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Total replacement of dietary fish oil with alternative lipid sources in a practical diet for mandarin fish, Siniperca scherzeri, juveniles

Total replacement of dietary fish oil with alternative lipid sources in a practical diet for... A 12-week feeding trial was designed to evaluate the effect of total replacement of fish oil (FO) with terrestrial alternative oils on growth, feed utilization, body composition, hematological parameters, and fillet fatty acid profile of mandarin fish juveniles. Four iso-nitrogenous (56% crude protein) and iso-lipidic (13% crude lipid) practical diets were formulated. A control diet contained 6% FO and three other experimental diets were prepared by replacing FO with linseed oil, soybean oil, and lard (designed as FO, LO, SO, and lard, respectively). Each diet was randomly allocated to triplicate groups of 25 fish (1.8 ± 0.03 g/fish) in a circular tank. Complete replacement of FO by three tested alternative oils had no remarkable impact on growth performance, feed utilization efficiency, and morphological and hematological parameters of juvenile mandarin fish. However, daily feed intake was found to be significantly higher for fish fed the SO diet compared with those fed the FO and LO diets. Fish fed LO and SO diets exhibited significantly higher levels of the whole body lipid compared to fish fed diet containing FO. Fillet fatty acid composition reflected dietary fatty acid profile. The highest level of α-linolenic acid, linoleic acid, and oleic acid was observed in fish fillet fed LO, SO, and lard, respectively. Although the eicosapentaenoic acid level of fish fillet fed diet FO was higher than other treatments, no significant difference was found in docosahexaenoic acid content among all dietary groups. The results of the present study clearly demonstrate that the complete replacement of FO in mandarin fish diets is achievable. These findings are useful in dietary formulation to reduce feed costs without compromising mandarin fish growth. Keywords: Growth performance, Feed utilization efficiency, Fillet fatty acid composition, Fish oil replacement, Mandarin fish, Siniperca scherzeri Background issues and rising costs linked with FO have exerted and Feed ingredients of marine origin such as fish meal (FM) continue to exert substantial pressure on global aquafeed and fish oil (FO) have been extensively used as the main sector to find economically viable and environmentally protein and lipid sources in the aquafeeds. Fish oil is sustainable substitutions. In this regard, terrestrial oils, particularly popular in aquafeed industry because of its particularly vegetable oils, have been considered as the high proportions of n-3 long-chain polyunsaturated fatty prime candidates for FO replacement in aquafeeds due to acids (LC-PUFA) that play an important role in suppor- their high availability and relatively lower prices (Turchini ting normal growth, health, and nutritional quality of et al. 2011b). In comparison to FO, however, oils of terres- farmed aquatic animals (Turchini et al. 2011b). However, trial origin are typically rich in C fatty acids, mainly lino- it is clearly evident that the aquafeed-manufacturing in- leic (LA, 18:2n-6), α-linolenic (ALA, 18:3n-3), and oleic dustry cannot continue to rely on this highly palatable and (OA, 18:1n-9) acids, but lack or have a very limited con- nutritious marine ingredient. Indeed, the sustainability tent of the n-3 LC-PUFA, such as eicosapentaenoic (EPA, 20:5-3) and docosahexaenoic (DHA, 22:6n-3) acids, which are regarded as undesirable nutritional properties (Bureau * Correspondence: smlee@gwnu.ac.kr and Meeker 2011; Nasopoulou and Zabetakis 2012). Con- Department of Marine Bioscience and Technology, Gangneung-Wonju National University, Gangneung 25457, South Korea sequently, numerous studies have investigated the efficacy Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 2 of 9 of various oils of terrestrial origin in feeds for cultured Methods fish. Overall, the literature evidence suggests that most al- Experimental diets ternative oil sources are able to replace FO to some extent Fatty acid composition of the tested oil sources are shown depending upon the species studied and also the type and in Table 1 and the formulation and proximate composition fatty acid content of the alternative oil used (Turchini et of the experimental diets are presented in Table 2.Four al. 2011b). It is also now generally recognized that partial iso-nitrogenous (approximately 56% crude protein) and or full substitution of FO is more feasible for freshwater iso-lipidic (approximately 13% crude lipid experimental di- fish than marine species which apparently lack the ability ets, varying only in the added lipid source) were formulated to desaturate and elongate C PUFA and therefore are using anchovy FM as the main source of protein. In all the very prone to n-3 LC-PUFA deficiency (Tocher 2010). In- experimental diets, ~ 6% lipid was provided from the re- deed, a review of previous experiments with freshwater sidual oil in the FM and other dietary ingredients, while the species such as Murray cod, Maccullochella peelii peelii other 6% lipid was achieved through separate addition of (Turchini et al. 2011a); pikeperch, Sander lucioperca (L.) four different oil sources including fish oil (FO), linseed oil (Kowalska et al. 2012); snakehead, Channa striatus (LO), soybean oil (SO), and lard to the diet, and the result- (Aliyu-Paiko and Hashim 2012); darkbarbel catfish, Pelteo- ant experimental diets were named accordingly. For prepar- bagrus vachelli (Jiang et al. 2013); Nile tilapia, Oreochro- ing each experimental diet, all the dry ingredients were mis niloticus (Peng et al. 2015;Apraku et al. 2017); gibel thoroughly mixed with oil and distilled water to form a carp, Carassius auratus gibelio (Zhou et al. 2016); silver sticky dough, which was then passed through a mincer catfish, Rhamdia quelen (Lazzari et al. 2016); and rainbow (SMC-32, SL Co., Incheon, South Korea) to produce trout, Oncorhynchus mykiss (Gause and Trushenski 2013; 3.0-mm-diameter feed strands. The moist feed strands were Yıldızetal. 2018); has shown that it is possible to replace then chopped into pellets of a desired length (approxi- FO by single or a mixture of terrestrial oils (both vegetable mately 15 to 18 mm), dried on wire racks at 25 °C in a and animal oils) without compromising growth or feed forced air oven overnight, and kept frozen at − 20 °C until efficiencies. used. A pilot study in our laboratory has shown that the Mandarin fish, Siniperca scherzeri, is a strict freshwater size, shape, and texture of the feed pellets play an important piscivore mainly found throughout East China, Korea, and role in the acceptance of artificial diets by mandarin fish Northern Vietnam (Zhou et al. 1988;Li 1991). The grow- which is well known for its very unique food preference ing interest in mandarin fish culture has been triggered by (Liang et al. 1998;Liet al. 2017). The fish was found to be increasing demand on its shrinking wild stock (Wu et al. most attracted to the 15 to 18-mm-long moist pellets, 1997; Chu et al. 2013). Yet, so far, there is relatively little which contained more than 30% moisture. scientific information available concerning mandarin fish nutrition (Zhang et al. 2009; Lee et al. 2012; Sankian et al. 2017, 2018, 2019), and its commercial production still Table 1 Major fatty acid composition (% total fatty acids) of the relies on expensive live prey. Hence, one of the most im- tested oil sources portant steps in developing and implementing a profitable Oil sources and sustainable culture practice for this species is to FO LO SO Lard formulate a nutritionally balanced and cost-effective com- 14:0 9.8 0.1 0.1 2.1 mercial feed. A recent feeding trial with mandarin fish 16:0 19.6 5.6 11.9 22.6 juveniles, of < 9 g, in our laboratory demonstrated that a diet containing 55% crude protein and 14% crude lipid 18:0 3.9 3.6 4.1 12.2 yielded the best feeding and growth performance (Sankian 16:1n-7 10.7 0.1 0.1 2.1 et al. 2017). However, there is no information available on 18:1n-9 (OA) 7.0 16.0 26.1 43.3 the use of alternative lipid source in a practical diet of this 18:2n-6 (LA) 1.5 15.5 48.2 11.2 species. Therefore, the overall aim of this study was to 18:3n-3 (ALA) 0.6 48.7 5.8 0.1 investigate the possible effects of total substitution of 20:4n-6 –––– dietary FO with alternative lipid sources including lin- seed oil, soybean oil, or lard on mandarin fish juve- 20:5n-3 (EPA) 15.4 ––– niles in terms of growth performance, efficiency of 22:5n-3 –––– feed utilization, whole body proximate composition, 22:6n-3 (DHA) 5.7 ––– biochemical indices, and fillet fatty acid profile. It is FO fish oil, LO linseed oil, SO soybean oil likely that the main findings in this study could be Oleic acid Linoleic acid useful in formulating a cost-effective practical diet for α-Linolenic acid this emerging species of increasing interest in the 4 Eicosapentaenoic acid South Korean