The importance of essential fatty acids and their ratios in aquafeeds to enhance salmonid production, welfare, and human health

Abstract

Long chain polyunsaturated fatty acids (LC-PUFA), namely those from omega-3 (n-3) and omega-6 (n-6) families, are paramount for both fish and human nutrition. Some of these biomolecules cannot be synthesized de novo and must be acquired through the diet, being termed dietary essential fatty acids (EFA). Fish requirements for EFA have traditionally been met through the incorporation of fish oil (FO) in the formulation of aquafeeds. However, with limited supply of FO the aquaculture industry is searching for additional sustainable sources of LC-PUFA. This has significantly shifted the type of ingredients used in aquafeed formulation, namely vegetable oils (VO) deficient in long-chain omega-3, often resulting in imbalanced levels and ratios of fatty acid classes. Such imbalances can negatively affect fish performance and welfare, as well as the levels of health promoting omega-3 LC-PUFA present in fish fillets. Given the relevance that salmonid aquaculture plays in global fish production (principally Atlantic salmon, Salmo salar), as well as its growing role as a source of dietary health promoting omega-3 LC-PUFA for humans, the present review summarizes the scientific knowledge available to date on the dietary requirements for LC-PUFA by salmonids and humans. We discuss the implications of using imbalanced aquafeed formulations upon fish performance and welfare, as well as the subsequent consequences for human nutrition, along with current efforts to replace FO by alternative ingredients such as algal oil (AO) that can safeguard high-quality salmonid products for human consumption.

1 Introduction

Aquaculture is among the most promising industries to address human malnutrition and diet-related diseases (Naylor et al., 2021). Seafood is an important source of vital nutrients, such as structural and functional lipids rich in omega-3 (n-3) fatty acids (FA), some of which are vital for human health (Tocher, 2015; Oliver et al., 2020). For all species, some of these FA are termed essential fatty acids (EFA) as they cannot be synthesized de novo and must be acquired through diet (Calder, 2020; Sharma and Mandal, 2020; Troesch et al., 2020). Among EFA, LC-PUFA act as regulators of metabolism and immune function, being key for disease prevention (see reviews by Tocher (2003); Glencross (2009); Oliver et al. (2020)). More specifically, omega-3 LC-PUFA participate in metabolic pathways in the resolving phase of inflammation and return to homeostasis, whereas omega-6 LC-PUFA participate in metabolic pathways associated with the formation of pro-inflammatory molecules (Calder, 2013; Ortega-Gómez et al., 2013; Hundal et al., 2022; Huyben et al., 2023).

Fish are acknowledged as important sources of dietary EFA for humans (Tocher, 2015; Oliver et al., 2020). Oily fish, particularly salmonids, are a versatile and popular seafood and regarded as one of the best sources of omega-3 PUFA for humans (Nichols et al., 2014; FAO, 2020). Salmonids, namely Atlantic salmon Salmo salar, are undeniably one of the pillars of marine fish aquaculture and the most important aquaculture commodity traded in value since 2013 (FAO, 2022). Salmonids have a limited ability to produce omega-3 long chain PUFA (omega-3 LC-PUFA) from their precursor alpha-linolenic acid, ALA; 18:3n-3 (Bell et al., 1997; Tocher et al., 2019). Whilst the levels of these LC-PUFA required to sustain good fish growth are relatively low (Ruyter et al., 1999; Menoyo et al., 2007), the dietary requirements to maintain suitable fish health are somewhat higher (Bou et al., 2017; Lutfi et al., 2022); so too are the levels needed to maintain fish as good sources of LC-PUFA for humans (Nichols et al., 2014; Tocher et al., 2019). Consequently, aquafeeds must incorporate suitable and balanced levels of LC-PUFA to support fish growth and health, as well as requirements for deposition in their muscle for human food requirements (Glencross et al., 2023).

The health benefits of omega-3 LC-PUFA and the need to diversify the source of ingredients displaying high levels of these EFA to be incorporated in aquafeeds is widely accepted (Tocher, 2015). Given the global importance of salmonid aquaculture, this review aims to 1) briefly summarize the scientific knowledge available on salmonid requirements for dietary EFA; 2) document the implications that the use of imbalanced aquafeed formulations can have on human nutrition; and 3) examine the potential alternative EFA sources to FO that can be considered, targeting the production of high-quality salmonid products. An emphasis is given on how optimizing the omega-3 nutritional parameters of aquafeeds can improve fish performance and welfare, while safeguarding those qualities that consumers rely on these seafoods to supply.

2 LC-PUFA importance for fish

2.1 Metabolism and role of LC-PUFA in fish

In general, freshwater fish species can synthesize LC-PUFA from precursors, whilst marine fish have a more limited capacity to do so (Ishikawa et al., 2019; Twining et al., 2021). Salmonids are diadromous and move from freshwater to marine environments or vice versa, being able to convert ALA into omega-3 LC-PUFA, such as eicosapentaenoic acid (EPA; 20:5n-3) and docosahexaenoic acid (DHA; 22:6n-3), as well as linoleic acid (LA, 18:2n-6) into arachidonic acid (ARA; 20:4n-6). Thus, ALA and LA are key precursors of other EFA (Punia et al., 2019). Unlike most marine fish to which EPA, DHA, and ARA are considered essential because their rate of biosynthesis is either non-existent, or low and insufficient to meet physiological demands (Glencross, 2009; Castro et al., 2016), salmonids have a relatively higher ability to produce EPA and DHA from ALA (Bell et al., 1997; Tocher et al., 2019). Despite some de novo synthesis, the levels of omega-3 and omega-6 LC-PUFA resulting from these pathways are not high enough to meet the nutritional requirements of fish when challenged (Agaba et al., 2005; Leaver et al., 2008; Castro et al., 2012; Sprague et al., 2019); and to meet the nutritional needs of human consumers (Sanden et al., 2011; Nichols et al., 2014; Tocher et al., 2019).

In fish, LC-PUFA play key roles in cell membranes and cellular synthesis, ionic regulation and pigmentation (Tocher, 1995; Sargent et al., 2003; Tocher, 2003; Glencross, 2009; Lutfi et al., 2022). They are also required for the proper development and function of the neural system (Innis, 2007; Litz et al., 2017), having an important role in reproduction (Tocher, 2003; Glencross, 2009) and the protective intestinal barrier function (Huyben et al., 2020; Løvmo et al., 2021). LC-PUFA also control metabolic functions (e.g., being chemical messengers or effectors of secondary messengers), endocrine pathways (e.g., acting as hormone precursors), and are key for immune functions (Glencross, 2009; Huyben et al., 2023).

2.2 Dietary requirements of LC-PUFA for salmonids

Farmed fish must be provided suitable levels of dietary LC-PUFA to meet their physiological demands, welfare, and produce high-quality fillets rich in omega-3 LC-PUFA. The dietary requirements of LC-PUFA for salmonids are summarized in Supplementary Table 1. These requirements vary among species, environmental conditions, stressors, and age, and are also influenced by the absolute and relative values of these fatty acids in the total dietary lipid. For instance, omega-3 LC-PUFA requirements range from 10 to 25 g/kg of aquafeed depending on species, fish age and farming conditions (Tocher et al., 2000; Glencross, 2009; Glencross et al., 2014; Bou et al., 2017; Huyben et al., 2021; Lutfi et al., 2022).

Requirements for LC-PUFA are typically higher during the early life stages to sustain the high level of demands required during early development of the neural and visual system in the fish (Tocher, 2010). Notably, EPA and DHA are especially important for the growth and development of fry, parr, and smolt, with DHA playing a pivotal role in neural growth and development (Innis, 2007; Litz et al., 2017). When salmonids undergo smoltification and transition from life in freshwater to seawater, their FA profile changes as a pre-adaptive response to this new environment. More specifically, there is a peak in omega-3 LC-PUFA biosynthesis, with FA profiles displaying higher levels of LC-PUFA, namely EPA and DHA (Tocher et al., 2000; Bendiksen et al., 2003). These shifts affect cellular processes involved in adaptation to seawater, such as ionic regulation and synthesis of prostaglandins (Spector and Yorek, 1985; Mustafa and Srivastava, 1989).

Dietary requirements for omega-3 LC-PUFA also change with farming conditions and the health status of fish. Compared to controlled laboratory systems, fish held in cage farming environments experience seasonal shifts in salinity, temperature, and incidence of pathogens. As an example, while n-3 LC-PUFA requirements for post-smolt Atlantic salmon (~185-550 g) range between 5-8% of the total pool of FA in the laboratory (Glencross et al., 2014; Bou et al., 2017; Huyben et al., 2021), under cage farming conditions these needs may exceed 10% (Lutfi et al., 2022). Indeed, lipid metabolism and the composition of cellular membranes are modified to endure changes in seawater temperature, with lower temperatures promoting higher levels of EPA and DHA (Norambuena et al., 2016; Rosenlund et al., 2016).

2.3 Implications of LC-PUFA deficiencies and imbalanced ratios in fish

Inadequate levels of LC-PUFA in the diet of salmonids can affect fish performance, particularly feed conversion, negatively impacting growth and survival (Ruyter, 2000; Berge et al., 2009; Glencross et al., 2015; Selvam et al., 2021). Some studies also report an increased sensitivity to stressful conditions (Bell et al., 1991; Thompson et al., 1996; Huyben et al., 2023) and a decreased resistance to pathogens (Martinez-Rubio et al., 2012). Stress and pathogens are common under fish-farming conditions, being responsible for mass mortalities that cause major economic losses. Therefore, it is desirable to preventively enhance fish resistance to these challenging conditions. For instance, by adjusting LC-PUFA levels in aquafeeds it is possible to reduce the impacts of heart and skeletal muscle inflammation associated with Atlantic salmon reovirus infection, one of the most prevalent inflammatory diseases in salmon farms (Martinez-Rubio et al., 2012). More recently, high levels of LC-PUFA have also been linked with higher resistance to chronic stress (Huyben et al., 2023).

Meeting an optimal ratio between LC-PUFA omega-6 and omega-3 FA is paramount, as it modulates metabolic and immune functions (Patterson et al., 2012; Huyben et al., 2020). In Atlantic salmon, this ratio is substantially affected when provided only with the short-chain PUFA (Sprague et al., 2019). Notably, when fed a diet devoid of any LC-PUFA but including a 3:1 ratio of ALA : LA, the salmon parr endogenously synthesize their own omega-3 LC-PUFA at a ratio of 27:1 against omega-6 LC-PUFA. Even with a 1:3 ratio of ALA : LA the fish synthesize omega-3 LC-PUFA at a ratio of about 3:1. Hundal et al. (2021) suggested that increasing the dietary n-6/n-3 FA ratio in salmon feeds can affect the way they respond to stressors in an aquaculture setting, possibly affecting the fish robustness. Other studies have suggested that EPA levels ideally should be higher than those of ARA and DHA, due to its role in the anti-inflammatory response and as an antagonizing agent of ARA-derived pro-inflammatory mediators (Martinez-Rubio et al., 2012). Consequently, the EPA : DHA ratio should also be considered and ideally maintained at 1.5:1, as insufficient EPA levels negatively affects the anti-inflammatory response (Martinez-Rubio et al., 2012). However, maintaining this optimal ratio in commercial farms is a challenge, as the abundance of EPA in LC-PUFA sources is limited, and therefore few LC-PUFA sources have such an ideal ratio of EPA : DHA. Furthermore, research on the effect of an imbalanced omega-3:omega-6 ratio on Atlantic salmon health and performance are somewhat contradictory; whilst some studies show no effects, or even negative results, others report no adverse impact of higher dietary levels of omega-6 LC-PUFA on fish growth and survival (Grisdale-Helland et al., 2002; Menoyo et al., 2007; Sissener et al., 2016). These discrepancies, however, might arise from differences in the trial design or nutritional history of the animals (e.g. lipid reserves), among other study parameters.

The FA composition of fish lipids is predominantly influenced by diet (Sargent et al., 1999; Glencross et al., 2014; Xu et al., 2020; Glencross et al., 2023). Changes in the final product are well known to impact its nutritional quality for consumers; it has also been observed to result in suboptimal pigmentation (Lutfi et al., 2022) and poorer processing (smoking) qualities, features that lead to processor and retailer rejection (Johansen and Jobling, 1998; Tocher et al., 2003).

3 LC-PUFA importance for humans

3.1 Dietary requirements for LC-PUFA by humans

Based on scientific evidence available, multiple organizations (e.g., the World Health Organization, the European Food Safety Authority, or the American Heart Association) promote the regular intake of omega-3 LC-PUFA, with recommended doses of up to 250 – 500 mg/day (EFSA Panel on Dietetic Products Nutrition, 2010). Oily fishes, such as salmon, are considered one of the best dietary sources of EPA and DHA (Henriques et al., 2014; Nichols et al., 2014). However, the FA profile of salmon is modulated by the aquafeeds provided during grow-out. Due to changes in aquafeed formulations, the content of EPA and DHA present in salmon fillets halved between 2004 and 2015 (Sprague et al., 2016). This shift has resulted in the need to increase the number of salmon servings to meet human dietary requirements. More specifically, international guidelines recommend consumers to now eat at least 2 servings per week of these oily fishes to meet requirements for omega-3 LC-PUFA (EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2014; Norwegian Scientific Committee for Food and Environment (VKM), 2022).

