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Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA, Scotland, UK and * EWOS Innovation, N-4335, Dirdal, Norway
1To whom correspondence should be addressed. E-mail: email gjb1{at}stir.ac.uk.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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70 and 75%, respectively, of the values in fish fed 100% FO. When vegetable oil was included at 100% of total dietary lipid, the concentrations of 20:5(n-3) and 22:6(n-3) were significantly reduced to 30 and 36%, respectively, of the values in fish fed FO. Transfer of fish previously fed 100% vegetable oil to a 100% FO diet for 20 wk restored the concentrations of 20:5(n-3) and 22:6(n-3) to 80% of the value in fish fed 100% FO for 70 wk, although the values were still significantly lower. However, in fish previously fed either 100% LO or RO, concentrations of 18:2(n-6) remained 50% higher than in fish fed 100% FO. This study suggests that RO and LO can be used successfully to culture salmon through the seawater phase of their growth cycle; this will result in reductions in flesh 20:5(n-3) and 22:6(n-3) concentrations that can be partially restored by feeding a diet containing only marine FO for a period before harvest.
KEY WORDS: • Atlantic salmon • linseed oil • rapeseed oil • polyunsaturated fatty acids • fish oil
Almost 30 y ago, it was discovered that native Inuits were apparently protected from cardiovascular disease by their high fish intake (1,2). The importance of the (n-3) highly unsaturated fatty acids (HUFA)1 in human nutrition has led to considerable research effort in the intervening years. Subsequently, the efficacy of (n-3) HUFA in the prevention or attenuation of many of the inflammatory conditions that are prevalent in the developed world, including rheumatoid arthritis, atopic illness, inflammatory bowel disease and various neurological conditions, has been established (3,4).
Fish, and particularly those with oily flesh, such as herring, mackerel and salmon, represent a rich, and almost unique source of the (n-3) HUFA, especially eicosapentaenoic acid [20:5(n-3), EPA] and docosahexaenoic acid [22:6(n-3), DHA]. Demand for fish products is increasing, yet the traditional capture fisheries are in decline worldwide (5) such that the potential shortfall in fish products must be met by aquaculture production (6). Aquaculture production currently uses >60% of global fish oil production and by 2010 >85% will be consumed in aquaculture feeds (7). Future expansion of aquaculture, and in particular salmon production, can continue only if suitable and sustainable alternatives to fish oil (FO) are developed and introduced.
In Atlantic salmon feeds, dietary lipids are a major source of energy (8) and also must provide essential PUFA, including 18:3(n-3) and 18:2(n-6), and especially EPA and DHA, to allow normal growth and development of cells and tissues (9,10). Measurement of ß-oxidation capacity in salmonid fish suggests that saturated and monounsaturated fatty acids (MUFA), especially 16:0, 16:1, 18:1(n-9) and 22:1(n-11), as well as 18:2(n-6), are the preferred substrates for energy production (11,12). A number of vegetable oils are rich in 16:0, 18:1(n-9) and 18:2(n-6), and in some cases 18:3(n-3) also, whereas, by comparison, Northern hemisphere fish oils are rich in the long-chain monoenes, 20:1(n-9) and 22:1(n-11). In terms of providing the essential fatty acids (EFA) required for normal growth and development, several studies have shown that salmon can be raised successfully when they consume diets that contain high levels of vegetable oils for periods up to 30 wk (13–15). In addition, the ability to convert 18:3(n-3) and 18:2(n-6) provided by the diet to their longer-chain HUFA products, including 20:5(n-3), 22:6(n-3) and 20:4(n-6), has been established (14–17). However, recent evidence in rainbow trout suggests that the capacity for endogenous production of HUFA may not fulfill requirements such that, for optimal growth and well being of the fish, some dietary 20:5(n-3) and 22:6(n-3) will be required (18). There is also evidence that the capacity to synthesize essential HUFA may decline with age in fish, as it does in humans (18,19).
