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Apparent digestibility coefficients (ADCs) of dry matter, crude protein, crude lipid, energy, essential amino acids, and fatty acids in extruded pellets containing various fish meals were determined for olive flounder (Paralichthys olivaceus). Eight extruded pellet diets were prepared to contain different fish meals (herring fish meal, anchovy fish meal, mackerel fish meal, sardine fish meal-A, sardine fish meal-B, tuna fish meal, pollock fish meal-A, and pollock fish meal-B) designated as HM, AM, MM, SM-A, SM-B, TM, PM-A, and PM-B, respectively. Chromic oxide (Cr O ) was used as an inert indicator at a concentration of 0.5 % in the diet. 2 3 Feces were collected from triplicate groups of fish (151 ± 4.0 g) using a fecal collection column attached to the fish rearing tank for 4 weeks. Dry matter ADCs of the MM, SM-A, SM-B, and PM-A diets were higher than those of all the other dietary groups, and the lowest digestibility of dry matter was observed in the PM-B diet. Fish fed the MM, SM-A, and PM-A diets showed significantly higher ADC of protein than those fed the AM, SM-B, TM, and PM-B diets. Lipid ADC of PM-B was significantly lower than that of the other diets. Energy ADCs of fish fed the MM, SM-A, and PM-A diets were significantly higher than those of the other diets. The availability of essential amino acids in the MM, SM-A, and PM-A diets were generally higher than that of the other fish meal diets, while TM showed the lowest values among all the experimental diets. ADCs of fatty acids in the AM, MM, SM-A, and PM-A diets were generally higher than those of fatty acids in the other diets, and the lowest values were recorded for the PM-B diet. These results provide information on the bioavailability of nutrients and energy in various fish meals which can be used to properly formulate practical extruded feeds for olive flounder. Keywords: Paralichthys olivaceus, Apparent digestibility coefficient, Fish meals Background some other substances (Hardy 2010). Fish meal is the pre- Determination of the digestibility of nutrients in diets pro- ferred animal protein supplement in the diets of aquatic vides the first indication of their nutritional value and is animals. It carries huge quantities of energy and is rich in considered as the first step of their quality evaluation protein, lipids, minerals, and vitamins. It also serves as the (Allan et al. 2000; Glencross et al. 2007; Luo et al. 2009; benchmark ingredient in aquaculture diets because of its Liu et al. 2009). Fish meal is certainly the best dietary pro- high nutrient content and digestibility (Udo et al. 2012). tein source because it is quite palatable and provides an ex- Fish meal in animal diets increases feed consumption, feed cellent balance of essential amino acids and fatty acids and efficiency, and growth through better feed palatability and also improves nutrient uptake, digestion, and absorption * Correspondence: email@example.com among other ingredients (Yisa et al. 2013). Some studies Department of Marine Biotechnology, Gangneung-Wonju National have investigated apparent digestibility coefficients of vari- University, Gangneung 25457, South Korea ous fish meals in several fish species such as grower Full list of author information is available at the end of the article © 2016 The Author(s). 