3.2 Benefits of adequate LC-PUFA intake in humans

There is growing scientific evidence highlighting the importance of LC-PUFA for humans (see reviews by Saini and Keum (2018) and Oliver et al. (2020)). The effects of LC-PUFA on human health and nutrition have been recognized since the 1970s, with the first studies evidencing the benefits of omega-3 LC-PUFA in mortality associated with cardiovascular disease (CVD) (Jump et al., 2012; Endo and Arita, 2016). Since then, the effectiveness of omega-3 LC-PUFA against CVD has further been confirmed (Bucher et al., 2002; Delgado-Lista et al., 2012). Omega-3 LC-PUFA also seem to play a role against age-related cognitive impairments, such as dementia or Alzheimer’s disease (Gogus and Smith, 2010; Dangour et al., 2012). Other conditions that may be regulated by LC-PUFA include eczema, diabetes, allergy, asthma, thrombosis, macular degeneration, and some types of cancer (Gogus and Smith, 2010; Oliver et al., 2020). Benefits have also been reported when fighting inflammatory diseases, such as rheumatoid arthritis, Crohn’s disease, and ulcerative colitis (Cabré et al., 2012; Miles and Calder, 2012). These health promoting features are attributed to the mechanism of action of these fatty acids on inflammatory pathways and their regulatory role in the immune system. More specifically, eicosanoids derived from ARA (e.g., prostaglandins and leukotrienes) drive inflammatory responses, whereas eicosanoids derived from EPA produce an anti-inflammatory response that antagonizes ARA-derived eicosanoids (Calder, 2007; Calder et al., 2009).

The optimal omega-6:omega-3 ratio for humans is yet to be fully understood, but it is suggested to range between 2.5-5:1 (Gogus and Smith, 2010). Current average diet of Western populations displays a much higher ratio, ranging approximately 10-25:1 (Molendi-Coste et al., 2011; Tocher et al., 2019). This ratio is distant from that of ancestral populations, which ranged at 1-4:1 (Tocher et al., 2019; Oliver et al., 2020).

Reducing the dietary intake of omega-6 PUFA may be difficult to achieve in some regions. For example, these are key nutrients in Mediterranean diets rich in olive oil, which is also rich in omega-9 but relatively poor in omega-3 (Calder et al., 2009). Consequently, increasing the intake of omega-3 LC-PUFA appears as a more feasible approach to attain a more balanced proportion between these two FA families (Tocher, 2015). This can be achieved by increasing the intake of EPA and DHA through an enhanced consumption of fish and other seafood with high levels of these fatty acids.

4 Aquafeeds as sources of LC-PUFA for aquaculture products

4.1 Traditional sources of LC-PUFA for aquafeeds

Traditionally, LC-PUFA requirements in farmed fish have been met using FO, as it features a relatively high content of omega-3 LC-PUFA and a balanced FA profile to support fish performance, welfare, and secure a high-quality final product for human consumption. However, the use of FO in aquafeeds is constrained because supply cannot keep up with demand (Delgado-Lista et al., 2012; Tocher, 2015).

Supply limitations of LC-PUFA in aquaculture were first addressed by using different VO. Whilst these oils can support fish growth, they display high levels of omega-6 PUFA and are devoid of omega-3 LC-PUFA (Tocher, 2003; Glencross, 2009). The dietary replacement of FO by VO also dilutes omega-3 content and modifies the FA profile and lipid content of fish (Bell et al., 1997; Bou et al., 2017; Hundal et al., 2022; Glencross et al., 2023). Often advocated as more sustainable ingredients for aquafeeds than FO, the production of VO also creates environmental impacts due to intensive agricultural practices impacting land use, freshwater use and biodiversity for example, which cannot be overlooked (Shepherd and Little, 2014).

4.2 Alternative sources of LC-PUFA for aquafeeds

To fill the gap between demand and supply of omega-3 LC-PUFA, the aquaculture industry has focused on the potential use of unexploited fisheries, such as krill, calanoid copepods, and mesopelagic fish (Tocher, 2015; Tocher et al., 2019). Whilst these are potentially good omega-3 sources, the harvesting of these organisms comes with technological challenges, high costs, and environmental concerns (Herbert-Read et al., 2022). Another alternative could be through the valorization of by-products resulting from fish processing industries. Indeed, by-product resources already comprise close to 50% of all fish oil produced in 2020 and 30% of all fishmeal (Glencross and Bachis, 2021).

The production of genetically modified (GM) oilseed products has also been advocated as a solution for supplying omega-3 LC-PUFA. It can be easily scalable by using the infrastructures already available to produce VO and its use in salmon diets does not negatively affect fish growth or health (Tocher et al., 2019; Napier and Betancor, 2022; Ruyter et al., 2022; Davis and Devine, 2023). GM yeast strains have also been developed for the same purpose, but these are still unlikely to produce sufficient volumes at affordable prices to meet current demands (Hatlen et al., 2012; Tocher et al., 2019),. Moreover, given the overall negative perception that GM products still have in some countries, the use of aquafeeds formulated using GM oilseed products remains less likely to be accepted by some consumers (Desaint and Varbanova, 2013; Lucht, 2015).

Of all alternatives currently being evaluated, algal oil (AO) derived from heterotrophic organisms - classified as such due the very close molecular phylogenetic relationship to microalgae and absence of a clear definition- appears to hold the greatest potential to fill the gap between demand and supply for affordable omega-3 LC-PUFA (Tocher et al., 2019; Santigosa et al., 2020; Tibbets et al., 2020; Santigosa et al., 2021). Lipid levels vary among algal species and growth conditions, but marine microalgae generally present higher concentrations of LC-PUFA, particularly EPA and DHA (Li-Beisson et al., 2019). While the development of efficient and cost-effective large-scale microalgal photoautotrophic cultivation systems is yet to be achieved (Oliver et al., 2020), heterotrophic production by fermentation under controlled conditions is already well established and can attain higher production yields (Vigani et al., 2015; Lowrey et al., 2016). Moreover, heterotrophic production delivers a higher level of lipid (Ríos et al., 2018) at lower production costs (Muller-Feuga, 2013).

Overall, it is expected that novel sources of omega-3 LC-PUFA will become available in greater volume and at a cost that enables their greater use in aquafeed to restore EPA and DHA levels and to safeguard the performance, health and welfare of farmed fish as well as delivering high quality seafood products for human consumption (Turchini et al., 2022).