Atlantic salmon produced using diets containing only marine fish oils are of high nutritional quality; they are rich in (n-3) HUFA and have a high (n-3)/(n-6) PUFA ratio of 4:1 (20–22). Potential changes in product quality resulting from vegetable oil inclusion in salmon feeds should be minimized if the health benefits of salmon in the human diet are to be maintained. To achieve these goals, any oil replacing fish oil should provide sufficient energy in the form of MUFA, and other easily catabolized fatty acids, to maintain high growth, while maximizing endogenous conversion of 18:3(n-3) to 20:5(n-3) and 22:6(n-3). Rapeseed oil (RO) is a potential candidate for FO substitution because it has moderate levels of 18:2(n-6) and 18:3(n-3), and is rich in 18:1(n-9). In addition, the ratio of 18:3(n-3)/18:2(n-6) in rapeseed oil of 1:2 is regarded as beneficial to human health and should not be detrimental for fish health, provided EPA and DHA are also present from dietary fishmeal (23). Linseed oil is also a potential candidate for FO replacement because it is rich in 
-linolenic acid [18:3(n-3)], is the substrate for synthesis of (n-3) HUFA and also contains significant levels of 18:2(n-6) such that it has an 18:3(n-3)/18:2(n-6) ratio of 3–4:1. -Linolenic acid also possesses anti-inflammatory properties due to inhibition of arachidonic acid synthesis from 18:2(n-6) at the 
6-desaturase step and by inhibition of cyclooxygenase (24,25).
In the present study, Atlantic salmon postsmolts were stocked into 12 seawater pens and fed one of nine experimental diets, containing blends of LO, RO and FO, or a control diet containing only FO, which was fed in triplicate. The fish were sampled after 50 wk and the fish previously fed the 100% FO, 100% LO and 100% RO diets were fed for a further 20 wk a diet containing only FO to follow the dilution of fatty acids from the vegetable oils.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Atlantic salmon postsmolts (n = 7200) of initial weight 120 ± 10 g (individual weights of 100 fish/pen) were distributed into 12 cages (5 x 5 m; 600 fish per cage) in Loch Duich, Lochalsh, Scotland, in February 1999. The temperature over the experimental period (February 1999–July 2000) ranged from 5.5 to 19.6°C with a mean temperature of 10.8 ± 3.4°C. The fish were allowed to acclimate for 2 wk before each pen was randomly assigned one of 10 diets including a control diet with FO alone, which was fed to three pens, and nine experimental diets containing blends of FO, LO and RO. In the period up to 32 wk, feed was distributed manually, whereas in the period from 32 to 50 wk, the fish were switched to automatic feeders controlled by AKVAsmart pellet counters (AKVAsmart ASA, Bryne, Norway.). Problems with the automatic feeders meant that 5 pens also received some feed manually. The 10 practical-type extruded diets were formulated (Ewos Technology Centre, Livingston, Scotland) into 3- and 6-mm pellets, to provide 47.0% crude protein, 24.1% crude lipid and 7.6% moisture and 41.8% protein, 30.5% crude lipid and 6.8% moisture, respectively (Table 1). The added oil comprised 100% FO, 100% LO, 100% RO, FO/RO (2:1 and 1:2 w/w), FO/LO (2:1 and 1:2 w/w), RO/LO (2:1 and 1:2 w/w) and FO/RO/LO (1:1:1 w/w/w) forming a triangular experimental design. The graded substitution of the three dietary oils was reflected in the fatty acid compositions of the 10 diets (Table 2). Thus, when RO was added, there were increased concentrations of 18:1(n-9) and 18:2(n-6) and, to a lesser degree, of 18:3(n-3). Similarly, increasing inclusion of LO increased concentrations of 18:3(n-3) and 18:2(n-6), with the precise amount of the latter depending on whether LO was replacing FO or RO. In all cases in which FO was replaced by a vegetable oil, there was a graded reduction in 20:5(n-3) and 22:6(n-3), as well as 16:0, 20:1(n-9), 22:1 and 20:4(n-6). After sampling at 50 wk, the remaining fish in pens fed the 100% FO, RO and LO diets were redistributed into three pens, with each pen containing 100 fish from each treatment. The fish were marked by fin clipping to identify their previous dietary history. All three pens were fed a diet containing 100% FO, in a 9-mm pellet, for a further 20 wk. The composition of this diet was essentially similar to the 6-mm 100% FO diet. The experimental diets differed only in their oil composition and were formulated to satisfy the nutritional requirements of salmonid fish, including (n-3) EFA, which are provided both by the inclusion of dietary fishmeal and by 18:3(n-3) present in LO and RO (26). The experiment was conducted in accordance with the British Home Office guidelines regarding research on experimental animals.