freshwater aquaculture sector. Decosahexaenoic acid Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 3 of 9 Table 2 Ingredients and proximate composition of the Fish and experimental design experimental diets (% DM) Mandarin fish juveniles were obtained from Inland Fisheries Experimental diets Research Institute (Chungcheongbuk-do, South Korea). The FO LO SO Lard fish were acclimated to the experimental condition in a 5000-L glass tank, connected to a recirculation system, at Ingredients (% DM) the GWNU Marine Biology Center in ambient freshwater Anchovy FM 55.0 55.0 55.0 55.0 temperature (24 ± 0.1 °C, mean ± SE), feeding on a repelleted Casein 5.0 5.0 5.0 5.0 commercial feed (50% crude protein and 13% lipid; Wheat gluten 10.0 10.0 10.0 10.0 Woosung, Daejeon, South Korea) with the same size as Wheat flour 20.0 20.0 20.0 20.0 the experimental diets. Following the 1-week accli- Fish oil 6.0 ––– mation procedure, 25 fish with an initial mean body Linseed oil – 6.0 –– weight of 1.8 ± 0.03 g were randomly stocked into each Soybean oil –– 6.0 – 65-L polyvinyl circular tank supplied with filtered and dechlorinated tap water using a freshwater recirculating Lard –– – 6.0 (closed) system. Triplicate groups of fish were fed one Vitamin premix 1.5 1.5 1.5 1.5 3 of the formulated diets to apparent satiation twice a Mineral premix 1.8 1.8 1.8 1.8 day at 09:00 and 17:00 for 12 weeks. The uneaten feed Stay-C (50%) 0.3 0.3 0.3 0.3 was siphoned out, dried to constant weight, and then Vitamin E (25%) 0.2 0.2 0.2 0.2 weighed to estimate the amount of feed consumed. The Choline (50%) 0.2 0.2 0.2 0.2 mean water temperature during the experimental period Proximate composition was 24 ± 0.1 °C. The photoperiod was maintained on a (% DM) 12:12-h (light/dark) schedule. Fish were deprived of feed Dry matter 70.5 63.7 66.8 60.4 for 16 h prior to weighing or sampling to minimize hand- Crude protein 56.0 56.2 56.8 56.9 ling stress on fish. Crude lipid 13.0 13.2 13.2 13.3 Ash 11.0 11.0 11.0 11.2 Sample collection Fatty acids (% total fatty acids) At the end of the experiment, all the survived fish in 14:0 8.5 1.7 1.6 3.0 each tank were counted and weighed for calculation of growth performance, feed utilization parameters, and 16:0 21.2 11.2 15.1 22.7 survival rates. Total body length was measured for each 18:0 4.5 4.2 4.5 10.1 individual fish to the nearest 0.1 mm. A random sample 16:1n-7 8.3 0.9 0.8 2.2 of 5 fish per tank was collected and stored at − 43 °C for 18:1n-9 (OA) 8.3 14.3 20.7 32.8 subsequent whole body proximate composition analyses. 18:2n-6 (LA) 1.6 11.2 32.7 8.1 Blood samples were collected from the caudal veins of 18:3n-3 (ALA) 0.7 33.7 4.2 0.4 six anesthetized (200 mg/L MS-222, Sigma, St. Louis, 20:4n-6 0.8 0.7 0.7 0.7 MO, USA) individual fish per tank (nine fish/dietary 20:5n-3 (EPA) 14.5 3.7 3.6 3.6 treatment) using heparinized syringes. Blood samples were kept on ice prior to plasma separation by centri- 22:5n-3 11.4 0.6 0.6 0.6 fugation at 7500 RPM for 10 min using a high-speed 22:6n-3 (DHA) 16.6 12.4 12.1 12.3 refrigerated microcentrifuge (HanilBioMed Inc., Gwangju, FO fish oil, LO linseed oil, SO soybean oil Pesquera Bahia Caldera, Caldera, Chile; with crude protein 69.1%, crude South Korea). Plasma samples were immediately stored at lipid 12.6%, ash 14.1% dry matter − 80 °C until used in subsequent hematological analyses Vitamin premix contained the following amounts which were diluted in including total protein (TP), total cholesterol (TCHO), cellulose (g/kg premix): DL-α-tocopheryl acetate, 18.8; thiamin hydrochloride, 2.7; riboflavin, 9.1; pyridoxine hydrochloride, 1.8; niacin, aspartate aminotransferase (AST), alanine aminotrans- 36.4; Ca-D-pantothenate, 12.7; myo-inositol, 181.8; D-biotin, 0.27; folic ferase (ALT), alkaline phosphatase (ALP), albumin acid, 0.68; p-aminobenzoic acid, 18.2; menadione, 1.8; retinyl acetate, 0.73; cholecalciferol, 0.003; cyanocobalamin, 0.003 (ALB), and total bilirubin (TBIL). Immediately after Mineral premix contained the following ingredients (g/kg premix): blood sampling, fish (6 fish/tank; 18 fish/dietary treat- MgSO ·7H O, 80.0; NaH PO ·2H O, 370.0; KCl, 130.0; ferric citrate, 40.0; 4 2 2 4 2 ment) were dissected to obtain their liver and visceral ZnSO ·7H O, 20.0; Ca-lactate, 356.5; CuCl, 0.2; AlCl ·6H O, 0.15; KI, 0.15; 4 2 3 2 Na Se O , 0.01; MnSO ·H O, 2.0; CoCl ·6H O, 1.0 2 2 3 4 2 2 2 weights for calculating the hepatosomatic (HSI) and Oleic acid viscerosomatic (VSI) indices, respectively. Fillet samples Linoleic acid α-Linolenic acid were subsequently dissected out of the same fish and Eicosapentaenoic acid stored at − 80 °C until proximate and fatty acid com- Decosahexaenoic acid position analyses. Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 4 of 9 Analytical methods Protein efficiency ratioðÞ PER ¼ Chemical composition analyses wet weight gain ðÞ g =total protein consumedðÞ g Chemical composition of the experimental diets, whole body, and fillet samples was determined according to the Condition factorðÞ CF;%¼ standard methods (AOAC 2005). Moisture content was fish body weight=ðÞ total length of fish ðÞ cm  100 estimated by oven drying at 105 °C for 6 h. Crude protein content was determined by an automated Kjeldahl system Hepatosomatic indexðÞ HSI;%¼ (Buchi, Flawil, Switzerland). Crude lipid was measured ðÞ liver weight ðÞ g =fish body weight 100 using a Soxhlet extractor (VELP Scientifica, Milano, Italy), and ash content by a Thermolyne™ combustion in a muffle Viscerosomatic indexðÞ VSI;%¼ furnace at 600 °C for 4 h. ðÞ viscera weight ðÞ g =fish body weight 100 Hematological analysis Data were analyzed as a completely random design Plasma samples were analyzed for TP, TCHO, AST, ALT, with the tank as the experimental unit, using one-way ALP, ALB, and TBIL concentrations using an automated ANOVA in SPSS program version 22.0 (SPSS Inc., blood analyzer (DRI-CHEM NX500i, FUJIFILM Corpo- Chicago, IL, USA). When ANOVA identified differences ration Tokyo, Japan). among groups, Tukey’s honest significant difference multiple range test was performed to detect statistically Fatty acid analyses significant differences between mean responses at a Total lipids in oil sources, experimental diets, and fillet significance level of P < 0.05. Data were checked for nor- samples were extracted following the Folch et al. (1957) mal distribution (Shapiro-Wilk’s test) and homogeneity method using a chloroform and methanol mixture (2:1 v/v). of variances (Levene’s test) and when necessary arcsine Extracted lipids were then submitted to acid-catalyzed transformed. Data were presented as mean ± standard transmethylation using BF -MeOH (Sigma, St. Louis, MO, error (SE.) of the triplicate groups. USA) to obtain fatty acid methyl esters (FAMEs). Then, FAMEs were analyzed using a PerkinElmer Clarus 600 gas Results chromatograph (Shelton, CT, USA) equipped with a The results of growth, feed utilization, and morphological flame-ionization detector and a SP-2560 capillary column parameters of mandarin fish juveniles are presented in (100 m × 0.25 mm i.d., 0.2-μm film thickness; Supelco, Bel- Table 3. The total replacement of dietary FO by different lefonte, PA, USA) using helium as the carrier gas and lipid sources showed no significant negative effect on temperature programmed operation from 140 to 240 °C in growth performance in terms of final body weight (10.3– increments of 5 °C/min. The temperature of both injector 11.6 g), WG (499–549%), and SGR (2.13–2.23%). Although and detector was adjusted at 240 °C. Fatty acids were identi- growth rates were not significantly affected, fish received fied by comparison with standard FAME mixtures (FAME FO and LO diets grew slightly better and were numerically 37 and PUFA 3; Supelco, Bellefonte, PA, USA) and data larger than those fed the other two diets. The DFI of fish analyzed using TotalChrom software (version 6.3.1; fed the SO diet was significantly higher than those of fish PerkinElmer Inc., Shelton, CT, USA). fed FO and LO diets. No remarkable differences on DPI, FE, and PER were observed among any of the treatments Formulae, calculations, and statistical analysis (P > 0.05). The survival rate was higher than 97%, and there was no significant difference among all experimental Weight gainðÞ WG;%¼ groups. Similarly, the total substitution of FO with LO, SO, ½ ðÞ final body weight−initial body weight =initial body weight 100 or lard had no significant effects on fish morphological parameters. Specific growth rateðÞ SGR;%=day¼ The results of whole body proximate composition are ½ ðÞ ln final body weight− ln initial body weight =days 100 presented in Table 4. No significant differences were ob- Daily feed intakeðÞ DFI;%¼ served in whole body composition in terms of moisture, ftotal dry feed consumedðÞ g =½ðinitial fish weight þ final fish weight crude protein, and ash contents among all experimental þdead fish weightÞ days=2g  100 groups. Total replacement of dietary FO with three dif- ferent oil sources resulted in increased fat levels in man- Daily protein intakeðÞ DPI;%¼ darin fish body. Fish fed the LO and SO diets had ftotal protein consumedðÞ g =½ðinitial fish weight significantly higher crude lipid level in the whole body þfinal fish weight þ dead fish weightÞ days=2g  100 than that of fish fed FO diet. Feed efficiencyðÞ FE;%¼ The results of hematological parameters are reported ðÞ wet weight gain ðÞ g =total dry feed consumedðÞ g 100 in Table 5. There was neither a considerable difference Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 5 of 9 Table 3 Growth performance, feed utilization efficiency, and Table 5 Hematological parameters of mandarin fish fed the morphological parameters of mandarin fish fed the four four experimental diets for 12 weeks experimental diets for 12 weeks Experimental diets Experimental diets FO LO SO Lard FO LO SO Lard TP 4.33 ± 0.17 4.17 ± 0.20 4.03 ± 0.32 4.80 ± 0.12 IBW 1.8 ± 0.02 1.8 ± 0.02 1.7 ± 0.01 1.8 ± 0.02 2 TCHO 205 ± 8 190 ± 13 187 ± 13 219 ± 9 FBW 11.6 ± 0.3 10.9 ± 0.3 10.3 ± 0.03 10.7 ± 0.4 3 AST 174 ± 16 224 ± 61 172 ± 22 274 ± 11 WG 549 ± 20 524 ± 18 503 ± 1 499 ± 13 4 ALT 10.0 ± 0.6 10.0 ± 0.0 8.7 ± 0.3 11.0 ± 6.7 SGR 2.23 ± 0.04 2.18 ± 0.04 2.14 ± 0.00 2.13 ± 0.03 5 ALP 412 ± 30 342 ± 30 341 ± 40 489 ± 34 5 a a b ab DFI 2.54 ± 0.10 2.50 ± 0.06 2.81 ± 0.02 2.72 ± 0.04 6 ALB 0.77 ± 0.03 0.67 ± 0.03 0.70 ± 0.06 0.83 ± 0.03 DPI 1.44 ± 0.06 1.42 ± 0.03 1.57 ± 0.01 1.53 ± 0.02 7 TBIL 0.53 ± 0.09 0.60 ± 0.12 0.77 ± 0.09 0.73 ± 0.17 FE 69.1 ± 3.2 69.1 ± 2.3 61.4 ± 0.8 62.5 ± 1.2 Values are mean of triplicate groups and presented as mean ± SE. Values with 8 different superscripts in the same row are significantly different (P < 0.05). The PER 1.44 ± 0.06 1.45 ± 0.04 1.31 ± 0.01 1.34 ± 0.02 lack of superscript letter indicates no significant differences among treatments Survival (%) 98.7 ± 1.33 97.3 ± 1.33 98.7 ± 1.33 98.7 ± 1.33 FO fish oil, LO linseed oil, SO soybean oil Total protein (g/dL) CF 1.14 ± 0.11 1.41 ± 0.06 1.17 ± 0.02 1.14 ± 0.11 2 Total cholesterol (mg/dL) 10 Asparatet aminotransferase activity (U/L) HSI 2.06 ± 0.10 3.04 ± 0.57 2.47 ± 0.28 2.24 ± 0.09 Alanine aminotransferase activity (U/L) 11 5 VSI 9.93 ± 0.73 10.42 ± 0.50 9.65 ± 0.74 8.95 ± 0.30 Alkaline phosphatase (U/L) Albumin (g/dL) Values are mean of triplicate groups and presented as mean ± SE. Values with Total bilirubin (mg/dL) different superscripts in the same row are significantly different (P < 0.05). The lack of superscript letter indicates no significant differences among treatments altered fillet fatty acid profile. Regarding saturated fatty FO fish oil, LO linseed oil, SO soybean oil Initial mean body weight (g) acids (SFAs), the highest content of myristic acid (14:0) Final mean body weight (g) 3 was noted in fish fed the FO diet, which differed signifi- Weight gain (%) = [(final bodyweight – initial bodyweight)/initial body weight] × 100 cantly from the other three dietary treatments. Fillets of Specific growth rate (%/day) = [( ln final fish fed diets containing lard in place of FO had signifi- bodyweight – ln initial bodyweight]/days] × 100 cantly higher levels of palmitic acid (16:0) than do fillets Daily feed intake (%) = {total dry feed consumed (g)/[(initial fish weight + final fishweight + dead fishweight) × days/2]} × 100 Daily protein intake (%) = {total of fish fed the other experimental diets. While no statis- protein consumed (g)/[(initial fishweight + final tically significant differences were found among LO, SO, fishweight + dead fishweight) × days/2]} × 100 Feed efficiency (%) = (wet weight gain (g)/total dry feed consumed (g)) × 100 and lard groups, the stearic acid (18:0) content of fillet Protein efficiency ratio = wet weight gain (g)/total protein consumed (g) in lard group was significantly higher than that of 9 3 Condition factor (%) = [fish body weight/(total length of fish) (cm) ] × 100 FO-fed fish. With respect to monounsaturated fatty Hepatosomatic index (%) = (liver weight (g)/fish body weight) × 100 Viscerosomatic index (%) = (viscera weight (g)/fish body weight) × 100 acids (MUFAs), fillets of fish fed FO and lard diets con- tained significantly higher palmitoleic acid (16:1n-7) nor any discernible trend among dietary groups regard- compared to fish fed on LO and SO diets. A significantly ing plasma hematological parameters. greater level of OA was found in the fillet of fish fed lard Results on fillet proximate composition and fatty acid diet compared to the other dietary groups. By evaluation profile are given in Table 6. No significant effect nor any of n-6 fatty acid levels in the fish fillet, the highest con- defined trend was found in fillet proximate composition centration of LA was found in fish fed on diets contain- among dietary treatments. However, the addition of ing SO. Alternative oil treatments had no significant vegetable oil or animal fat in fish diet significantly impact on fillet arachidonic acid (AA, 20:4n-6) content. With respect to the fillet n-3 fatty acid composition, fish fed the LO diet had significantly higher levels of ALA Table 4 Whole body proximate composition of mandarin fish fed the four experimental diets for 12 weeks (% wet weight) than that of fish fed the FO-based diet, which was itself significantly higher than those found in the SO and lard Experimental diets groups. Fillets of fish fed diets containing FO had signifi- FO LO SO Lard cantly higher concentrations of EPA than those fed diets Moisture 79.1 ± 1.5 77.0 ± 0.6 76.7 ± 1.7 77.8 ± 1.52 containing the other three oil sources. The 22:5n-3 con- Crude protein 11.3 ± 0.6 11.8 ± 0.5 13.4 ± 0.9 12.4 ± 1.8 tent of fillet in FO fish was significantly higher than that a b b ab Crude lipid 3.85 ± 0.17 5.95 ± 0.34 5.80 ± 0.12 4.84 ± 0.67 of lard diet-fed fish, while no significant differences in Ash 3.34 ± 0.12 3.36 ± 0.21 3.55 ± 0.48 3.51 ± 0.24 fillet 22:5n-3 among LO, SO, and lard diet-fed fish were Values are mean of triplicate groups and presented as mean ± SE. Values with observed. The DHA contents of the fish fillets were different superscripts in the same row are significantly different (P < 0.05). The numerically lower in the LO, SO, and lard groups lack of superscript letter indicates no significant differences among treatments FO fish oil, LO linseed oil, SO soybean oil compared to fish fed the FO diet. Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 6 of 9 Table 6 Fillet proximate and fatty acid composition of mandarin fish fed the four experimental diets for 12 weeks Experimental diets FO LO SO Lard Proximate composition (% wet weight) Moisture 77.9 ± 0.8 79.1 ± 0.4 78.7 ± 1.2 77.6 ± 0.4 Crude protein 18.1 ± 0.5 18.1 ± 0.8 17.6 ± 0.9 18.8 ± 0.6 Crude lipid 1.44 ± 0.36 1.70 ± 0.27 1.36 ± 0.17 1.32 ± 0.24 Ash 1.37 ± 0.16 1.03 ± 0.11 1.14 ± 0.09 1.46 ± 0.02 Fatty acid (% total fatty acid) b a a a 14:0 2.54 ± 0.17 1.84 ± 0.12 1.45 ± 0.02 1.68 ± 0.03 a a a b 16:0 21.8 ± 0.5 20.8 ± 0.1 20.8 ± 0.2 23.4 ± 0.7 a ab ab b 18:0 5.30 ± 0.12 5.91 ± 0.14 6.01 ± 0.28 6.64 ± 0.25 b a a b 16:1n-7 5.61 ± 0.58 2.42 ± 0.18 2.49 ± 0.37 4.94 ± 0.12 1 a a a b 18:1n-9 (OA) 21.5 ± 1.7 21.2 ± 0.7 20.3 ± 0.1 27.98 ± 1.2 2 a b c ab 18:2n-6 (LA) 4.90 ± 0.31 7.38 ± 0.20 15.86 ± 0.45 6.29 ± 0.39 3 b c a a 18:3n-3 (ALA) 4.90 ± 0.28 10.47 ± 0.48 2.78 ± 0.31 1.67 ± 0.02 20:4n-6 1.92 ± 0.32 1.09 ± 0.04 1.09 ± 0.02 1.42 ± 0.04 4 b a a a 20:5n-3 (EPA) 6.20 ± 0.31 4.96 ± 0.05 4.49 ± 0.13 4.59 ± 0.38 b ab ab a 22:5n-3 1.56 ± 0.15 1.42 ± 0.05 1.30 ± 0.03 1.04 ± 0.13 22:6n-3 (DHA) 18.2 ± 1.8 16.4 ± 1.0 15.7 ± 0.2 14.0 ± 1.9 Values are mean of triplicate groups and presented as mean ± SE. Values with different superscripts in the same row are significantly different (P < 0.05). The lack of superscript letter indicates no significant differences among treatments FO fish oil, LO linseed oil, SO soybean oil Oleic acid Linoleic acid α-Linolenic acid Eicosapentaenoic acid Decosahexaenoic acid Discussion diets. Similarly, Du et al. (2008) found markedly higher The growth rate values observed in the present study were feed intake in grass carp, Ctenopharyngodon idella,fnger- much higher than those previously reported for the same lings fed lard or a blend of vegetable oils in comparison species by our research team using practical diets with with a FO-based diet. A large body of literature provides relatively similar protein and lipid contents (Sankian et al. strong evidence to suggest that fish are able to regulate 2017, 2018). This is probably due to the higher initial feed intake in order to meet their metabolizable energy weight of the fish in the previous studies (8–20 vs. 1.8 g in demands (De la Higuera 2001). Within the context of FO the present study). To our knowledge, so far, there is no replacement in aquafeed, if FO is replaced with an equal previous record on the effects of different dietary lipid amount of alternative oil source, minimal differences in source on growth, feed utilization, hematological indices, the total dietary energy content are expected. However, and body/fillet nutritional traits of mandarin fish. The since different oils may have different digestibility, it