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. Rahman et al. Fisheries and Aquatic Sciences (2016) 19:27 Page 2 of 8 rockfish, Sebastes schlegeli (Lee 2002); juvenile snakehead, respectively) (Table 3). Chromic oxide (Cr O ) served as 2 3 Ophiocephalus argus (Yu et al. 2013); juvenile cobia, the inert indicator at a concentration of 0.5 % in the diet. Rachycentron canadum (Zhou et al. 2004); Nile tilapia, All dry ingredients were thoroughly mixed, and the ex- Oreochromis niloticus (Köprücü and Özdemir 2005); perimental diets were manufactured using a twin-screw Atlantic cod, Gadus morhua (Tibbetts et al. 2006); and extruder (Model ATX-2, Fesco Precision Co., Daegu, juvenile haddock, Melanogrammus aeglefinus L. (Tibbetts Korea). Extrusion conditions were as follows: feeder speed, et al. 2004). The raw materials of fish meal are processed 16 to 18 rpm; conditioner temperature, 75 °C; main screw by heating, pressing, separation, evaporation, and drying. speed, 640 rpm; and barrel temperature, 100 to 115 °C. Heating condenses the protein, breaks the fat depots, and Extruder pellets were oven-dried at 60 °C for 6 h to main- also releases oil and water. Pressing improves the meal tain the moderate moisture content of 5 to 8 % and stored quality and decreases the moisture content of the press at −25 °C until use. cake as much as possible. Drying process removes suffi- cient water from the wet and unstable mixture of press cake to form a stable fish meal. Fish and experimental condition Extrusion process can cause physical and chemical Juvenile olive flounder were obtained from a hatchery changes, such as ingredient particle size reduction and (Namhae, Korea) and acclimated to the laboratory inactivation of enzymes. In addition, the heat associated conditions for 10 months. The experimental fish (151 ± with the extrusion process may also cause deactivation of 4.0 g) were then randomly distributed into 400-l cylin- anti-nutritional factors (Allan and Booth 2004) and drical fiberglass tanks filled with 200 l of water at a improve the utilization of nitrogen-free extracts or other density of 25 fish per tank. Filtered seawater was elements (Burel et al. 2000). Extrusion may also confer supplied at a flow rate of 3 l/min to each rearing tank. important benefits to the physical attributes of pellets Fish rearing tanks had a sloping bottom leading to a including nutrient digestibility, palatability, pellet durabil- centrally located drainage slot, and the effluent water ity, water stability, and pellet storage life (Barrows and was first directed over a fecal collection column before Hardy 2000). Extruded pellets are highly recommended going to waste (Lee 2002). The water temperature was for fish culture because of easy observation of feeding ac- tivity, easy management, and minimal water pollution. Table 1 Proximate and amino acid compositions of the fish Cho et al. (2006) reported that extruded pellets can im- meals used to test diets prove the digestibility of ingredients and they are generally Fish meals well accepted by olive flounder, Paralichthys olivaceus. HM AM MM SM-A SM-B TM PM-A PM-B Olive flounder is a commercially important carnivor- Proximate analysis ous fish widely cultured in Eastern Asia including Korea, (% in dry matter) Japan, and China (Kim et al. 2014). Previous studies Dry matter 93.3 92.2 92.4 91.3 94.0 92.0 93.7 93.1 were conducted to investigate apparent digestibility coef- Crude protein 73.4 67.3 76.6 71.5 71.0 62.7 74.7 63.3 ficients of various fish meals for flounder (Deng et al. 2010; Kim et al. 2010). However, only limited informa- Crude lipid 10.4 8.6 6.8 10.0 10.2 10.6 5.9 5.4 tion is available on the digestibility of different fish meals Ash 16.6 19.7 16.7 16.0 14.6 20.1 15.7 26.4 in flounder-extruded pellets. Therefore, the present Gross energy 4.9 4.5 4.6 4.7 4.8 4.3 4.7 3.9 study was conducted to determine the apparent