5 Guidelines for future research

Current commercial aquafeed formulations for salmonids are generally designed to meet the minimum requirements of EPA and DHA (Lutfi et al., 2022). However, although these low levels can support fish growth, there have been numerous incidences where levels this low have negatively impacted fish health and welfare, robustness, and nutritional value of the final product. It is therefore critical to re-evaluate the benefits of increasing EPA and DHA levels in salmonid diets, restoring nutritional qualities back to those levels seen before FO became a limiting ingredient. Additionally, requirements for LC-PUFA need to be further considered under non-ideal farming conditions, such as higher thermal regimes, hypoxia and/or infections (Huyben et al., 2021; Huyben et al., 2023).

References

• 1

  AgabaM. K.TocherD. R.ZhengX.DicksonC. A.DickJ. R.TealeA. J. (2005). Cloning and functional characterisation of polyunsaturated fatty acid elongases of marine and freshwater teleost fish. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol.142 (3), 342–352. doi: 10.1016/j.cbpb.2005.08.005

  • CrossRef
  • Google Scholar
  • View reference in article

• 2

  BellJ. G.McVicarA. H.ParkM. T.SargentJ. R. (1991). High dietary linoleic acid affects the fatty acid compositions of individual phospholipids from tissues of atlantic salmon (Salmo salar): association with stress susceptibility and cardiac lesion. J. Nutr.121 (8), 1163–1172. doi: 10.1093/jn/121.8.1163

  • CrossRef
  • Google Scholar
  • View reference in article

• 3

  BellJ. G.TocherD. R.FarndaleB. M.CoxD. I.McKinneyR. W.SargentJ. R. (1997). The effect of dietary lipid on polyunsaturated fatty acid metabolism in atlantic salmon (Salmo salar) undergoing parr-smolt transformation. Lipids. Springer32 (5), 515–525. doi: 10.1007/s11745-997-0066-4

  • CrossRef
  • Google Scholar
  • View reference in article

• 4

  BendiksenE. Å.ArnesenA. M.JoblingM. (2003). Effects of dietary fatty acid profile and fat content on smolting and seawater performance in atlantic salmon (Salmo salar l.). Aquaculture225 (1), 149–163. doi: 10.1016/S0044-8486(03)00286-2

  • CrossRef
  • Google Scholar
  • View reference in article

• 5

  BergeG. M.WittenE.BaeverfjordG.VegusdalA.WadsworthS.RuyterB. (2009). Diets with different n – 6/n – 3 fatty acid ratio in diets for juvenile atlantic salmon, effects on growth, body composition, bone development and eicosanoid production. Aquaculture296, 299–308. doi: 10.1016/j.aquaculture.2009.08.029

  • CrossRef
  • Google Scholar
  • View reference in article

• 6

  BouM.BergeG. M.BaeverfjordG.SigholtT.ØstbyeT. K.RuyterB. (2017). Low levels of very-long-chainn-3 PUFA in atlantic salmon (Salmo salar) diet reduce fish robustness under challenging conditions in sea cages. J. Nutr. Sci.6, e32. doi: 10.1017/jns.2017.28

  • CrossRef
  • Google Scholar
  • View reference in article

• 7

  BucherH. C.HengstlerP.SchindlerC.MeierG. (2002). N-3 polyunsaturated fatty acids in coronary heart disease: a meta-analysis of randomized controlled trials. Am. J. Med.112 (4), 298–304. doi: 10.1016/S0002-9343(01)01114-7

  • CrossRef
  • Google Scholar
  • View reference in article

• 8

  CabréE.MañosaM.GassullM. A. (2012). Omega-3 fatty acids and inflammatory bowel diseases - a systematic review. Br. J. Nutr.107 Suppl 2 (S2), S240–S252. doi: 10.1017/S0007114512001626

  • CrossRef
  • Google Scholar
  • View reference in article

• 9

  CalderP. C. (2007). Immunomodulation by omega-3 fatty acids. Prostaglandins leukotrienes essential Fatty Acids77 (5–6), 327–335. doi: 10.1016/j.plefa.2007.10.015

  • CrossRef
  • Google Scholar
  • View reference in article

• 10

  CalderC. (2013). Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology? Br. J. Clin. Pharmacol.75 (3), 645–662. doi: 10.1111/j.1365-2125.2012.04374.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 11

  CalderC. (2020). Eicosapentaenoic and docosahexaenoic acid derived specialised pro-resolving mediators: concentrations in humans and the effects of age, sex, disease and increased omega-3 fatty acid intake. Biochimie178, 105–123. doi: 10.1016/j.biochi.2020.08.015

  • CrossRef
  • Google Scholar
  • View reference in article

• 12

  CalderP. C.AlbersR.AntoineJ. M.BlumS.Bourdet-SicardR.FernsG. A.et al. (2009). Inflammatory disease processes and interactions with nutrition. Br. J. Nutr.101 Suppl 1, S1–45. doi: 10.1017/S0007114509377867

  • CrossRef
  • Google Scholar
  • View reference in article

• 13

  CastroL. F. C.MonroigO.LeaverM. J.WilsonJ.CunhaI.Tocher.D. R. (2012). Functional desaturase Fads1 (Δ5) and Fads2 (Δ6) orthologues evolved before the origin of jawed vertebrates. PloS One7 (2), e31950. doi: 10.1371/journal.pone.0031950

  • CrossRef
  • Google Scholar
  • View reference in article

• 14

  CastroL. F. C.TocherD. R.MonroigO. (2016). Long-chain polyunsaturated fatty acid biosynthesis in chordates: Insights into the evolution of fads and elovl gene repertoire. Prog. Lipid Res.62, 25–40. doi: 10.1016/j.plipres.2016.01.001

  • CrossRef
  • Google Scholar
  • View reference in article

• 15

  DangourA. D.AndreevaV. A.SydenhamE.UauyR. (2012). Omega 3 fatty acids and cognitive health in older people. Br. J. Nutr.107 Suppl 2, S152–S158. doi: 10.1017/S0007114512001547

  • CrossRef
  • Google Scholar
  • View reference in article

• 16

  DavisB.DevineM. D. (2023). Evaluation of long-chain omega-3 canola oil on atlantic salmon growth, performance, and essential fatty acid tissue accretion across the life cycle: a review. Aquaculture Int. 107 (Suppl 2), S152–S158. doi: 10.1007/s10499-023-01099-3

  • CrossRef
  • Google Scholar
  • View reference in article

• 17

  Delgado-ListaJ.Perez-MartinezP.Lopez-MirandaJ.Perez-JimenezF. (2012). Long chain omega-3 fatty acids and cardiovascular disease: a systematic review. Br. J. Nutr.107 Suppl 2, S201–S213. doi: 10.1017/S0007114512001596

  • CrossRef
  • Google Scholar
  • View reference in article

• 18

  DesaintN.VarbanovaM. (2013). The use and value of polling to determine public opinion on GMOs in europe: limitations and ways forward. GM Crops Food.4 (3), 183–194. doi: 10.4161/gmcr.26776

  • CrossRef
  • Google Scholar
  • View reference in article

• 19

  EFSA Panel on Dietetic Products Nutrition (2010). Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J.8 (3), 1461. doi: 10.2903/j.efsa.2010.1461

  • CrossRef
  • Google Scholar
  • View reference in article

• 20

  EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA) (2014). Scientific opinion on health benefits of seafood (fish and shellfish) consumption in relation to health risks associated with exposure to methylmercury. EFSA J.12 (7), 3761.