is findings of the present study showed that FO in a practical possible that the total digestible/metabolizable energy of diet with 13% lipid for juvenile mandarin fish can be com- feed can be partially changed, resulting in variations in pletely replaced by LO, SO, or lard without markedly feed intake. This may partly explain the DFI differences compromising growth performance and feed efficiency. observed in the present study. Our results are in agreement with the previous studies in The replacement of the dietary FO by three different which it was demonstrated that various alternative oils oils, in the present study, did not affect the morpho- could be used to completely replace FO in freshwater fish logical indices of fish, which is often used to indicate the diets without any adverse effect on the nutrient utilization nutritional status of fish. This was in agreement with or growth rates (Turchini et al. 2011a; Kowalska et al. previous studies in other freshwater species, which re- 2012; Jiang et al. 2013; Han et al. 2013; Zhou et al. 2016). ported that the replacement of dietary FO with vegetable However, the DFI value in fish fed with SO diet was oils and rendered animal fat did not affect the morpho- significantly higher than those of fish fed the FO and LO logical parameters of snakehead, Murray cod, rainbow Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 7 of 9 trout, darkbarbel catfish, Nile tilapia, and gibel carp were still higher than their respective levels in diets. This (Figueiredo-Silva et al. 2005; Turchini et al. 2011a; could be due either to selective retention and/or active Aliyu-Paiko and Hashim 2012; Jiang et al. 2013; Peng et synthesis of these fatty acids (Turchini et al. 2011b). al. 2015; Zhou et al. 2016). Similar results were observed in other freshwater fish In the present study, the whole body lipid content of species such as rainbow trout (Caballero et al. 2002; mandarin fish fed the LO and SO diets were significantly Turchini and Francis 2009), Murray cod (Turchini et al. higher than that of fish fed the FO diet. In accordance 2006), common carp (Ren et al. 2012), tilapia (Al-Souti with the present study, significantly high fat was re- et al. 2012, Li et al. 2016), Chinese long snout catfish, corded by Aliyu-Paiko and Hashim (2012) in whole body Leiocassis longirostris Günther (Choi and Lee 2015), and proximate composition of snakehead fingerlings, fed silver barb, Puntius gonionotus (Nayak et al. 2017). It is palm oil as a FO replacer. Similarly, in hybrid tilapia, widely believed that freshwater fish can convert C Oreochromis niloticus × O. aureus, fed tea see oil for PUFA of both n-6 and n-3 series to their corresponding 10 weeks, significantly higher body lipid levels were LC-PUFA via a series of desaturation and elongation re- obtained compared to fish fed FO (Han et al. 2013). It actions (NRC 2011; Turchini et al. 2011b). However, the has been suggested that diets enriched in n-3 LC-PUFA capacity of C PUFAs desaturation/elongation to n-3 may suppress fatty acids synthesis, simulate fatty acid LC-PUFAs is depended on the species (Sargent et al. β-oxidation, activate lipoprotein lipase, and reduce tri- 2002). Therefore, the decreased deposition of dietary acylglycerol synthesis, thereby leading to an overall ALA, LA, and OA along with good growth, feed reduction in lipid deposition and suppressing the de- utilization, and survival in this study is suggestive of the velopment of obesity in mammals (Al-Hasani and ability of mandarin fish to meet their essential fatty acid Joost 2005;Madsenet al. 2005). Indeed, Todorčević requirement by the use of C PUFA. It could also be et al. (2009) reported that feeding FO to Atlantic salmon, assumed that residual fish oil from dietary FM was prob- Salmo salar, for 21 weeks reduced white adipose tissue fat ably adequate to provide essential fatty acids for normal content and increased fatty acid β-oxidation activity growth and development of juvenile mandarin fish. The compared to fish fed rapeseed oil. results of this experiment presented a higher retention Hematological parameters are important indicators of of DHA in fish fed vegetable oil-based or lard diets. fish’s physiological and health status (Maita 2007). Previous studies in which fish were fed vegetable Hematological responses of juvenile mandarin fish were oil-based diets reported high DHA retention in the unaffected by the complete substitution of FO in this muscles of salmonids (Bell et al. 2001, 2003; Caballero study. There are conflicting reports concerning the et al. 2002;Thanuthong etal. 2011). The preferred effects of FO substitution by other oil sources on retention of DHA over EPA may also indicate a se- hematological indices, with some studies suggesting lective utilization of EPA over DHA when dietary marked modifications (Ferreira et al. 2011; Peng et al. levels decrease, as a means of meeting the require- 2015; Mozanzadeh et al. 2016), while others show no ments for tissue membrane integrity and function discernible effects (Figueiredo-Silva et al. 2005; Twibell (Fountoulaki et al. 2009). et al. 2012). This discrepancy can be attributed to va- rious factors including fish species, life stage, compo- Conclusion sition and nutrient content of the diet, source or quality This study indicates that total FO replacement with LO, of the alternative oil source, and experimental condi- SO, or lard can be tolerated by juvenile mandarin fish tions, mainly water temperature. However, since dietary without any pronounced adverse effects on fish perfor- FO replacement with alternative oils caused no detec- mance and health. The abundance of C PUFAs pro- table change either in morphological indices or in vided by tested alternative oil sources coupled with hematological parameters of juvenile mandarin fish in some n-3 LC-PUFA from the residual lipid of FM in the the present study, it can be concluded that fish were in basal diet appeared to meet the essential fatty acid re- overall good health and nutritional status. quirements of ~ 1.8 g mandarin fish under the condi- The fatty acid composition of mandarin fish fillets tions of the present study. This probably stemmed from closely resembled those of the experimental diets, with the ability of this species to bioconvert C PUFA to fish fed the LO, SO, and lard having remarkably elevated their corresponding LC-PUFA and selectively retain EPA levels of ALA, LA, and OA, respectively. It is well docu- and DHA to some extent. Our findings therefore suggest mented that the fatty acid profile of farmed-fish fillets that mandarin fish juveniles have high tolerance to diets reflects the fatty acid composition of the dietary oil used that differ markedly in fatty acid composition. (Bell et al. 1994). Although replacement of FO with Abbreviations alternative oils resulted in reduced levels of EPA and AA: Arachidonic acid; ALA: α-Linolenic acid; ALB: Albumin; ALP: Alkaline DHA, the levels of these fatty acids in the fish fillets phosphatase; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 8 of 9 CF: Condition factor; DFI: Daily feed intake; DHA: Docosahexaenoic acid; Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR. Replacement of fish DPI: Daily protein intake; EPA: Eicosapentaenoic acid; FE: Feed efficiency; oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid FM: Fish meal; FO: Fish oil; HIS: Hepatosomatic index; LA: Linoleic acid; LC- composition and hepatocyte fatty acid metabolism. J Nutr. 2001;131:1535–43. PUFA: Long-chain polyunsaturated fatty acid; LO: Linseed oil; OA: Oleic acid; Bell JG, McGhee F, Campbell PJ, Sargent JR. Rapeseed oil as an alternative to PER: Protein efficiency ratio; SGR: Specific growth rate; SO: Soybean oil; marine fish oil in diets of post-smolt Atlantic salmon (Salmo salar): changes TCHO: Total cholesterol; TP: Total protein; VSI: Viscerosomatic index; in flesh fatty acid composition and effectiveness of subsequent fish oil “wash WG: Weight gain out”. Aquaculture. 2003;218:515–28. Bell JG, Tocher DR, MacDonald FM, Sargent JR. Effects of diets rich in linoleic (18: Acknowledgements 2n-6) and α-linonenic (18:3n-3) acids on growth, lipid class and fatty acid This research was financially supported by the Fishery Commercialization compositions and eicosanoid production in juvenile turbot (Scophtalmus Technology Development Program [20150575] funded by the Korean maximus L.). Fish Physiol Biochem. 1994;13:105–18. Ministry of Oceans and Fisheries and Basic Science Research Program Bureau DP, Meeker DL. Terrestrial animal fats. In: Turchini GM, Ng WK, Tocher DR, through the National Research Foundation of Korea (NRF) funded by the editors. Fish oil replacement and alternative lipid sources in aquaculture Ministry of Education (No. 2018R1A6A1A03023584). feeds. Boca Raton: CRC Press; 2011. p. 245–66. Caballero MJ, Obach A, Rosenlund G, Montero D, Gisvold M, Izquierdo MS. Funding Impact of different dietary lipid sources on growth, lipid digestibility, tissue This study was financially supported by the Fishery Commercialization fat composition and histology of rainbow trout, Oncorhynchus mykiss. Technology Development Program [20150575] funded by the Korean Aquaculture. 2002;214:253–71. Ministry of Oceans and Fisheries and Basic Science Research Program Choi J, Lee SM. Effect of dietary lipid sources on body fatty acid composition of through the National Research Foundation of Korea (NRF) funded by the Chinese long snout catfish Leiocassis longirostris Günther. Fish Aquat Sci. Ministry of Education (No.2018R1A6A1A03023584). The funding organizations 2015;18:359–65. played an active role in the manufacturing of the experimental diets and Chu W, Li W, Wang K, Liu L, Leng X, Zhang J. Comparative studies on muscle analyses. cellularity and flesh quality of two mandarin fish species, Siniperca chuatsi and Siniperca scherzeri. 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Total replacement of dietary fish oil with alternative lipid sources in a practical diet for mandarin fish, Siniperca scherzeri, juveniles

