MI (2017) Effect of season and trophic level on fatty acid composition and content of four commercial fish species from Krasnoyarsk Reservoir (Siberia, Russia). Fish Res 187:178–187
Mairesse G, Thomas M, Gardeur J-N, Brun-Bellut J (2006) Effects of geographic source, rearing system, and season on the nutritional quality of wild and farmed Perca fluviatilis. Lipids 41:221–229
Benedito-Palos L, Calduch-Giner JA, Ballester-Lozano GF, Perez-Sanchez J (2013) 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 109:1175–1187
Suomela J-P, Lundén S, Kaimainen M, Mattila S, Kallio H, Airaksinen S (2016) Effects of origin and season on the lipids and sensory quality of European whitefish (Coregonus lavaretus). Food Chem 197:1031–1037
Acknowledgements
The work was supported by Grant of Russian Science Foundation No. 16-14-10001. We are grateful to Ya. I. Alekseeva, V. S. Artamonova, I. L. Schurov, V. A. Shirokov for their kind help in sample collecting.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors have no conflicts of interest.
About this article
Cite this article
Gladyshev, M.I., Sushchik, N.N., Makhutova, O.N. et al. Fatty Acid Composition and Contents of Seven Commercial Fish Species of Genus Coregonus from Russian Subarctic Water Bodies. Lipids 52, 1033–1044 (2017). https://doi.org/10.1007/s11745-017-4304-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11745-017-4304-8