  • Google Scholar
  • View reference in article

• 21

  EndoJ.AritaM. (2016). Cardioprotective mechanism of omega-3 polyunsaturated fatty acids. J. Cardiol.67 (1), 22–27. doi: 10.1016/j.jjcc.2015.08.002

  • CrossRef
  • Google Scholar
  • View reference in article

• 22

  FAO (2020). The state of world fisheries and aquaculture 2020: Sustainability in action (Rome, Italy: Food and Agriculture Organization of the United Nations). doi: 10.4060/ca9229en

  • CrossRef
  • Google Scholar
  • View reference in article

• 23

  FAO (2022). “The state of world fisheries and aquaculture 2022,” in Towards blue transformation. (Rome, Italy). doi: 10.4060/cc0461en

  • CrossRef
  • Google Scholar
  • View reference in article

• 24

  GlencrossB. D. (2009). Exploring the nutritional demand for essential fatty acids by aquaculture species. Rev. aquaculture.1 (2), 71–124. doi: 10.1111/j.1753-5131.2009.01006.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 25

  GlencrossB. D.BachisE. (2021). Byproduct-based fishmeals: Adding to the future of fishmeal production. Aquafeed13 (4), 21–24.

  • Google Scholar
  • View reference in article

• 26

  GlencrossB. D.CarrI.SantigosaE. (2023). Distribution, deposition, and modelling of lipid and long-chain polyunsaturated fatty acids in atlantic salmon fillets. Rev. Fisheries Sci. Aquaculture31 (1), 119–140. doi: 10.1080/23308249.2022.2090831

  • CrossRef
  • Google Scholar
  • View reference in article

• 27

  GlencrossB. D.De SantisC.BicskeiB.TaggartJ. B.BronJ. E.BetancorM. B.et al (2015). And tocher, dA comparative analysis of the response of the hepatic transcriptome to dietary docosahexaenoic acid in atlantic salmon (Salmo salar) post-smolts. BMC Genomics16 (1), 684. doi: 10.1186/s12864-015-1810-z

  • CrossRef
  • Google Scholar
  • View reference in article

• 28

  GlencrossB. D.TocherD. R.MatthewC.Gordon BellJ. (2014). Interactions between dietary docosahexaenoic acid and other long-chain polyunsaturated fatty acids on performance and fatty acid retention in post-smolt atlantic salmon (Salmo salar). Fish Physiol. Biochem.40 (4), 1213–1227. doi: 10.1007/s10695-014-9917-8

  • CrossRef
  • Google Scholar
  • View reference in article

• 29

  GogusU.SmithC. (2010). N-3 omega fatty acids: a review of current knowledge. Int. J. Food Sci. technology.45 (3), 417–436. doi: 10.1111/j.1365-2621.2009.02151.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 30

  Grisdale-HellandB.RuyterB.RosenlundG.ObachA.HellandS. J.SandbergM.et al. (2002). Influence of high contents of dietary soybean oil on growth, feed utilization, tissue fatty acid composition, heart histology and standard oxygen consumption of atlantic salmon (Salmo salar) raised at two temperatures. Aquaculture207 (3–4), 311–329. doi: 10.1016/S0044-8486(01)00743-8

  • CrossRef
  • Google Scholar
  • View reference in article

• 31

  HatlenB.BergeG. M.OdomJ. M.MundheimH.RuyterB. (2012). Growth performance, feed utilisation and fatty acid deposition in atlantic salmon, salmo salar l., fed graded levels of high-lipid/high-EPA yarrowia lipolytica biomass. Aquaculture364, 39–47. doi: 10.1016/j.aquaculture.2012.07.005

  • CrossRef
  • Google Scholar
  • View reference in article

• 32

  HenriquesJ.DickJ. R.TocherD. R.BellJ. G. (2014). Nutritional quality of salmon products available from major retailers in the UK: content and composition of n-3 long-chain PUFA. Br. J. Nutr.112 (6), 964–975. doi: 10.1017/S0007114514001603

  • CrossRef
  • Google Scholar
  • View reference in article

• 33

  Herbert-ReadJ. E.ThorntonA.AmonD. J.BirchenoughS. N.CôtéI. M.DiasM.et al. (2022). A global horizon scan of issues impacting marine and coastal biodiversity conservation. Nat. Ecol. Evolution.6 (9), 1262–1270. doi: 10.1038/s41559-022-01812-0

  • CrossRef
  • Google Scholar
  • View reference in article

• 34

  HundalB. K.LilandN. S.RosenlundG.HöglundE.AraujoP.StubhaugI.et al. (2021). Increasing the dietary n-6/n-3 ratio alters the hepatic eicosanoid production after acute stress in atlantic salmon (Salmo salar). Aquaculture534, 736272. doi: 10.1016/j.aquaculture.2020.736272

  • CrossRef
  • Google Scholar
  • View reference in article

• 35

  HundalB. K.LutfiE.SigholtT.RosenlundG.LilandN. S.GlencrossB.et al. (2022). A piece of the puzzle-possible mechanisms for why low dietary EPA and DHA cause hepatic lipid accumulation in atlantic salmon (Salmo salar). Metabolites12 (2), 159. doi: 10.3390/metabo12020159

  • CrossRef
  • Google Scholar
  • View reference in article

• 36

  HuybenD.CroninT.BartieK. L.MatthewC.SissenerN. H.HundalB. K.et al. (2023). Steroidogenic and innate immune responses in atlantic salmon are influenced by dietary total lipid, long chain polyunsaturated fatty acids and dissolved oxygen. Aquaculture564, 739028. doi: 10.1016/j.aquaculture.2022.739028

  • CrossRef
  • Google Scholar
  • View reference in article

• 37

  HuybenD.GroblerT.MatthewC.BouM.RuyterB.GlencrossB. (2021). Requirement for omega-3 long-chain polyunsaturated fatty acids by atlantic salmon is relative to the dietary lipid level. Aquaculture531, 735805. doi: 10.1016/j.aquaculture.2020.735805

  • CrossRef
  • Google Scholar
  • View reference in article

• 38

  HuybenD.RoeheB. K.BekaertM.RuyterB.GlencrossB. (2020). Dietary Lipid:Protein ratio and n-3 long-chain polyunsaturated fatty acids alters the gut microbiome of atlantic salmon under hypoxic and normoxic conditions. Front. Microbiol.11, 589898. doi: 10.3389/fmicb.2020.589898

  • CrossRef
  • Google Scholar
  • View reference in article

• 39

  IFFO (2022) The role of marine ingredients, IFFO - the marine ingredients organisation. Available at: https://www.iffo.com/role-marine-ingredients (Accessed December 9, 2022).