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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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Abstract

A 12-week feeding trial was designed to evaluate the effect of total replacement of fish oil (FO) with terrestrial alternative oils on growth, feed utilization, body composition, hematological parameters, and fillet fatty acid profile of mandarin fish juveniles. Four iso-nitrogenous (56% crude protein) and iso-lipidic (13% crude lipid) practical diets were formulated. A control diet contained 6% FO and three other experimental diets were prepared by replacing FO with linseed oil, soybean oil, and lard (designed as FO, LO, SO, and lard, respectively). Each diet was randomly allocated to triplicate groups of 25 fish (1.8 ± 0.03 g/fish) in a circular tank. Complete replacement of FO by three tested alternative oils had no remarkable impact on growth performance, feed utilization efficiency, and morphological and hematological parameters of juvenile mandarin fish. However, daily feed intake was found to be significantly higher for fish fed the SO diet compared with those fed the FO and LO diets. Fish fed LO and SO diets exhibited significantly higher levels of the whole body lipid compared to fish fed diet containing FO. Fillet fatty acid composition reflected dietary fatty acid profile. The highest level of α-linolenic acid, linoleic acid, and oleic acid was observed in fish fillet fed LO, SO, and lard, respectively. Although the eicosapentaenoic acid level of fish fillet fed diet FO was higher than other treatments, no significant difference was found in docosahexaenoic acid content among all dietary groups. The results of the present study clearly demonstrate that the complete replacement of FO in mandarin fish diets is achievable. These findings are useful in dietary formulation to reduce feed costs without compromising mandarin fish growth. Keywords: Growth performance, Feed utilization efficiency, Fillet fatty acid composition, Fish oil replacement, Mandarin fish, Siniperca scherzeri Background issues and rising costs linked with FO have exerted and Feed ingredients of marine origin such as fish meal (FM) continue to exert substantial pressure on global aquafeed and fish oil (FO) have been extensively used as the main sector to find economically viable and environmentally protein and lipid sources in the aquafeeds. Fish oil is sustainable substitutions. In this regard, terrestrial oils, particularly popular in aquafeed industry because of its particularly vegetable oils, have been considered as the high proportions of n-3 long-chain polyunsaturated fatty prime candidates for FO replacement in aquafeeds due to acids (LC-PUFA) that play an important role in suppor- their high availability and relatively lower prices (Turchini ting normal growth, health, and nutritional quality of et al. 2011b). In comparison to FO, however, oils of terres- farmed aquatic animals (Turchini et al. 2011b). However, trial origin are typically rich in C fatty acids, mainly lino- it is clearly evident that the aquafeed-manufacturing in- leic (LA, 18:2n-6), α-linolenic (ALA, 18:3n-3), and oleic dustry cannot continue to rely on this highly palatable and (OA, 18:1n-9) acids, but lack or have a very limited con- nutritious marine ingredient. Indeed, the sustainability tent of the n-3 LC-PUFA, such as eicosapentaenoic (EPA, 20:5-3) and docosahexaenoic (DHA, 22:6n-3) acids, which are regarded as undesirable nutritional properties (Bureau * Correspondence: smlee@gwnu.ac.kr and Meeker 2011; Nasopoulou and Zabetakis 2012). Con- Department of Marine Bioscience and Technology, Gangneung-Wonju National University, Gangneung 25457, South Korea sequently, numerous studies have investigated the efficacy Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 2 of 9 of various oils of terrestrial origin in feeds for cultured Methods fish. Overall, the literature evidence suggests that most al- Experimental diets ternative oil sources are able to replace FO to some extent Fatty acid composition of the tested oil sources are shown depending upon the species studied and also the type and in Table 1 and the formulation and proximate composition fatty acid content of the alternative oil used (Turchini et of the experimental diets are presented in Table 2.Four al. 2011b). It is also now generally recognized that partial iso-nitrogenous (approximately 56% crude protein) and or full substitution of FO is more feasible for freshwater iso-lipidic (approximately 13% crude lipid experimental di- fish than marine species which apparently lack the ability ets, varying only in the added lipid source) were formulated to desaturate and elongate C PUFA and therefore are using anchovy FM as the main source of protein. In all the very prone to n-3 LC-PUFA deficiency (Tocher 2010). In- experimental diets, ~ 6% lipid was provided from the re- deed, a review of previous experiments with freshwater sidual oil in the FM and other dietary ingredients, while the species such as Murray cod, Maccullochella peelii peelii other 6% lipid was achieved through separate addition of (Turchini et al. 2011a); pikeperch, Sander lucioperca (L.) four different oil sources including fish oil (FO), linseed oil (Kowalska et al. 2012); snakehead, Channa striatus (LO), soybean oil (SO), and lard to the diet, and the result- (Aliyu-Paiko and Hashim 2012); darkbarbel catfish, Pelteo- ant experimental diets were named accordingly. For prepar- bagrus vachelli (Jiang et al. 2013); Nile tilapia, Oreochro- ing each experimental diet, all the dry ingredients were mis niloticus (Peng et al. 2015;Apraku et al. 2017); gibel thoroughly mixed with oil and distilled water to form a carp, Carassius auratus gibelio (Zhou et al. 2016); silver sticky dough, which was then passed through a mincer catfish, Rhamdia quelen (Lazzari et al. 2016); and rainbow (SMC-32, SL Co., Incheon, South Korea) to produce trout, Oncorhynchus mykiss (Gause and Trushenski 2013; 3.0-mm-diameter feed strands. The moist feed strands were Yıldızetal. 2018); has shown that it is possible to replace then chopped into pellets of a desired length (approxi- FO by single or a mixture of terrestrial oils (both vegetable mately 15 to 18 mm), dried on wire racks at 25 °C in a and animal oils) without compromising growth or feed forced air oven overnight, and kept frozen at − 20 °C until efficiencies. used. A pilot study in our laboratory has shown that the Mandarin fish, Siniperca scherzeri, is a strict freshwater size, shape, and texture of the feed pellets play an important piscivore mainly found throughout East China, Korea, and role in the acceptance of artificial diets by mandarin fish Northern Vietnam (Zhou et al. 1988;Li 1991). The grow- which is well known for its very unique food preference ing interest in mandarin fish culture has been triggered by (Liang et al. 1998;Liet al. 2017). The fish was found to be increasing demand on its shrinking wild stock (Wu et al. most attracted to the 15 to 18-mm-long moist pellets, 1997; Chu et al. 2013). Yet, so far, there is relatively little which contained more than 30% moisture. scientific information available concerning mandarin fish nutrition (Zhang et al. 2009; Lee et al. 2012; Sankian et al. 2017, 2018, 2019), and its commercial production still Table 1 Major fatty acid composition (% total fatty acids) of the relies on expensive live prey. Hence, one of the most im- tested oil sources portant steps in developing and implementing a profitable Oil sources and sustainable culture practice for this species is to FO LO SO Lard formulate a nutritionally balanced and cost-effective com- 14:0 9.8 0.1 0.1 2.1 mercial feed. A recent feeding trial with mandarin fish 16:0 19.6 5.6 11.9 22.6 juveniles, of < 9 g, in our laboratory demonstrated that a diet containing 55% crude protein and 14% crude lipid 18:0 3.9 3.6 4.1 12.2 yielded the best feeding and growth performance (Sankian 16:1n-7 10.7 0.1 0.1 2.1 et al. 2017). However, there is no information available on 18:1n-9 (OA) 