digest- (kcal/g) ibility coefficients of dry matter, crude protein, crude Essential amino acids lipid, energy, essential amino acids, and selected fatty (% in protein) acids from different fish meals used in extruded diets for Arg 6.4 6.0 6.5 7.1 6.4 6.4 7.1 7.0 olive flounder. His 2.8 2.0 4.5 2.5 3.0 3.3 2.5 2.5 Ile 4.4 4.0 4.5 4.1 4.7 4.2 3.9 4.2 Methods Leu 8.0 6.6 7.9 7.8 8.3 7.6 8.0 8.0 Diet preparation Lys 8.4 7.2 8.6 5.8 8.9 9.3 5.7 5.3 The proximate, essential amino acid and fatty acid (% of total fatty acids) compositions of the test ingredients (fish Met + Cys 4.2 3.9 4.3 2.7 4.3 4.0 2.8 2.9 meals) are shown in Tables 1 and 2, respectively. Eight ex- Phe + Tyr 7.6 6.3 7.5 8.0 8.0 7.2 8.3 8.3 perimental diets were formulated using steam-dried her- Thr 4.8 4.8 4.7 4.2 4.9 4.8 4.9 4.3 ring fish meal, anchovy fish meal, mackerel fish meal, Val 5.9 4.9 5.0 4.4 5.3 5.6 4.3 4.7 sardine fish meal-A, sardine fish meal-B, tuna fish meal, HM herring fish meal, AM anchovy fish meal, MM mackerel fish meal, SM-A pollock fish meal-A, and pollock fish meal-B (designated sardine fish meal-A, SM-B sardine fish meal-B, TM tuna meal, PM-A pollock fish as HM, AM, MM, SM-A, SM-B, TM, PM-A, and PM-B, meal-A, PM-B pollock fish meal-B Rahman et al. Fisheries and Aquatic Sciences (2016) 19:27 Page 3 of 8 Table 2 Fatty acid compositions (% of fatty acids) of the fish meals Table 3 Formulation and chemical composition of the experimental diets Fish meals Diets HM AM MM SM-A SM-B TM PM-A PM-B HM AM MM SM-A SM-B TM PM-A PM-B C14:0 4.6 4.2 3.6 4.7 5.4 3.8 2.2 3.3 Ingredients (%) C14:1 0.4 0.3 0.6 0.6 0.5 1.0 0.4 Herring fish meal 72 C16:0 21.0 21.8 19.7 21.0 22.8 26.1 17.9 23.4 Anchovy fish meal 72 C16:1 3.5 5.6 3.6 5.1 6.0 4.7 3.8 5.7 Mackerel fish meal 72 C18:0 4.5 5.9 7.9 6.9 6.0 8.1 4.8 6.6 Sardine fish 72 C18:1n-9 10.8 15.1 12.9 13.9 9.6 17.1 16.9 27.2 meal-A C18:2n-6 2.1 2.2 2.4 1.5 3.3 2.1 1.7 3.1 Sardine fish 72 C20:0 0.3 0.4 1.8 0.8 2.6 0.5 1.5 0.3 meal-B C20:1n-9 3.3 1.7 0.9 1.0 0.8 1.2 3.5 3.3 Tuna meal 72 C18:3n-3 0.8 0.4 2.6 0.5 3.1 0.8 1.8 0.3 Pollock fish 72 meal-A C20:2n-6 2.6 2.0 1.4 1.5 1.4 1.2 1.3 0.6 Pollock fish 72 C22:1n-9 0.5 0.9 0.9 2.5 0.9 meal-B C20:3n-3 1.6 0.7 2.0 1.1 Wheat flour 14 14 14 14 14 14 14 14 C20:4n-6 1.2 0.8 1.6 1.8 1.6 2.5 1.7 0.8 α-potato-starch 5 5 5 5 5 5 5 5 C22:2n-6 0.6 0.6 0.6 1.5 0.8 Wheat gluten 2 2 2 2 2 2 2 2 C20:5n-3 12.4 16.4 9.4 11.1 13.0 6.2 14.1 7.9 Fish oil 3.7 3.7 3.7 3.7 3.7 3.7 3.7 3.7 C22:3n-3 0.4 0.7 0.6 0.5 0.3 Vitamin premix 1 111 1 11 1 C22:5n-3 1.3 3.2 2.5 2.5 1.4 1.2 1.6 0.9 Mineral premix 1 111 1 11 1 C22:6n-3 25.2 17.5 22.5 20.9 15.3 20.4 20.1 9.3 Stay-C (50 %) 0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.3 n-3HUFA 39.3 37.7 36.5 35.8 31.7 28.1 36.9 18.1 Vitamin E (25 %) 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.2 HM herring fish meal, AM anchovy fish meal, MM mackerel fish meal, SM-A Choline salt (50 %) 0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.3 sardine fish meal-A, SM-B sardine fish meal-B, TM tuna meal, PM-A pollock fish meal-A, PM-B pollock fish meal-B Cr O 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 2 3 Nutrient content 21.4 ± 2.10 °C, and the photoperiod followed the natural (dry matter basis) conditions during the experimental period. Crude protein (%) 53.4 51.7 54.9 52.9 51.8 47.6 54.0 47.5 Crude lipid (%) 9.3 8.5 7.8 9.6 8.6 9.7 8.0 7.5 Feces collection Ash (%) 12.6 16.0 13.1 13.4 12.8 16.4 12.3 20.2 Triplicate groups of fish were hand-fed with one of the NFE (%) 24.7 23.8 24.2 24.1 26.8 26.3 25.7 26.6 experimental diets to apparent satiation once a day at Vitamin premix contained