  • Google Scholar
  • View reference in article

• 40

  InnisS. M. (2007). Dietary (n-3) fatty acids and brain development. J. Nutr.137 (4), 855–859. doi: 10.1093/jn/137.4.855

  • CrossRef
  • Google Scholar
  • View reference in article

• 41

  IshikawaA.IshikawaA.KabeyaN.IkeyaK.KakiokaR.CechJ. N.et al. (2019). A key metabolic gene for recurrent freshwater colonization and radiation in fishes. Science364 (6443), 886–889. doi: 10.1126/science.aau5656

  • CrossRef
  • Google Scholar
  • View reference in article

• 42

  JohansenS. J. S.JoblingM. (1998). The influence of feeding regime on growth and slaughter traits of cage-reared atlantic salmon. Aquaculture Int.6, 1–17. doi: 10.1126/science.aau5656

  • CrossRef
  • Google Scholar
  • View reference in article

• 43

  JumpD. B.DepnerC. M.TripathyS. (2012). Omega-3 fatty acid supplementation and cardiovascular disease: Thematic review series: New lipid and lipoprotein targets for the treatment of cardiometabolic diseases. J. Lipid Res.53 (12), 2525–2545. doi: 10.1194/jlr.R027904

  • CrossRef
  • Google Scholar
  • View reference in article

• 44

  LeaverM. J.BautistaJ. M.BjörnssonB. T.JönssonE.KreyG.TocherD. R.et al. (2008). Towards fish lipid nutrigenomics: Current state and prospects for fin-fish aquaculture. Rev. Fisheries Science.16 (sup1), 73–94. doi: 10.1080/10641260802325278

  • CrossRef
  • Google Scholar
  • View reference in article

• 45

  Li-BeissonY.ThelenJ. J.FedosejevsE.HarwoodJ. L. (2019). The lipid biochemistry of eukaryotic algae. Prog. Lipid Res.74, 31–68. doi: 10.1016/j.plipres.2019.01.003

  • CrossRef
  • Google Scholar
  • View reference in article

• 46

  LitzM. N.MillerJ. A.CopemanL. A.HurstT. P. (2017). Effects of dietary fatty acids on juvenile salmon growth, biochemistry, and aerobic performance: A laboratory rearing experiment. J. Exp. Mar. Biol. Ecol.494, 20–31. doi: 10.1016/j.jembe.2017.04.007

  • CrossRef
  • Google Scholar
  • View reference in article

• 47

  LøvmoS. D.WhatmoreP.SundhH.SigholtT.MadaroA.BardalT.et al. (2021). Effects of atlantic salmon (Salmo salar) fed low- and high HUFA diets on growth and midgut intestinal health. Aquaculture539, 736653. doi: 10.1016/j.aquaculture.2021.736653

  • CrossRef
  • Google Scholar
  • View reference in article

• 48

  LowreyJ.ArmentaR. E.BrooksM. S. (2016). Nutrient and media recycling in heterotrophic microalgae cultures. Appl. Microbiol. Biotechnol.100 (3), 1061–1075. doi: 10.1007/s00253-015-7138-4

  • CrossRef
  • Google Scholar
  • View reference in article

• 49

  LuchtJ. M. (2015). Public acceptance of plant biotechnology and GM crops. Viruses7 (8), 4254–4281. doi: 10.3390/v7082819

  • CrossRef
  • Google Scholar
  • View reference in article

• 50

  LutfiE.BergeG.BæverfjordG.SigholtT.BouM.LarssonT.et al. (2022). Increasing dietary levels of the omega-3 long-chain polyunsaturated fatty acids, EPA and DHA, improves the growth, welfare, robustness, and fillet quality of atlantic salmon in sea cages. Br. J. Nutr.129 (1), 1–48. doi: 10.1017/S0007114522000642

  • CrossRef
  • Google Scholar
  • View reference in article

• 51

  Martinez-RubioL.MoraisS.EvensenØ.WadsworthS.RuohonenK.VecinoJ. L.et al. (2012). Functional feeds reduce heart inflammation and pathology in atlantic salmon (Salmo salar l.) following experimental challenge with atlantic salmon reovirus (ASRV). PloS One7 (11), e40266. doi: 10.1371/journal.pone.0040266

  • CrossRef
  • Google Scholar
  • View reference in article

• 52

  MenoyoD.Lopez-BoteC. J.DiezA.ObachA.BautistaJ. M. (2007). Impact of n- 3 fatty acid chain length and n- 3/n- 6 ratio in atlantic salmon (Salmo salar) diets. Aquaculture267 (1–4), 248–259. doi: 10.1016/j.aquaculture.2007.02.031

  • CrossRef
  • Google Scholar
  • View reference in article

• 53

  MilesE. A.CalderC. (2012). Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. Br. J. Nutr.107 Suppl 2, S171–S184. doi: 10.1017/S0007114512001560

  • CrossRef
  • Google Scholar
  • View reference in article

• 54

  Molendi-CosteO.LegryV.LeclercqI. A. (2011). Why and how meet n-3 PUFA dietary recommendations? Gastroenterol. Res. practice.2011, 364040. doi: 10.1155/2011/364040

  • CrossRef
  • Google Scholar
  • View reference in article

• 55

  Muller-FeugaA. (2013). “Microalgae for aquaculture: The current global situation and future trends,” in Handbook of microalgal culture (Oxford, UK: John Wiley & Sons, Ltd), 613–627.

  • Google Scholar
  • View reference in article

• 56

  MustafaT.SrivastavaK. C. (1989). “Prostaglandins (Eicosanoids) and their role in ectothermic organisms,” in Advances in comparative and environmental physiology. Ed. BrouwerM.et al (Berlin, Heidelberg: Springer Berlin Heidelberg), 157–207.