7.0 16.0 26.1 43.3 the use of alternative lipid source in a practical diet of this 18:2n-6 (LA) 1.5 15.5 48.2 11.2 species. Therefore, the overall aim of this study was to 18:3n-3 (ALA) 0.6 48.7 5.8 0.1 investigate the possible effects of total substitution of 20:4n-6 –––– dietary FO with alternative lipid sources including lin- seed oil, soybean oil, or lard on mandarin fish juve- 20:5n-3 (EPA) 15.4 ––– niles in terms of growth performance, efficiency of 22:5n-3 –––– feed utilization, whole body proximate composition, 22:6n-3 (DHA) 5.7 ––– biochemical indices, and fillet fatty acid profile. It is FO fish oil, LO linseed oil, SO soybean oil likely that the main findings in this study could be Oleic acid Linoleic acid useful in formulating a cost-effective practical diet for α-Linolenic acid this emerging species of increasing interest in the 4 Eicosapentaenoic acid South Korean freshwater aquaculture sector. Decosahexaenoic acid Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 3 of 9 Table 2 Ingredients and proximate composition of the Fish and experimental design experimental diets (% DM) Mandarin fish juveniles were obtained from Inland Fisheries Experimental diets Research Institute (Chungcheongbuk-do, South Korea). The FO LO SO Lard fish were acclimated to the experimental condition in a 5000-L glass tank, connected to a recirculation system, at Ingredients (% DM) the GWNU Marine Biology Center in ambient freshwater Anchovy FM 55.0 55.0 55.0 55.0 temperature (24 ± 0.1 °C, mean ± SE), feeding on a repelleted Casein 5.0 5.0 5.0 5.0 commercial feed (50% crude protein and 13% lipid; Wheat gluten 10.0 10.0 10.0 10.0 Woosung, Daejeon, South Korea) with the same size as Wheat flour 20.0 20.0 20.0 20.0 the experimental diets. Following the 1-week accli- Fish oil 6.0 ––– mation procedure, 25 fish with an initial mean body Linseed oil – 6.0 –– weight of 1.8 ± 0.03 g were randomly stocked into each Soybean oil –– 6.0 – 65-L polyvinyl circular tank supplied with filtered and dechlorinated tap water using a freshwater recirculating Lard –– – 6.0 (closed) system. Triplicate groups of fish were fed one Vitamin premix 1.5 1.5 1.5 1.5 3 of the formulated diets to apparent satiation twice a Mineral premix 1.8 1.8 1.8 1.8 day at 09:00 and 17:00 for 12 weeks. The uneaten feed Stay-C (50%) 0.3 0.3 0.3 0.3 was siphoned out, dried to constant weight, and then Vitamin E (25%) 0.2 0.2 0.2 0.2 weighed to estimate the amount of feed consumed. The Choline (50%) 0.2 0.2 0.2 0.2 mean water temperature during the experimental period Proximate composition was 24 ± 0.1 °C. The photoperiod was maintained on a (% DM) 12:12-h (light/dark) schedule. Fish were deprived of feed Dry matter 70.5 63.7 66.8 60.4 for 16 h prior to weighing or sampling to minimize hand- Crude protein 56.0 56.2 56.8 56.9 ling stress on fish. Crude lipid 13.0 13.2 13.2 13.3 Ash 11.0 11.0 11.0 11.2 Sample collection Fatty acids (% total fatty acids) At the end of the experiment, all the survived fish in 14:0 8.5 1.7 1.6 3.0 each tank were counted and weighed for calculation of growth performance, feed utilization parameters, and 16:0 21.2 11.2 15.1 22.7 survival rates. Total body length was measured for each 18:0 4.5 4.2 4.5 10.1 individual fish to the nearest 0.1 mm. A random sample 16:1n-7 8.3 0.9 0.8 2.2 of 5 fish per tank was collected and stored at − 43 °C for 18:1n-9 (OA) 8.3 14.3 20.7 32.8 subsequent whole body proximate composition analyses. 18:2n-6 (LA) 1.6 11.2 32.7 8.1 Blood samples were collected from the caudal veins of 18:3n-3 (ALA) 0.7 33.7 4.2 0.4 six anesthetized (200 mg/L MS-222, Sigma, St. Louis, 20:4n-6 0.8 0.7 0.7 0.7 MO, USA) individual fish per tank (nine fish/dietary 20:5n-3 (EPA) 14.5 3.7 3.6 3.6 treatment) using heparinized syringes. Blood samples were kept on ice prior to plasma separation by centri- 22:5n-3 11.4 0.6 0.6 0.6 fugation at 7500 RPM for 10 min using a high-speed 22:6n-3 (DHA) 16.6 12.4 12.1 12.3 refrigerated microcentrifuge (HanilBioMed Inc., Gwangju, FO fish oil, LO linseed oil, SO soybean oil Pesquera Bahia Caldera, Caldera, Chile; with crude protein 69.1%, crude South Korea). Plasma samples were immediately stored at lipid 12.6%, ash 14.1% dry matter − 80 °C until used in subsequent hematological analyses Vitamin premix contained the following amounts which were diluted in including total protein (TP), total cholesterol (TCHO), cellulose (g/kg premix): DL-α-tocopheryl acetate, 18.8; thiamin hydrochloride, 2.7; riboflavin, 9.1; pyridoxine hydrochloride, 1.8; niacin, aspartate aminotransferase (AST), alanine aminotrans- 36.4; Ca-D-pantothenate, 12.7; myo-inositol, 181.8; D-biotin, 0.27; folic ferase (ALT), alkaline phosphatase (ALP), albumin acid, 0.68; p-aminobenzoic acid, 18.2; menadione, 1.8; retinyl acetate, 0.73; cholecalciferol, 0.003; cyanocobalamin, 0.003 (ALB), and total bilirubin (TBIL). Immediately after Mineral premix contained the following ingredients (g/kg premix): blood sampling, fish (6 fish/tank; 18 fish/dietary treat- MgSO ·7H O, 80.0; NaH PO ·2H O, 370.0; KCl, 130.0; ferric citrate, 40.0; 4 2 2 4 2 ment) were dissected to obtain their liver and visceral ZnSO ·7H O, 20.0; Ca-lactate, 356.5; CuCl, 0.2; AlCl ·6H O, 0.15; KI, 0.15; 4 2 3 2 Na Se O , 0.01; MnSO ·H O, 2.0; CoCl ·6H O, 1.0 2 2 3 4 2 2 2 weights for calculating the hepatosomatic (HSI) and Oleic acid viscerosomatic (VSI) indices, respectively. Fillet samples Linoleic acid α-Linolenic acid were subsequently dissected out of the same fish and Eicosapentaenoic acid stored at − 80 °C until proximate and fatty acid com- Decosahexaenoic acid position analyses. Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 4 of 9 Analytical methods Protein efficiency ratioðÞ PER ¼ Chemical composition analyses wet weight gain ðÞ g =total protein consumedðÞ g Chemical composition of the experimental diets, whole body, and fillet samples was determined according to the Condition factorðÞ CF;%¼ standard methods (AOAC 2005). Moisture content was fish body weight=ðÞ total length of fish ðÞ cm  100 estimated by oven drying at 105 °C for 6 h. Crude protein content was determined by an automated Kjeldahl system Hepatosomatic indexðÞ HSI;%¼ (Buchi, Flawil, Switzerland). Crude lipid was measured ðÞ liver weight ðÞ g =fish body weight 100 using a Soxhlet extractor (VELP Scientifica, Milano, Italy), and ash content by a Thermolyne™ combustion in a muffle Viscerosomatic indexðÞ VSI;%¼ furnace at 600 °C for 4 h. ðÞ viscera weight ðÞ g =fish body weight 100 Hematological analysis Data were analyzed as a completely random design Plasma samples were analyzed for TP, TCHO, AST, ALT, with the tank as the experimental unit, using one-way ALP, ALB, and TBIL concentrations using an automated ANOVA in SPSS program version 22.0 (SPSS Inc., blood analyzer (DRI-CHEM NX500i, FUJIFILM Corpo- Chicago, IL, USA). When ANOVA identified differences ration Tokyo, Japan). among groups, Tukey’s honest significant difference multiple range test was performed to detect statistically Fatty acid analyses significant differences between mean responses at a Total lipids in oil sources, experimental diets, and fillet significance level of P < 0.05. Data were checked for nor- samples were extracted following the Folch et al. (1957) mal distribution (Shapiro-Wilk’s test) and homogeneity method using a chloroform and methanol mixture (2:1 v/v). of variances (Levene’s test) and when necessary arcsine Extracted lipids were then submitted to acid-catalyzed transformed. Data were presented as mean ± standard transmethylation using BF -MeOH (Sigma, St. Louis, MO, error (SE.) of the triplicate groups. USA) to obtain fatty acid methyl esters (FAMEs). Then, FAMEs were analyzed using a PerkinElmer Clarus 600 gas Results chromatograph (Shelton, CT, USA) equipped with a The results of growth, feed utilization, and morphological flame-ionization detector and a SP-2560 capillary column parameters of mandarin fish juveniles are presented in (100 m × 0.25 mm i.d., 0.2-μm film thickness; Supelco, Bel- Table 3. The total replacement of dietary FO by different lefonte, PA, USA) using helium as the carrier gas and lipid sources showed no significant negative effect on temperature programmed operation from 140 to 240 °C in growth performance in terms of final body weight (10.3– increments of 5 °C/min. The temperature of both injector 11.6 g), WG (499–549%), and SGR (2.13–2.23%). Although and detector was adjusted at 240 °C. Fatty acids were identi- growth rates were not significantly affected, fish received fied by comparison with standard FAME mixtures (FAME FO and LO diets grew slightly better and were numerically 37 and PUFA 3; Supelco, Bellefonte, PA, USA) and data larger than those fed the other two diets. The DFI of fish analyzed using TotalChrom software (version 6.3.1; fed the SO diet was significantly higher than those of fish PerkinElmer Inc., Shelton, CT, USA). fed FO and LO diets. No remarkable differences on DPI, FE, and PER were observed among any of the treatments Formulae, calculations, and statistical analysis (P > 0.05). The survival rate