the following ingredients (g/kg premix), which 15.00 h. Two hours after feeding, the rearing tanks and were diluted in cellulose: thiamin hydrochloride, 2.7; riboflavin, 9.1; pyridoxine collection column were brushed out in order to remove hydrochloride, 1.8; niacin, 36.4; Ca-D-pantothenate, 12.7; myo-inositol, 181.8; uneaten feed and fecal residues. The next day, feces were D-biotin, 0.27; folic acid, 0.68; p-aminobenzoic acid, 18.2; menadione, 1.8; retinyl acetate, 0.73; cholecalciferol, 0.003; and cyanocobalamin, 0.003 collected from the fecal collection columns at 9:00 h. Mineral premix contained the following ingredients (g/kg premix): Feces collected from the settling columns were immedi- MgSO ·7H O, 80.0; NaH PO ·2H O, 370.0; KCl, 130.0; ferric citrate, 40.0; 4 2 2 4 2 ZnSO ·7H O, 20.0; Ca-lactate, 356.5; CuCl, 0.2; AlCl ·6H O, 0.15; KI, 0.15; 4 2 3 2 ately filtered with filter paper (Whatman # 1) for 60 min Na Se O , 0.01; MnSO ·H O, 2.0; and CoCl ·6H O, 1.0 2 2 3 4 2 2 2 at 4 °C and stored at −75 °C for chemical analyses. Fecal c Calculated = 100 − (crude protein + crude lipid + ash) samples from each tank were pooled at the end of the experiment. using an automatic analyzer (Fibertec, Tecator, Sweden), while ash content was determined by treatment in a Analytical methods muffle furnace at 600 °C for 4 h. Gross energy content Freeze-dried feed and feces samples were finely was analyzed using an adiabatic bomb calorimeter (Parr, grounded using a grinder. Fish scales were removed USA). For amino acid composition, samples were freeze- from the feces samples using a 300-μm sieve before dried and then hydrolyzed with 6 N HCl at 110 °C for analysis. Crude protein content was determined by the 24 h. Amino acid concentrations in the experimental Kjeldahl method using an Auto Kjeldahl System (Buchi, diets and fecal samples were determined using an Flawil, Switzerland). Crude lipid was determined by the automatic analyzer (Hitachi Model 835-50, Japan) ether-extraction method. Crude fiber was determined equipped with an ion exchange column (Hitachi Resin # Rahman et al. Fisheries and Aquatic Sciences (2016) 19:27 Page 4 of 8 2619, 2.6 × 150 mm, Japan). Lipid for fatty acid analysis Table 4 Apparent digestibility coefficients (%) of dry matter, crude protein, crude lipid, and energy in olive flounder fed the was extracted by a combination of chloroform and diets containing various fish meals methanol (2:1, v/v) using the method of Folch et al. Diets Dry matter Crude protein Crude lipid Energy (1957). Fatty acid methyl esters were measured by trans- bc cd b c esterification with 14 % BF methanol (Sigma, St Louis, HM 81.5 ± 1.47 93.2 ± 0.31 90.5 ± 1.24 90.7 ± 0.65 bc bc cd c MO, USA). The particular fatty acid composition was AM 80.7 ± 1.71 91.6 ± 1.47 94.6 ± 0.71 90.3 ± 0.24 identified using a gas chromatography (PerkinElmer, cd d cd d MM 83.6 ± 0.74 95.3 ± 0.16 94.7 ± 0.91 93.5 ± 0.49 Clarus 600, GC, USA) that has a flame ionization cd d d d SM-A 84.4 ± 0.51 95.1 ± 0.18 95.9 ± 0.06 93.0 ± 0.07 detector, equipped with SPTM-2560 capillary column cd b bcd c SM-B 83.5 ± 0.06 90.8 ± 0.08 93.1 ± 0.46 89.3 ± 0.11 (100 m × 0.25 mm i.d., film thickness 0.20 mm; Supelco, b a bc b TM 77.5 ± 1.04 87.2 ± 0.70 92.4 ± 1.59 86.2 ± 0.40 Bellefonte, PA, USA). Injector and detector temperatures d d bcd d were 260 °C. The column temperature was programmed PM-A 87.0 ± 0.45 95.4 ± 0.20 93.6 ± 1.24 93.9 ± 0.39 a a a a from 140 to 240 °C at a rate of 5 °C/min. Helium was PM-B 69.2 ± 2.97 87.2 ± 1.29 83.0 ± 1.82 83.5 ± 0.98 utilized by the carrier gas. Fatty acid composition from Values (mean ± SE of triplicate