  • Google Scholar
  • View reference in article

• 57

  NapierJ. A.BetancorM. B. (2022). Engineering plant-based feedstocks for sustainable aquaculture. Curr. Opin. Plant Biol.71. doi: 10.1016/j.pbi.2022.102323

  • CrossRef
  • Google Scholar
  • View reference in article

• 58

  NaylorR. L.KishoreA.SumailaU. R.IssifuI.HunterB. P.BeltonB. (2021). Blue food demand across geographic and temporal scales. Nat. Commun.12 (1), 5413. doi: 10.1038/s41467-021-25516-4

  • CrossRef
  • Google Scholar
  • View reference in article

• 59

  NicholsD.GlencrossB.PetrieJ. R.SinghS. P. (2014). Readily available sources of long-chain omega-3 oils: is farmed australian seafood a better source of the good oil than wild-caught seafood? Nutrients6 (3), 1063–1079. doi: 10.3390/nu6031063

  • CrossRef
  • Google Scholar
  • View reference in article

• 60

  NorambuenaF.RombensoA.TurchiniG. M. (2016). Towards the optimization of performance of atlantic salmon reared at different water temperatures via the manipulation of dietary ARA/EPA ratio. Aquaculture450, 48–57. doi: 10.1016/j.aquaculture.2015.06.044

  • CrossRef
  • Google Scholar
  • View reference in article

• 61

  Norwegian Scientific Committee for Food and Environment (VKM) (2022). Benefit and risk assessment of fish in the norwegian diet Vol. 2022. VKM Report (Oslo, Norway), 17.

  • Google Scholar
  • View reference in article

• 62

  OliverL.DietrichT.MarañónI.VillaránM. C.BarrioR. J. (2020). Producing omega-3 polyunsaturated fatty acids: A review of sustainable sources and future trends for the EPA and DHA market. Resources9 (12), 148. doi: 10.3390/resources9120148

  • CrossRef
  • Google Scholar
  • View reference in article

• 63

  Ortega-GómezA.PerrettiM.SoehnleinO. (2013). Resolution of inflammation: an integrated view. EMBO Mol. Med.5 (5), 661–674. doi: 10.1002/emmm.201202382

  • CrossRef
  • Google Scholar
  • View reference in article

• 64

  PattersonE.WallR.FitzgeraldG. F.RossR. P.StantonC. (2012). Health implications of high dietary omega-6 polyunsaturated fatty acids. J. Nutr. Metab.2012, 539426. doi: 10.1155/2012/539426

  • CrossRef
  • Google Scholar
  • View reference in article

• 65

  PuniaS.SandhuK. S.SirohaA. K.DhullS. B. (2019). Omega 3-metabolism, absorption, bioavailability and health benefits–a review. PharmaNutrition10, 100162. doi: 10.1016/j.phanu.2019.100162

  • CrossRef
  • Google Scholar
  • View reference in article

• 66

  RíosL. F.MartinezA.KleinB. C.MacielM. W.FilhoR. M. (2018). Comparison of growth and lipid accumulation at three different growth regimes with desmodesmus sp. Waste Biomass valorization.9 (3), 421–427. doi: 10.1007/s12649-016-9811-y

  • CrossRef
  • Google Scholar
  • View reference in article

• 67

  RosenlundG.TorstensenB. E.StubhaugI.UsmanN.SissenerN. H. (2016). Atlantic salmon require long-chain n-3 fatty acids for optimal growth throughout the seawater period. J. Nutr. Sci.5, e19. doi: 10.1017/jns.2016.10

  • CrossRef
  • Google Scholar
  • View reference in article

• 68

  RuyterB. (2000). Essential fatty acids in atlantic salmon: effects of increasing dietary doses of n-6 and n-3 fatty acids on growth, survival and fatty acid composition of liver, blood and carcass. Aquaculture Nutr.6 (2), 119–127. doi: 10.1046/j.1365-2095.2000.00137.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 69

  RuyterB.ThomassenM. S. (1999). Metabolism of n–3 and n–6 fatty acids in atlantic salmon liver: stimulation by essential fatty acid deficiency. Lipids34 (11), pp. 1137–1176.

  • Google Scholar
  • View reference in article

• 70

  RuyterB.BouM.BergeG. M.MørkøreT.SissenerN. H.SandenM.et al. (2022). A dose-response study with omega-3 rich canola oil as a novel source of docosahexaenoic acid (DHA) in feed for atlantic salmon (Salmo salar) in seawater; effects on performance, tissue fatty acid composition, and fillet quality. Aquaculture561, 738733. doi: 10.1016/j.aquaculture.2022.738733

  • CrossRef
  • Google Scholar
  • View reference in article

• 71

  SainiR. K.KeumY.-S. (2018). Omega-3 and omega-6 polyunsaturated fatty acids: Dietary sources, metabolism, and significance–a review. Life Sci.203, 255–267. doi: 10.1016/j.lfs.2018.04.049

  • CrossRef
  • Google Scholar
  • View reference in article

• 72

  SandenM.StubhaugI.BerntssenM. H.LieØ.TorstensenB. E. (2011). Atlantic salmon (Salmo salar l.) as a net producer of long-chain marine ω-3 fatty acids. J. Agric. Food Chem.59 (23), 12697–12706. doi: 10.1021/jf203289s

  • CrossRef
  • Google Scholar
  • View reference in article

• 73

  SantigosaE.BrambillaF.MilaneseL. (2021). Microalgae oil as an effective alternative source of EPA and DHA for gilthead seabream (Sparus aurata) aquaculture. Animals: an Open Access J. MDPI11 (4), 971. doi: 10.3390/ani11040971

  • CrossRef
  • Google Scholar
  • View reference in article

• 74

  SantigosaE.ConstantD.PrudenceD.WahliT.Verlhac-TrichetV. (2020). A novel marine algal oil containing both EPA and DHA is an effective source of omega-3 fatty acids for rainbow trout (Oncorhynchus mykiss). J. World Aquaculture Society.51 (3), 649–665. doi: 10.1111/jwas.12699

  • CrossRef
  • Google Scholar
  • View reference in article

• 75

  SargentJ.BellG.McEvoyL.TocherD.EstevezA. (1999). Recent developments in the essential fatty acid nutrition of fish. Aquaculture177 (1), 191–199. doi: 10.1016/S0044-8486(99)00083-6

  • CrossRef
  • Google Scholar
  • View reference in article

• 76

  SargentJ. R.TocherD. R.BellJ. G. (2003). “4 - the lipids,” in Fish nutrition (Third edition). Eds. HalverJ. E.HardyR. W. (San Diego: Academic Press), 181–257.

  • Google Scholar
  • View reference in article

• 77

  SelvamC.PowellM. D.LilandN. S.RosenlundG.SissenerN. H. (2021). Impact of dietary level and ratio of n-6 and n-3 fatty acids on disease progression and mRNA expression of immune and inflammatory markers in atlantic salmon (Salmo salar) challenged with paramoeba perurans. Peer J. publising. doi: 10.7717/peerj.12028

  • CrossRef
  • Google Scholar
  • View reference in article

• 78

  SharmaT.MandalC. C. (2020). Omega-3 fatty acids in pathological calcification and bone health. J. Food Biochem.44 (8), e13333. doi: 10.1111/jfbc.13333

  • CrossRef
  • Google Scholar
  • View reference in article

• 79

  ShepherdC. J.LittleD. C. (2014). Aquaculture: Are the criticisms justified? II–aquaculture’s environmental impact and use of resources, with special reference to farming atlantic salmon. World Agric.4, 37–52.