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After 50 wk, 18 fish were selected at random from each cage. Fish were killed by a blow to the head and a sample of muscle, representative of the edible portion, was obtained by cutting a steak between the leading and trailing edges of the dorsal fin. The samples from each cage were pooled, by weight, in threepools of six fish each; that is, pool A comprised the six smallest fish, pool B, the next six largest fish and pool C, the largest six fish sampled. The pooled steaks were frozen and stored at -25°C until processed. The six steaks were then skinned, deboned and the muscle homogenized in a food processor, after removal of the dorsal fat body. The homogenate was immediately frozen and samples were stored at -40°C before analysis. After the 20-wk washout period, 15 fish per treatment (5 per pen) were sampled as described above except that each sample was an individual fish. Each steak was processed and the homogenate stored as described above.
Lipid extraction and fatty acid analysis.
Total lipid was extracted from 2 g of homogenized muscle by homogenizing in 20 volumes of chloroform/methanol (2:1, v/v) in an Ultra-Turrax tissue disrupter (Fisher Scientific, Loughborough, UK). Total lipid was prepared according to the method of Folch et al. (27) and nonlipid impurities removed by washing with 8.8 g/L KCl. The weight of lipid was determined gravimetrically after evaporation of solvent and overnight desiccation in vacuo. FAME were prepared by acid-catalyzed transesterification of total lipid according to the method of Christie (28). Extraction and purification of FAME were performed as described by Ghioni et al. (29). FAME were separated and quantified by GLC (Carlo Erba Vega 8160, Milan, Italy) using a 30 m x 0.32 mm i.d. capillary column (CP Wax 52CB, Chrompak, London, UK). Hydrogen was used as carrier gas and temperature programming was from 50 to 150°C at 40°C/min and then to 230°C at 2.0°C/min. Individual methyl esters were identified by comparison with known standards and by reference to published data (30). Data were collected and processed using the Chromcard for Windows (version 1.19) computer package (Thermoquest Italia S.p.A., Milan, Italy).
Statistical analysis.
Significance of difference (P < 0.05) between dietary treatments was determined by one-way ANOVA. Differences between means were determined by Tukey’s test. Data identified as nonhomogeneous, using Bartlett’s test, were subjected to log or arcsin transformation before applying the ANOVA. ANOVA and regression analysis was performed using a GraphPad Prism (version 3.0) statistical package (GraphPad Software, San Diego, CA).
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The fatty acid compositions of muscle total lipid reflected the variation in dietary lipid (Table 4). Plots of fatty acid concentration (g/100 g) in flesh lipid (Table 4) against fatty acid concentration (g/100 g) in dietary lipid (Table 2) resulted in straight lines; typical examples of these are shown in Figures 1and 2. Thus, the concentrations of fatty acids in dietary lipid were related linearly to their concentrations in flesh total lipid although the slopes of the plots in Figures 1and 2 and in Table 5 are different for each fatty acid. This indicates that the relationship between the concentration of a fatty acid in the diet and the concentration in flesh is different for each fatty acid. This is demonstrated more clearly in Table 5 from the differences ( values) between the concentration of individual fatty acids in dietary lipid and flesh lipid for fish fed the diets containing 100% FO, 100% LO and 100% RO. This demonstrates that, of all the fatty acids shown in Table 5, only 22:6(n-3) was present in flesh at a concentration equal to or greater than that in the diet for all three treatment groups. This is in contrast to the other (n-3) PUFA, 18:3(n-3) and 20:5(n-3), which were always present at lower concentrations in the flesh compared with the diets. Oleic acid [18:1(n-9)] was the only other fatty acid showing a positive value for FO and LO, and these were negligible. The saturated fatty acids were also preferentially retained when present at low concentrations as in the LO and RO treatments. In contrast to 22:6(n-3), the fatty acids:18:1(n-9), 18:2(n-6), 18:3(n-3) and 22:1 were preferentially discriminated against in flesh relative to diet when present at high concentrations in dietary lipid. Thus, when a particular fatty acid was abundant in the diet, such as 18:3(n-3) in 100% LO or 22:1 in 100% FO, that fatty acid was not selected for deposition in the flesh but was selectively utilized for metabolism, probably for energy production.