groups) in the same column with different the samples was identified by comparison with retention superscripts are significantly different (P < 0.05) times of the known standard fatty acid methyl esters (PUFA 37 component FAME Mix Supelco). Chromic to 96 %. The lipid ADCs of the PM-B diet was signifi- oxide was determined by a wet-acid digestion method cantly lower than those of the other diets, and the SM-A (Furukawa and Tsukahara 1966). group showed the highest value. Energy ADCs ranged Apparent dry matter digestibility coefficients were from 84 to 94 %. The energy ADCs of the MM, SM-A, calculated as 100 − (100 × (% Cr O in diet/% Cr O and PM-A diets were significantly higher than those of 2 3 2 3 in feces)). the other groups while the PM-B diet showed the lowest Apparent digestibility coefficients of nutrients, energy, value. essential amino acids, and selected fatty acids were calcu- Essential amino acid ADCs of diets containing various lated as 100 − (100 × (% feed marker/% feces marker) × fish meals for olive flounder are shown in Table 5. In (% nutrient, energy, amino acid, or fatty acid in feces/ general, essential amino acid availability reflected crude % nutrient, energy, amino acid, or fatty acid in feed)). protein digestibility, with fish fed the MM, SM-A, and PM-A diets showing the highest values compared to the other experimental groups. Amino acid digestibility Statistical analysis values, for most essential amino acids, in TM were the All data were subjected to one-way analysis of variance, lowest for juvenile olive flounder among the fish meals followed by Duncan’s multiple range test (Duncan 1955) tested. Fatty acid ADCs of diets containing various fish at a significance level of P < 0.05. Linear correlations meals for olive flounder are shown in Table 6. Among were determined between nutrient digestibility and all fish meals, the ADC of selected fatty acids in PM-B contents of the test ingredients (fish meals). All data are was significantly lower than that of fatty acids in other presented as mean ± SE (standard error) of three repli- fish meals. cate groups. All statistical analyses were carried out using SPSS version 20.0 (SPSS Inc., Chicago, IL, USA). Discussion Dry matter ADC of various protein feedstuffs offers Results an estimate of overall digestibility, and a low value The apparent digestibility coefficients (ADCs) of dry generally indicates that a high level of indigestible matter, crude protein, crude lipid, and energy of the material is present in the feedstuff (Li et al. 2013). extruded floating pellet diets containing various fish Thus, dry matter ADCs have been considered to meals for olive flounder are shown in Table 4. The provide a better estimate of the amount of indigest- ADCs of dry matter ranged from 69 to 87 %. Dry matter ible material present in feedstuffs in comparison with ADCs of the MM, SM-A, SM-B, and PM-A diets were digestibility coefficients for individual nutrients (Luo higher than those of the TM and PM-B diets. The dry et al. 2008). In this study, the MM, SM-A, SM-B, and matter ADC of PM-B was the lowest among the experi- PM-A diets were equally well digested and had higher mental groups. dry matter ADCs than the TM and PM-B diets. These Protein ADCs of diets ranged from 87 to 95 %. Protein differences can be explained by the differences in ADCs of the MM, SM-A, and PM-A diets were signifi- origin, quality, and chemical composition of ingredi- cantly higher than those of the AM, SM-B, TM, and ents used in the diet. We found that the dry matter PM-B diets while the lowest values were observed in fish digestibility was positively