was higher than 97%, and there was no significant difference among all experimental Weight gainðÞ WG;%¼ groups. Similarly, the total substitution of FO with LO, SO, ½ ðÞ final body weight−initial body weight =initial body weight 100 or lard had no significant effects on fish morphological parameters. Specific growth rateðÞ SGR;%=day¼ The results of whole body proximate composition are ½ ðÞ ln final body weight− ln initial body weight =days 100 presented in Table 4. No significant differences were ob- Daily feed intakeðÞ DFI;%¼ served in whole body composition in terms of moisture, ftotal dry feed consumedðÞ g =½ðinitial fish weight þ final fish weight crude protein, and ash contents among all experimental þdead fish weightÞ days=2g  100 groups. Total replacement of dietary FO with three dif- ferent oil sources resulted in increased fat levels in man- Daily protein intakeðÞ DPI;%¼ darin fish body. Fish fed the LO and SO diets had ftotal protein consumedðÞ g =½ðinitial fish weight significantly higher crude lipid level in the whole body þfinal fish weight þ dead fish weightÞ days=2g  100 than that of fish fed FO diet. Feed efficiencyðÞ FE;%¼ The results of hematological parameters are reported ðÞ wet weight gain ðÞ g =total dry feed consumedðÞ g 100 in Table 5. There was neither a considerable difference Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 5 of 9 Table 3 Growth performance, feed utilization efficiency, and Table 5 Hematological parameters of mandarin fish fed the morphological parameters of mandarin fish fed the four four experimental diets for 12 weeks experimental diets for 12 weeks Experimental diets Experimental diets FO LO SO Lard FO LO SO Lard TP 4.33 ± 0.17 4.17 ± 0.20 4.03 ± 0.32 4.80 ± 0.12 IBW 1.8 ± 0.02 1.8 ± 0.02 1.7 ± 0.01 1.8 ± 0.02 2 TCHO 205 ± 8 190 ± 13 187 ± 13 219 ± 9 FBW 11.6 ± 0.3 10.9 ± 0.3 10.3 ± 0.03 10.7 ± 0.4 3 AST 174 ± 16 224 ± 61 172 ± 22 274 ± 11 WG 549 ± 20 524 ± 18 503 ± 1 499 ± 13 4 ALT 10.0 ± 0.6 10.0 ± 0.0 8.7 ± 0.3 11.0 ± 6.7 SGR 2.23 ± 0.04 2.18 ± 0.04 2.14 ± 0.00 2.13 ± 0.03 5 ALP 412 ± 30 342 ± 30 341 ± 40 489 ± 34 5 a a b ab DFI 2.54 ± 0.10 2.50 ± 0.06 2.81 ± 0.02 2.72 ± 0.04 6 ALB 0.77 ± 0.03 0.67 ± 0.03 0.70 ± 0.06 0.83 ± 0.03 DPI 1.44 ± 0.06 1.42 ± 0.03 1.57 ± 0.01 1.53 ± 0.02 7 TBIL 0.53 ± 0.09 0.60 ± 0.12 0.77 ± 0.09 0.73 ± 0.17 FE 69.1 ± 3.2 69.1 ± 2.3 61.4 ± 0.8 62.5 ± 1.2 Values are mean of triplicate groups and presented as mean ± SE. Values with 8 different superscripts in the same row are significantly different (P < 0.05). The PER 1.44 ± 0.06 1.45 ± 0.04 1.31 ± 0.01 1.34 ± 0.02 lack of superscript letter indicates no significant differences among treatments Survival (%) 98.7 ± 1.33 97.3 ± 1.33 98.7 ± 1.33 98.7 ± 1.33 FO fish oil, LO linseed oil, SO soybean oil Total protein (g/dL) CF 1.14 ± 0.11 1.41 ± 0.06 1.17 ± 0.02 1.14 ± 0.11 2 Total cholesterol (mg/dL) 10 Asparatet aminotransferase activity (U/L) HSI 2.06 ± 0.10 3.04 ± 0.57 2.47 ± 0.28 2.24 ± 0.09 Alanine aminotransferase activity (U/L) 11 5 VSI 9.93 ± 0.73 10.42 ± 0.50 9.65 ± 0.74 8.95 ± 0.30 Alkaline phosphatase (U/L) Albumin (g/dL) Values are mean of triplicate groups and presented as mean ± SE. Values with Total bilirubin (mg/dL) different superscripts in the same row are significantly different (P < 0.05). The lack of superscript letter indicates no significant differences among treatments altered fillet fatty acid profile. Regarding saturated fatty FO fish oil, LO linseed oil, SO soybean oil Initial mean body weight (g) acids (SFAs), the highest content of myristic acid (14:0) Final mean body weight (g) 3 was noted in fish fed the FO diet, which differed signifi- Weight gain (%) = [(final bodyweight – initial bodyweight)/initial body weight] × 100 cantly from the other three dietary treatments. Fillets of Specific growth rate (%/day) = [( ln final fish fed diets containing lard in place of FO had signifi- bodyweight – ln initial bodyweight]/days] × 100 cantly higher levels of palmitic acid (16:0) than do fillets Daily feed intake (%) = {total dry feed consumed (g)/[(initial fish weight + final fishweight + dead fishweight) × days/2]} × 100 Daily protein intake (%) = {total of fish fed the other experimental diets. While no statis- protein consumed (g)/[(initial fishweight + final tically significant differences were found among LO, SO, fishweight + dead fishweight) × days/2]} × 100 Feed efficiency (%) = (wet weight gain (g)/total dry feed consumed (g)) × 100 and lard groups, the stearic acid (18:0) content of fillet Protein efficiency ratio = wet weight gain (g)/total protein consumed (g) in lard group was significantly higher than that of 9 3 Condition factor (%) = [fish body weight/(total length of fish) (cm) ] × 100 FO-fed fish. With respect to monounsaturated fatty Hepatosomatic index (%) = (liver weight (g)/fish body weight) × 100 Viscerosomatic index (%) = (viscera weight (g)/fish body weight) × 100 acids (MUFAs), fillets of fish fed FO and lard diets con- tained significantly higher palmitoleic acid (16:1n-7) nor any discernible trend among dietary groups regard- compared to fish fed on LO and SO diets. A significantly ing plasma hematological parameters. greater level of OA was found in the fillet of fish fed lard Results on fillet proximate composition and fatty acid diet compared to the other dietary groups. By evaluation profile are given in Table 6. No significant effect nor any of n-6 fatty acid levels in the fish fillet, the highest con- defined trend was found in fillet proximate composition centration of LA was found in fish fed on diets contain- among dietary treatments. However, the addition of ing SO. Alternative oil treatments had no significant vegetable oil or animal fat in fish diet significantly impact on fillet arachidonic acid (AA, 20:4n-6) content. With respect to the fillet n-3 fatty acid composition, fish fed the LO diet had significantly higher levels of ALA Table 4 Whole body proximate composition of mandarin fish fed the four experimental diets for 12 weeks (% wet weight) than that of fish fed the FO-based diet, which was itself significantly higher than those found in the SO and lard Experimental diets groups. Fillets of fish fed diets containing FO had signifi- FO LO SO Lard cantly higher concentrations of EPA than those fed diets Moisture 79.1 ± 1.5 77.0 ± 0.6 76.7 ± 1.7 77.8 ± 1.52 containing the other three oil sources. The 22:5n-3 con- Crude protein 11.3 ± 0.6 11.8 ± 0.5 13.4 ± 0.9 12.4 ± 1.8 tent of fillet in FO fish was significantly higher than that a b b ab Crude lipid 3.85 ± 0.17 5.95 ± 0.34 5.80 ± 0.12 4.84 ± 0.67 of lard diet-fed fish, while no significant differences in Ash 3.34 ± 0.12 3.36 ± 0.21 3.55 ± 0.48 3.51 ± 0.24 fillet 22:5n-3 among LO, SO, and lard diet-fed fish were Values are mean of triplicate groups and presented as mean ± SE. Values with observed. The DHA contents of the fish fillets were different superscripts in the same row are significantly different (P < 0.05). The numerically lower in the LO, SO, and lard groups lack of superscript letter indicates no significant differences among treatments FO fish oil, LO linseed oil, SO soybean oil compared to fish fed the FO diet. Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 6 of 9 Table 6 Fillet proximate and fatty acid composition of mandarin fish fed the four experimental diets for 12 weeks Experimental diets FO LO SO Lard Proximate composition (% wet weight) Moisture 77.9 ± 0.8 79.1 ± 0.4 78.7 ± 1.2 77.6 ± 0.4 Crude protein 18.1 ± 0.5 18.1 ± 0.8 17.6 ± 0.9 18.8 ± 0.6 Crude lipid 1.44 ± 0.36 1.70 ± 0.27 1.36 ± 0.17 1.32 ± 0.24 Ash 1.37 ± 0.16 1.03 ± 0.11 1.14 ± 0.09 1.46 ± 0.02 Fatty acid (% total fatty acid) b a a a 14:0 2.54 ± 0.17 1.84 ± 0.12 1.45 ± 0.02 1.68 ± 0.03 a a a b 16:0 21.8 ± 0.5 20.8 ± 0.1 20.8 ± 0.2 23.4 ± 0.7 a ab ab b 18:0 5.30 ± 0.12 5.91 ± 0.14 6.01 ± 0.28 6.64 ± 0.25 b a a b 16:1n-7 5.61 ± 0.58 2.42 ± 0.18 2.49 ± 0.37 4.94 ± 0.12 1 a a a b 18:1n-9 (OA) 21.5 ± 1.7 21.2 ± 0.7 20.3 ± 0.1 27.98 ± 1.2 2 a b c ab 18:2n-6 (LA) 4.90 ± 0.31 7.38 ± 0.20 15.86 ± 0.45 6.29 ± 0.39 3 b c a a 18:3n-3 (ALA) 4.90 ± 0.28 10.47 ± 0.48 2.78 ± 0.31 1.67 ± 0.02 20:4n-6 1.92 ± 0.32 1.09 ± 0.04 1.09 ± 0.02 1.42 ± 0.04 4 b a a a 20:5n-3 (EPA) 6.20 ± 0.31 4.96 ± 0.05 4.49 ± 0.13 4.59 ± 0.38 b ab ab a 22:5n-3 1.56 ± 0.15 1.42 ± 0.05 1.30 ± 0.03 1.04 ± 0.13 22:6n-3 (DHA) 18.2 ± 1.8 16.4 ± 1.0 15.7 ± 0.2 14.0 ± 1.9 Values are mean of triplicate groups and presented as mean ± SE. Values with different superscripts in the same row are significantly different (P < 0.05). The lack of superscript letter indicates no significant differences among treatments FO fish oil, LO linseed oil, SO soybean oil Oleic acid Linoleic acid α-Linolenic acid Eicosapentaenoic acid Decosahexaenoic acid Discussion diets. Similarly, Du et al. (2008) found markedly higher The growth rate values observed in the present study were feed intake in grass carp, Ctenopharyngodon idella,fnger- much higher than those previously reported for the same lings fed lard or a blend of vegetable oils in comparison species by our research team