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40% compared with fish fed the 100% FO diet throughout. A similar result was observed for 18:3(n-3) for which concentrations in fish previously fed the 100% LO and RO diets were still significantly higher than those fed 100% FO but had declined by 64 and 56% for fish fed LO and RO, respectively, after the 20-wk washout period (Fig. 3B).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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400 g. In the present study, salmon smolts with an initial weight of 120 g were grown to their harvest weight of 2 kg using diets in which the added oil component contained between 33 and 100% LO and/or RO. Although neither RO and LO contain any (n-3) HUFA, they do contain substantial levels of -linolenic acid, which is also thought to be beneficial for human health (23,31). There were no significant effects of dietary treatment on fish weights when measured after 32 wk (results not shown) but by 50 wk, the weights were significantly different and ranged from 1.92 to 2.59 kg. However, regression analysis showed no relationship between final weight and any dietary fatty acid [including 16:0, 18:1(n-9) or total monoenes], suggesting that dietary treatment was not responsible for the differences (results not shown).
A number of earlier studies utilized RO in feed formulations for salmonids, and no changes in growth rates and feed conversion were observed (17,32–34). Linseed oil has also been used, either alone or blended with RO, with no apparent detrimental effects on growth (16,17,35,36). However, some of these studies used purified or semipurified diets containing relatively low dietary lipid levels, and they were conducted for relatively short periods of time compared with the present study. A number of recent studies have used high energy/lipid formulations with various vegetable oils and found no detrimental effects on growth, although these were also of shorter duration than the present study (13–15).
In the present study, flesh lipid content ranged from 6.9 to 9.5% although there were no significant differences between dietary treatments (P = 0.099). In previous studies in which RO or palm oil was substituted for FO, flesh lipid concentration was reduced in fish fed 50% RO and 50 and 100% palm oil compared with fish fed 100% FO (14,15).
In salmonid fish, the fatty acid compositions of tissue lipids are closely related to that of dietary fatty acid compositions (13,33,37), especially in the flesh in which triacylglycerols (TAG) are the predominant lipid class (20). This relationship is clearly demonstrated in the present study in which linear correlations were observed between flesh fatty acid concentrations and their concentrations in dietary lipid. Similar linear relationships were demonstrated in previous trials in which graded inclusion of RO or palm oil was used to replace FO (14,15). However, slopes and correlation coefficients differed among these studies, suggesting that selective retention or metabolism of individual fatty acids may vary depending on the blend of dietary fatty acids, and the size and age of the fish. The correlation coefficients in the present study are particularly high, with r values between 0.99 and 1.00, which may reflect the longer trial period and the larger size of fish at sampling, compared with previous studies (14,15). These linear correlations can be used practically to predict the flesh fatty acid concentration in salmon fed different blends of LO, RO and FO in the later stages of the seawater growth phase. In addition, the data in Figures 1and 2, along with data in Tables 4, and 5 reveal how different dietary fatty acids are selectively retained or metabolized in flesh lipids depending on their relative concentration in each oil blend. For example, in all dietary treatments, 22:6(n-3) was selectively deposited in muscle lipid regardless of the concentration in the diet. This preferential retention of 22:6(n-3), presumably via specificity of the fatty acyl transferases for incorporation into flesh TAG and phospholipid, is clearly demonstrated (Table 5). The differences ( values) between diet and flesh 22:6(n-3) concentration (Table 5) give values of 1.5–2.3 for the 100% FO, LO and RO treatments.
In contrast, all other fatty acids described in Table 5, including EPA, were progressively favored for metabolism, presumably largely for energy production, as their dietary concentration increased. This is true for the monoenes 22:1 and 18:1(n-9) which were selectively utilized in the 100% FO and 100% RO treatments, respectively, and presumably reflects the ease with which these fatty acids can be catabolized by ß-oxidation (11,38). However, when 18:1(n-9) and 22:1 are present in the diet in similar quantities, as in the 100% FO diet, then 22:1 appears to be the preferred substrate for catabolism. By contrast, when 18:1(n-9) is present in excess as in the 100% RO diet then 18:1(n-9) appears to be readily oxidized. However, when 18:1(n-9) and 18:3(n-3) are present in similar concentrations, as in the FO/LO 2:1 diet, then the values between diet and flesh suggest that 18:3(n-3) is selectively catabolized in preference to18:1(n-9) ( values were -6.6 and -0.2, respectively). There was a similar apparent preference of 18:2(n-6) over 18:1(n-9) in fish fed the 100% LO diet ( values of -1.9 and 0.1, respectively), whereas there was also an apparent preference for catabolism of 18:3(n-3) over 18:2(n-6), when present at similar concentrations, in fish fed the LO/RO 1:2 diet ( values of -3.7 and -2.7, respectively). These results support those found in a recent study using deuterated 18:3(n-3), which showed that catabolism via ß-oxidation was preferred over conversion to 22:6(n-3) in juvenile rainbow trout (18). The apparent selection against metabolism of 18:1(n-9), and also of the saturated fatty acids, principally 16:0 and 18:0, might be due to their structural function as components of membrane phospholipids at the sn-1 position, with HUFA, particularly 22:6(n-3), being favored in the sn-2 position (39,40). These data suggest that, unless 18:1(n-9) is present in excess, 22:1, 18:3(n-3) and 18:2(n-6) appear to be the preferred substrates for oxidation.