correlated (r =0.95) with fed the TM and PM-B diets. Lipid ADCs ranged from 83 ash content of fish meals tested in the current study. Rahman et al. Fisheries and Aquatic Sciences (2016) 19:27 Page 5 of 8 Table 5 Apparent amino acid digestibility coefficients (%) of diets containing various fish meals for olive flounder Essential Diets amino HM AM MM SM-A SM-B TM PM-A PM-B acids cd bc f ef bc a de b Arg 94.3 ± 0.39 93.1 ± 1.46 98.1 ± 0.03 96.6 ± 0.19 92.9 ± 0.27 89.8 ± 0.65 96.1 ± 0.14 92.0 ± 0.39 bc a e de ab a cd a His 93.2 ± 0.41 90.8 ± 1.77 98.1 ± 0.13 96.1 ± 0.06 92.1 ± 0.15 90.3 ± 0.62 95.0 ± 0.28 89.8 ± 0.75 cd bc e de bc a de ab Ile 92.7 ± 0.60 90.5 ± 2.23 97.0 ± 0.13 94.9 ± 0.10 90.6 ± 0.28 87.6 ± 0.86 94.8 ± 0.32 89.0 ± 0.48 cd bc e de bc a de ab Leu 93.1 ± 0.48 91.3 ± 2.04 97.3 ± 0.11 95.3 ± 0.14 91.0 ± 0.21 88.0 ± 0.79 95.0 ± 0.19 89.3 ± 0.43 de cd f ef bc a ef ab Lys 84.5 ± 0.62 92.3 ± 2.08 97.8 ± 0.11 96.4 ± 0.04 91.3 ± 0.12 88.6 ± 0.93 95.3 ± 0.21 89.5 ± 0.50 d c e de c a de b Met + Cys 96.1 ± 0.26 94.5 ± 1.23 98.5 ± 0.02 97.3 ± 0.01 94.0 ± 0.11 88.5 ± 0.36 97.1 ± 0.09 91.1 ± 0.37 bc ab d d ab a cd a Phe + Tyr 92.2 ± 0.67 90.2 ± 1.89 96.9 ± 0.10 94.8 ± 0.21 90.2 ± 0.22 88.5 ± 0.71 94.6 ± 0.35 88.7 ± 0.42 b b c c b a c a Thr 92.0 ± 0.42 90.1 ± 1.83 96.7 ± 0.12 94.4 ± 0.24 90.1 ± 0.12 86.6 ± 0.66 94.7 ± 0.34 87.7 ± 0.48 c b e d bc a de ab Val 89.9 ± 0.36 86.5 ± 1.94 95.7 ± 0.16 92.7 ± 0.24 88.6 ± 0.20 83.9 ± 0.81 93.4 ± 0.76 86.3 ± 0.51 Values (mean ± SE of triplicate groups) in the same row with different superscripts are significantly different (P < 0.05) It has been suggested that a high level of ash generally 2008). The ADC of protein for the MM diet (95 %) is affects digestibility of dry matter and results in high higher than that reported for juvenile Pacific white waste outputs and can also cause mineral imbalances. shrimp, Litopenaeus vannamei (Lemos et al. 2009). The Therefore, the low dry matter digestibility of the TM ADC of protein for the HM diet (93 %) is similar to that and PM-B diets may be attributed to their high ash reported for herring fish meal in the Atlantic cod, G. content (20.1 and 26.4 %, respectively). Kitagima and morhua (Tibbetts et al. 2006), and salmonids such as the Fracalossi (2011) reported low dry matter digestibility Atlantic salmon, Salmo salar (Anderson et al. 1997); for fish and shrimp offal meal with high ash contents. coho salmon, O. kisutch (Sugiura et al. 1998); and Similar results have also been observed in rainbow rainbow trout (Burel et al. 2000). The ADC of protein trout (Oncorhynchus mykiss) (Bureau et al. 1999) and for the AM diet (91 %) is similar to that reported for hybrid tilapia (O. niloticus × Oreochromis aureus) anchovy fish meal in salmonid species (Anderson et al. (Zhou and Yue 2012). 1995; Sugiura et al. 1998, 2000; Thiessen et al. 2004; The protein quality of the dietary ingredients is usually Glencross et al. 2005). In the present study, the protein the leading factor affecting fish performance and protein ADCs of the TM and PM-B diets were lower than those digestibility and is the first measure of its availability for of the other ingredients tested. The ADC of protein fish (Yu et al. 2013). The ADC of protein in this study appeared to have a positive relationship with dry matter of revealed that the protein of HM, MM, SM-A, and PM-A the test ingredients (r = 0.84). The differences in ADC of must be highly digestible by olive flounder. This indi- protein among fish meals can be attributed to their differ- cates that each of these fish meals can be utilized effi- ent nutrient compositions, raw