using practical diets with with a FO-based diet. A large body of literature provides relatively similar protein and lipid contents (Sankian et al. strong evidence to suggest that fish are able to regulate 2017, 2018). This is probably due to the higher initial feed intake in order to meet their metabolizable energy weight of the fish in the previous studies (8–20 vs. 1.8 g in demands (De la Higuera 2001). Within the context of FO the present study). To our knowledge, so far, there is no replacement in aquafeed, if FO is replaced with an equal previous record on the effects of different dietary lipid amount of alternative oil source, minimal differences in source on growth, feed utilization, hematological indices, the total dietary energy content are expected. However, and body/fillet nutritional traits of mandarin fish. The since different oils may have different digestibility, it is findings of the present study showed that FO in a practical possible that the total digestible/metabolizable energy of diet with 13% lipid for juvenile mandarin fish can be com- feed can be partially changed, resulting in variations in pletely replaced by LO, SO, or lard without markedly feed intake. This may partly explain the DFI differences compromising growth performance and feed efficiency. observed in the present study. Our results are in agreement with the previous studies in The replacement of the dietary FO by three different which it was demonstrated that various alternative oils oils, in the present study, did not affect the morpho- could be used to completely replace FO in freshwater fish logical indices of fish, which is often used to indicate the diets without any adverse effect on the nutrient utilization nutritional status of fish. This was in agreement with or growth rates (Turchini et al. 2011a; Kowalska et al. previous studies in other freshwater species, which re- 2012; Jiang et al. 2013; Han et al. 2013; Zhou et al. 2016). ported that the replacement of dietary FO with vegetable However, the DFI value in fish fed with SO diet was oils and rendered animal fat did not affect the morpho- significantly higher than those of fish fed the FO and LO logical parameters of snakehead, Murray cod, rainbow Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 7 of 9 trout, darkbarbel catfish, Nile tilapia, and gibel carp were still higher than their respective levels in diets. This (Figueiredo-Silva et al. 2005; Turchini et al. 2011a; could be due either to selective retention and/or active Aliyu-Paiko and Hashim 2012; Jiang et al. 2013; Peng et synthesis of these fatty acids (Turchini et al. 2011b). al. 2015; Zhou et al. 2016). Similar results were observed in other freshwater fish In the present study, the whole body lipid content of species such as rainbow trout (Caballero et al. 2002; mandarin fish fed the LO and SO diets were significantly Turchini and Francis 2009), Murray cod (Turchini et al. higher than that of fish fed the FO diet. In accordance 2006), common carp (Ren et al. 2012), tilapia (Al-Souti with the present study, significantly high fat was re- et al. 2012, Li et al. 2016), Chinese long snout catfish, corded by Aliyu-Paiko and Hashim (2012) in whole body Leiocassis longirostris Günther (Choi and Lee 2015), and proximate composition of snakehead fingerlings, fed silver barb, Puntius gonionotus (Nayak et al. 2017). It is palm oil as a FO replacer. Similarly, in hybrid tilapia, widely believed that freshwater fish can convert C Oreochromis niloticus × O. aureus, fed tea see oil for PUFA of both n-6 and n-3 series to their corresponding 10 weeks, significantly higher body lipid levels were LC-PUFA via a series of desaturation and elongation re- obtained compared to fish fed FO (Han et al. 2013). It actions (NRC 2011; Turchini et al. 2011b). However, the has been suggested that diets enriched in n-3 LC-PUFA capacity of C PUFAs desaturation/elongation to n-3 may suppress fatty acids synthesis, simulate fatty acid LC-PUFAs is depended on the species (Sargent et al. β-oxidation, activate lipoprotein lipase, and reduce tri- 2002). Therefore, the decreased deposition of dietary acylglycerol synthesis, thereby leading to an overall ALA, LA, and OA along with good growth, feed reduction in lipid deposition and suppressing the de- utilization, and survival in this study is suggestive of the velopment of obesity in mammals (Al-Hasani and ability of mandarin fish to meet their essential fatty acid Joost 2005;Madsenet al. 2005). Indeed, Todorčević requirement by the use of C PUFA. It could also be et al. (2009) reported that feeding FO to Atlantic salmon, assumed that residual fish oil from dietary FM was prob- Salmo salar, for 21 weeks reduced white adipose tissue fat ably adequate to provide essential fatty acids for normal content and increased fatty acid β-oxidation activity growth and development of juvenile mandarin fish. The compared to fish fed rapeseed oil. results of this experiment presented a higher retention Hematological parameters are important indicators of of DHA in fish fed vegetable oil-based or lard diets. fish’s physiological and health status (Maita 2007). Previous studies in which fish were fed vegetable Hematological responses of juvenile mandarin fish were oil-based diets reported high DHA retention in the unaffected by the complete substitution of FO in this muscles of salmonids (Bell et al. 2001, 2003; Caballero study. There are conflicting reports concerning the et al. 2002;Thanuthong etal. 2011). The preferred effects of FO substitution by other oil sources on retention of DHA over EPA may also indicate a se- hematological indices, with some studies suggesting lective utilization of EPA over DHA when dietary marked modifications (Ferreira et al. 2011; Peng et al. levels decrease, as a means of meeting the require- 2015; Mozanzadeh et al. 2016), while others show no ments for tissue membrane integrity and function discernible effects (Figueiredo-Silva et al. 2005; Twibell (Fountoulaki et al. 2009). et al. 2012). This discrepancy can be attributed to va- rious factors including fish species, life stage, compo- Conclusion sition and nutrient content of the diet, source or quality This study indicates that total FO replacement with LO, of the alternative oil source, and experimental condi- SO, or lard can be tolerated by juvenile mandarin fish tions, mainly water temperature. However, since dietary without any pronounced adverse effects on fish perfor- FO replacement with alternative oils caused no detec- mance and health. The abundance of C PUFAs pro- table change either in morphological indices or in vided by tested alternative oil sources coupled with hematological parameters of juvenile mandarin fish in some n-3 LC-PUFA from the residual lipid of FM in the the present study, it can be concluded that fish were in basal diet appeared to meet the essential fatty acid re- overall good health and nutritional status. quirements of ~ 1.8 g mandarin fish under the condi- The fatty acid composition of mandarin fish fillets tions of the present study. This probably stemmed from closely resembled those of the experimental diets, with the ability of this species to bioconvert C PUFA to fish fed the LO, SO, and lard having remarkably elevated their corresponding LC-PUFA and selectively retain EPA levels of ALA, LA, and OA, respectively. It is well docu- and DHA to some extent. Our findings therefore suggest mented that the fatty acid profile of farmed-fish fillets that mandarin fish juveniles have high tolerance to diets reflects the fatty acid composition of the dietary oil used that differ markedly in fatty acid composition. (Bell et al. 1994). Although replacement of FO with Abbreviations alternative oils resulted in reduced levels of EPA and AA: Arachidonic acid; ALA: α-Linolenic acid; ALB: Albumin; ALP: Alkaline DHA, the levels of these fatty acids in the fish fillets phosphatase; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; Sankian et al. Fisheries and Aquatic Sciences (2019) 22:8 Page 8 of 9 CF: Condition factor; DFI: Daily feed intake; DHA: Docosahexaenoic acid; Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR. Replacement of fish DPI: Daily protein intake; EPA: Eicosapentaenoic acid; FE: Feed efficiency; oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid FM: Fish meal; FO: Fish oil; HIS: Hepatosomatic index; LA: Linoleic acid; LC- composition and hepatocyte fatty acid metabolism. J Nutr. 2001;131:1535–43. PUFA: Long-chain polyunsaturated fatty acid; LO: Linseed oil; OA: Oleic acid; Bell JG, McGhee F, Campbell PJ, Sargent JR. Rapeseed oil as an alternative to PER: Protein efficiency ratio; SGR: Specific growth rate; SO: Soybean oil; marine fish oil in diets of post-smolt Atlantic salmon (Salmo salar): changes TCHO: Total cholesterol; TP: Total protein; VSI: Viscerosomatic index; in flesh fatty acid composition and effectiveness of subsequent fish oil “wash WG: Weight gain out”. Aquaculture. 2003;218:515–28. Bell JG, Tocher DR, MacDonald FM, Sargent JR. 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