In addition to being oxidized for energy, both 18:3(n-3) and 18:2(n-6) are substrates for 6-desaturation and elongation. It was shown previously that Atlantic salmon hepatocytes favor 18:3(n-3) over 18:2(n-6) as a substrate for desaturation and elongation (16); thus, the apparent differences among mobilization of flesh 18:3(n-3),18:2(n-6) and 18:1(n-9), described above, may be due in part to the favoring of the former for conversion to HUFA as well as for oxidation (16). A number of previous studies confirmed that the activity of the desaturation and elongation pathways is significantly increased after inclusion of dietary vegetable oils (14–17).
There is now considerable evidence that increased consumption of (n-3) HUFA, especially 20:5(n-3) and 22:6(n-3) and reduced consumption of (n-6) PUFA, principally 18:2(n-6), can have significant benefits for human health (3,41,42). Increased consumption of oily fish including herring, sardines, mackerel and salmon can provide the necessary (n-3) HUFA in human diets. However, because global capture fisheries have reached their sustainable limit, further demand for fish for human consumption will have to be provided by increased aquaculture production (6). At the present time, salmon produced by aquaculture, using diets containing only marine FO, is rich in (n-3) HUFA and is a valuable component of human diets (20,21,43). Therefore, any substitution of FO with vegetable oils should be carried out in such a way as to ensure that the qualities that make cultured salmon a healthy food option, i.e., high levels of 20:5(n-3) and 22:6(n-3), are maintained. The present study suggests that substitution of FO with RO and/or LO, up to 66% of total added oil, results in a moderate reduction of (n-3) HUFA but also leads to increased deposition of 18:2(n-6). The second phase of the experiment involved returning fish, previously fed 100% LO and RO to diets containing only FO for a period of 20 wk, in an attempt to "wash out" the C18 PUFA from the vegetable oils. This action restored (n-3) HUFA levels to 80% and lowered 18:2(n-6) levels, although they later remained 50% higher than those present in fish fed 100% FO. These data are similar to a previous study using smaller salmon smolts in which diets containing increasing levels of RO were fed for 16 wk, followed by a 12-wk washout phase (44). In both studies, the washout phase restored DHA and EPA levels to values similar to those in fish fed FO throughout, yet 18:2(n-6) values remained significantly elevated (44). These results support the rationale that vegetable oils used for FO replacement in salmon should ideally contain minimal levels of 18:2(n-6). If salmon is to be regarded as a valuable source of (n-3) HUFA for humans, then it should also ideally contain low levels of 18:2(n-6). It is widely known that the dietary intake of 18:2(n-6) in the Western diet is too high and that a high ratio of (n-6)/(n-3) PUFA is proinflammatory (3,4,45).
In summary, the results from the present study suggest that Atlantic salmon can be raised on diets in which FO is replaced with different blends of LO, RO and FO for the entire seawater culture phase, without apparent detriment to fish growth and health. However, for fish in which vegetable oil replaced >66% of the added dietary oil, considerable reductions of flesh concentrations of both 20:5(n-3) and 22:6(n-3) occurred. Returning fish previously fed 100% RO or LO to a marine FO diet for a period before harvest allowed flesh (n-3) HUFA concentrations to be restored to 80% of values in fish fed FO throughout the seawater phase although 18:2(n-6) remained significantly higher.
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FOOTNOTES |
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Manuscript received 31 March 2003. Initial review completed 25 April 2003. Revision accepted 25 June 2003.
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