materials, species, ciently as protein sources for olive flounder. The ADC locations, seasons of catch, and processing conditions of protein for the SM-A diet (95 %) is higher than that used to produce the meal (Luo et al. 2008; Lemos et al. previously reported for rainbow trout (Gaylord et al. 2009; Terrazas-Fierro et al. 2010). Table 6 Apparent fatty acid digestibility coefficients (%) of diets containing various fish meals for olive flounder Fatty Diets acids HM AM MM SM-A SM-B TM PM-A PM-B b bc c c bc bc bc a C14:0 91.7 ± 0.12 94.9 ± 0.12 96.1 ± 0.16 97.0 ± 1.51 93.0 ± 0.47 92.9 ± 0.59 93.2 ± 0.47 80.6 ± 3.12 bc bc c c bc b c a C16:0 90.0 ± 0.13 92.2 ± 0.34 94.6 ± 0.17 93.1 ± 0.40 89.4 ± 0.71 87.4 ± 0.77 93.7 ± 0.26 69.7 ± 4.70 bcd de de e bc b cde a C18:0 86.8 ± 0.27 90.7 ± 0.66 91.9 ± 0.24 94.1 ± 0.37 84.3 ± 1.02 83.7 ± 0.82 89.4 ± 0.38 68.9 ± 4.69 b b b b b b b a C18:1n-9 92.5 ± 0.62 95.5 ± 0.17 95.8 ± 0.31 95.2 ± 0.25 93.8 ± 0.32 95.9 ± 2.16 95.2 ± 0.21 80.5 ± 2.53 b c c c bc bc bc a C18:2n-6 88.9 ± 0.74 96.6 ± 0.27 97.1 ± 0.29 96.9 ± 0.22 93.3 ± 0.75 95.5 ± 0.22 93.9 ± 0.24 72.1 ± 6.24 cd cd d cd bc b bcd a C18:3n-3 93.4 ± 0.11 96.5 ± 0.27 97.8 ± 0.80 96.4 ± 0.27 90.1 ± 0.40 85.8 ± 0.60 91.7 ± 0.44 61.3 ± 6.39 c c c bc bc bc b a C20:4n-6 95.7 ± 0.19 97.4 ± 0.18 97.1 ± 0.12 94.3 ± 0.43 92.7 ± 1.87 94.4 ± 0.63 89.9 ± 3.15 82.6 ± 2.59 b b b b b b b a C20:5n-3 97.2 ± 0.07 98.5 ± 0.08 98.7 ± 0.08 97.3 ± 0.48 97.5 ± 0.21 98.2 ± 0.34 97.9 ± 0.20 92.5 ± 1.52 b b b b b b b a C22:6n-3 96.7 ± 0.05 98.0 ± 0.14 98.0 ± 0.36 97.3 ± 0.20 96.8 ± 0.14 96.9 ± 0.57 97.4 ± 0.10 88.0 ± 1.89 Values (mean ± SE of triplicate groups) in the same row with different superscripts are significantly different (P < 0.05) Rahman et al. Fisheries and Aquatic Sciences (2016) 19:27 Page 6 of 8 The quality of dietary protein depends on its amino energy from animal products (Sullivan and Reigh 1995; acid composition and their digestibility and availability Gaylord and Gatlin 1996; McGoogan and Reigh 1996; (Rollin et al. 2003). Lack of an essential amino acid Lee 2002; Zhou et al. 2004). It was found that a high ash leads to poor dietary protein utilization and therefore content of fish meal might reduce energy digestibility reduces growth and deceases feed efficiency. Although (Gomes et al. 1995). the data presented in this study suggest a reasonable agreement between protein and amino acid digestibili- Conclusions ties, individual amino acid availabilities within a feed The MM, SM-A, and PM-A diets showed higher dry ingredient are variable. The amino acid availability matter, crude protein, crude lipid, and energy ADCs coefficients of the MM, SM-A, and PM-A diets were than the other diets. Due to variation within individual significantly higher than those of the other experi- amino acid and fatty acid ADCs among diets, the use of mental diets, suggesting that olive flounder can effi- specific amino acid and fatty acid ADCs may allow more ciently utilize these fish meals. In most of the cases, accurate and economical formulation of the feed for ADCs of essential amino acid in the TM diet were olive flounder. the lowest of all the fish meals that were tested, Abbreviations possibly due to lower quality of the starting raw ADCs, apparent digestibility coefficients; AM, anchovy fish meal; Arg, material. Many researchers have reported that some arginine; His, histidine; HM, herring fish meal; Ile, isoleucine; Leu, leucine; Lys, amino acids of fish meal are inefficiently utilized or lysine; Met + Cys, methionine + cysteine; MM, mackerel fish meal; Phe + Tyr, phenylalanine + tyrosine; PM-A, pollock fish meal-A; PM-B, pollock