  • Google Scholar
  • View reference in article

• 80

  SissenerN. H.WaagbøR.RosenlundG.TvenningL.SusortS.LeaT. B.et al. (2016). Reduced n-3 long chain fatty acid levels in feed for atlantic salmon (Salmo salar l.) do not reduce growth, robustness or product quality through an entire full scale commercial production cycle in seawater. Aquaculture464, 236–245. doi: 10.1016/j.aquaculture.2016.06.034

  • CrossRef
  • Google Scholar
  • View reference in article

• 81

  SpectorA. A.YorekM. A. (1985). Membrane lipid composition and cellular function. J. Lipid Res.26 (9), 1015–1035. doi: 10.1016/S0022-2275(20)34276-0

  • CrossRef
  • Google Scholar
  • View reference in article

• 82

  SpragueM.DickJ. R.TocherD. R. (2016). Impact of sustainable feeds on omega-3 long-chain fatty acid levels in farmed atlantic salmo–2015. Sci. Rep.6 (1), 1–9.

  • Google Scholar
  • View reference in article

• 83

  SpragueM.XuG.BetancorM. B.OlsenR. E.TorrissenO.GlencrossB. D.et al. (2019). Endogenous production of n-3 long-chain PUFA from first feeding and the influence of dietary linoleic acid and the α-linolenic:linoleic ratio in atlantic salmon (Salmo salar). Br. J. Nutr.122 (10), 1091–1102. doi: 10.1017/S0007114519001946

  • CrossRef
  • Google Scholar
  • View reference in article

• 84

  ThompsonK. D.TatnerM. F.HendersonR. J. (1996). Effects of dietary (n-3) and (n-6) polyunsaturated fatty acid ratio on the immune response of atlantic salmon, salmo salar l. Aquaculture Nutr.2 (1), 21–31. doi: 10.1111/j.1365-2095.1996.tb00004.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 85

  TibbettsS. M.ScaifeM. A.ArmentaR. E. (2020). Apparent digestibility of proximate nutrients, energy and fatty acids in nutritionally-balanced diets with partial or complete replacement of dietary fish oil with microbial oil from a novel schizochytrium sp. (T18) by juvenile atlantic salmon (Salmo salar l.). Aquaculture520, 735003. doi: 10.1016/j.aquaculture.2020.735003

  • CrossRef
  • Google Scholar
  • View reference in article

• 86

  TocherD. R. (1995). “Chapter 6 glycerophospholipid metabolism,” in Biochemistry and molecular biology of fishes. Eds. HochachkaW.MommsenT. P. (Elsevier), 119–157.

  • Google Scholar
  • View reference in article

• 87

  TocherD. R. (2003). Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fisheries Science.11 (2), 107–184. doi: 10.1080/713610925

  • CrossRef
  • Google Scholar
  • View reference in article

• 88

  TocherD. R. (2010). Fatty acid requirements in ontogeny of marine and freshwater fish. Aquaculture Res.41 (5), 717–732. doi: 10.1111/j.1365-2109.2008.02150.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 89

  TocherD. R. (2015). Omega-3 long-chain polyunsaturated fatty acids and aquaculture in perspective. Aquaculture449, 94–107. doi: 10.1016/j.aquaculture.2015.01.010

  • CrossRef
  • Google Scholar
  • View reference in article

• 90

  TocherD. R.BellJ. G.DickJ. R.HendersonR. J.McGheeF.MichellD.et al. (2000). Polyunsaturated fatty acid metabolism in atlantic salmon (Salmo salar) undergoing parr-smolt transformation and the effects of dietary linseed and rapeseed oils. Fish Physiol. Biochem.23 (1), 59–73. doi: 10.1023/A:1007807201093

  • CrossRef
  • Google Scholar
  • View reference in article

• 91

  TocherD. R.BetancorM. B.SpragueM.OlsenR. E.NapierJ. A. (2019). Omega-3 long-chain polyunsaturated fatty acids, EPA and DHA: Bridging the gap between supply and demand. Nutrients11 (1), 89. doi: 10.3390/nu11010089

  • CrossRef
  • Google Scholar
  • View reference in article

• 92

  TocherD. R.BellJ. G.DickJ. R.CramptonV. O. (2003). Effects of dietary vegetable oil on atlantic salmon hepatocyte fatty acid desaturation and liver fatty acid compositions. Lipids38 (7), 723–732. doi: 10.1007/s11745-003-1120-y

  • CrossRef
  • Google Scholar
  • View reference in article

• 93

  TroeschB.EggersdorferM.LavianoA.RollandY.SmithA. D.WarnkeI.et al. (2020). Expert opinion on benefits of long-chain omega-3 fatty acids (DHA and EPA) in aging and clinical nutrition. Nutrients12 (9), 2555. doi: 10.3390/nu12092555

  • CrossRef
  • Google Scholar
  • View reference in article

• 94

  TurchiniG. M.FrancisD. S.DuZ.OlsenR. E.RingøE.TocherD. R.et al. (2022 2022). “The lipids,” in Fish nutrition (Fourth edition). Eds. HardyR. W.KaushikS. J. (Academic Press), 303–467.

  • Google Scholar
  • View reference in article

• 95

  TwiningC. W.BernhardtJ. R.DerryA. M.HudsonC. M.IshikawaA.KabeyaN.et al. (2021). The evolutionary ecology of fatty-acid variation: Implications for consumer adaptation and diversification. Ecol. letters.24 (8), 1709–1731. doi: 10.1111/ele.13771

  • CrossRef
  • Google Scholar
  • View reference in article

• 96

  ViganiM.ParisiC.Rodríguez-CerezoE.BarbosaM. J.SijtsmaL.PloegM.et al. (2015). Food and feed products from micro-algae: Market opportunities and challenges for the EU. Trends Food Sci. Technology.42 (1), 81–92. doi: 10.1016/j.tifs.2014.12.004

  • CrossRef
  • Google Scholar
  • View reference in article

• 97

  XuH.TurchiniG. M.FrancisD. S.LiangM.MockT. S.RombensoA.et al. (2020). Are fish what they eat? a fatty acid’s perspective. Prog. Lipid Res.80, 101064. doi: 10.1016/j.plipres.2020.101064

  • CrossRef
  • Google Scholar
  • View reference in article