fish meal-B; made unavailable due to differences in the processing SE, standard error; SM-A, sardine fish meal-A; SM-B, sardine fish meal-B; Thr, conditions or the low quality of the raw material threonine; TM, tuna fish meal; Val, valine processed (Wilson et al. 1981; Anderson et al. 1992, Anderson et al. 1995; Yamamoto et al. 1998; Mu Acknowledgements This work was supported by a grant from the National Institute of Fisheries et al. 2000, Chu et al. 2015). Science (R2016016) in Korea. The ADC of dietary lipid usually ranges from 85 to 95 % in fish (NRC 1993). In the present study, lipid digestibilities Funding This study was funded by a grant from the National Institute of Fisheries were considered to be high (>90 %), except for PM-B Science (R2016016) in Korea. The funding organization played an active role (83 %). Previous studies reported ADC values of lipid in dif- in the manufacture of the experimental feed and analyses. ferent fish meals including Peruvian fish meal (94 %) for ju- venile snakehead, O. argus (Yu et al. 2013); white fish meal Availability of data and materials All datasets generated during and/or analyzed during the current study are (78 %); and brown fish meal (76 %) for loach, Misgurnus available from the corresponding author on reasonable request. anguillicaudatus (Chu et al. 2015). The digestibility of lipids is known to be influenced by a number of factors, including Authors’ contributions degree of unsaturation, dietary lipid level, and various other MMR conducted the feeding trial and drafted the manuscript. HSH, KWK, KDK, and BJL manufactured the experimental feed and performed the constituents (Yuan et al. 2010). analyses. SML conceived and designed the study and experimental facility Digestibility of fatty acids is identified to be influenced and also revised the manuscript. All authors read and approved the final by a number of factors including their chain length, manuscript. degree of unsaturation, level of incorporation in dietary Competing interests fat, and other constituent fatty acids and their melting The authors declare that they have no competing interests. points (Olsen et al. 2000; Martins et al. 2009; Oujifard et al. 2012). High specificity towards unsaturated fatty Consent for publication Not applicable acids has commonly been found for fish digestive lipases (Caballero et al. 2002). In the present study, all diets Ethics approval and consent to participate showed high fatty acid digestibility except for PM-B. The Experimental protocols followed the guidelines of the Animal Care and Use low digestibility coefficient of fatty acids for the PM-B Committee of Gangneung-Wonju National University. diet may be attributed to the poor quality of raw mater- Author details ial processed. However, digestibility of individual fatty Department of Marine Biotechnology, Gangneung-Wonju National acids has been affected by other factors including emul- University, Gangneung 25457, South Korea. Aquafeed Research Center, National Institute of Fisheries Science, Pohang 37517, South Korea. sification, enzymatic hydrolysis, and micellar incorpor- ation (Francis et al. 2007). Received: 4 March 2016 Accepted: 18 July 2016 The ADCs of energy for the HM and SM-A diets, in the current study, are in the same range as reported in References Atlantic cod (93 %) (Tibbetts et al. 2006) and rainbow Allan GL, Booth MA. Effects of extrusion processing on digestibility of peas, trout (95 %) (Gaylord et al. 2008). 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Fisheries and Aquatic Sciences – Springer Journals
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