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Effects of enzymatically hydrolyzed fish by-products in diet of juvenile rainbow trout (Oncorhynchus mykiss)

Effects of enzymatically hydrolyzed fish by-products in diet of juvenile rainbow trout... Five experimental diets were formulated to evaluate the effects of dietary enzymatically hydrolyzed tuna by-product on growth, non-specific immune responses, and hematology of juvenile rainbow trout (Oncorhynchus mykiss). A basal diet with 50% of fishmeal was used as control (CON) and four other diets replaced 12.5% (TBB ), 25% (TBB ), 37.5% 12.5 25 (TBB ), and 50% (TBB ) of fish meal in the CON diet. Juvenile rainbow trout (4.87 ± 0.05 g) were randomly distributed 37.5 50 into 15 tanks (50 L) and fed 3–4% of wet body weight two times a day. At the end of 7 weeks of feeding trial, weight gain, specific growth rate, feed efficiency, and protein efficiency ratio of fish fed CON diet were significantly higher than those of fish fed TB diet (P< 0.05). But there were no significant differences among fish fed CON, TBB ,TBB ,and 50 12.5 25 TBB diets (P> 0.05). There were no significant differences in GPT levels among fish fed CON, TBB ,TBB ,and 37.5 12.5 25 TBB diets. Also, there were no significant differences in lysozyme, superoxide dismutase, glucose, and total protein 37.5 levels in all experimental diet (P> 0.05). The broken-line analysis indicated that the minimum dietary level of enzymatically hydrolyzed tuna by-product to replace fishmeal could be 29.7% in rainbow trout. These results indicated that the optimum level of dietary enzymatically hydrolyzed tuna by-product could replace greater than 29.7% but less than 37.5% of fishmeal in juvenile rainbow trout diet. Keywords: Rainbow trout, Enzymatic hydrolysis, Growth performance, Immune response, Tuna by-products Background increase. According to a recent report, the global pro- Fish meal (FM) is the one of the most important ingredi- duction of fish meal has decreased by about 1.1 million ents used in aquafeed. FM is a high-quality source of tons compared to the production in 2000 (IFFO 2018). protein and is desirable for its rich essential amino acids Tremendous price increases for FM together with envir- profile (Cho and Kim 2011; Anderson et al. 2016) as well onmental concerns have forced the aquaculture industry as for its vitamin and mineral content (IFOMA 2000). to find alternative protein sources for aquafeed formula- Typically, FM (66% crude protein) is the preferred tion. As a result, at this moment, the replacement of FM source of protein in aquafeed formulation, yet the cost in aqua feeds is one of the most pressing issues facing of FM is continually increasing (Tomas et al. 2005; the industry. Conversely, alternative protein sources can Anderson et al. 2016;FAO 2018). It is to be noted that relieve this problem by lowering the cost of feed, redu- the world demand of FM increased by only about 27% cing the amount of dependence on wild fish, and poten- during the past two decades, while FM output by the tially reduces the nutrient levels in effluent waste (Van major FM-producing countries actually decreased. Be- Weerd et al. 1999; Papatryphon and Soares Jr. 2001; cause of the limited supply of FM coupled with its in- Masumoto et al. 2001). However, for most species, there is creasing demand, the cost of producing fish is likely to a limit on amount of FM that can be replaced by alterna- tive protein sources without causing negative effects on the health and physiology of the fish. Therefore, a new * Correspondence: scbai@pknu.ac.kr feed ingredient that is both cheaper and free from disease Department of Marine Bio-Materials and Aquaculture/Feeds and Foods is highly desirable. Therefore, fishery by-products could Nutrition Research Center (FFNRC), Pukyong National University, 599-1 Daeyeon 3-Dong, Busan 608-737, Republic of Korea be a possible solution. Uyan et al. (2006)reported that 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. Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 2 of 8 tuna muscle by-product powder is a promising feed ingre- growth and non-specific immune responses in juvenile dient to replace 50% FM protein without reduction in the rainbow trout. growth performance of olive flounder. Enzymatic hydrolysis is a process by which enzymes Materials and methods facilitate the cleavage of chemical bonds by water, play- Experimental design and diets ing a pivotal role in the digestion of food (Nielsang et al. A basal diet was formulated containing crude protein 2005). This process makes it possible to improve the nu- 50.22%, crude lipid 13.71%, ash 9.79%, and moisture tritive value of individual feed ingredients (PER, digest- 4.93%; without inclusion of enzymatically hydrolyzed ibility and FCR). Moreover, the moisture contents of the tuna backbone by-products, used as control diet (CON) ingredients remain almost the same, varying only by 2.5 and four other experimental diets were formulated using ± 4.4%, maintaining typical parameters for storage of in- enzymatically hydrolyzed tuna backbone by-products. gredients. Lastly, an important benefit of extrusion after TBB , TBB , TBB , and TBB diet were formulated enzymatic hydrolysis is the sterilization of the ingredi- 12.5 25 37.5 50 with hydrolyzed tuna by-products level of 12.5%, 25%, ents. Enzymatic hydrolyzed by-products are now 37.5%, and 50% replacement of FM respectively (Table 1). widely used to modify or improve protein quality and The ingredients were grounded into powder form using a their digestibility (Panyam and Kilara 1996; Liaset et grinding machine and sieved before inclusion of ingredi- al. 2000;Je etal. 2007; Baek and Cadwallader 1995; ents. The resultant mixtures become pelletized with a pel- Nielsang et al. 2005). Nevertheless, the presence of let machine with no heating using a module of 2-mm endogenous enzymes in by-products may induce auto diameter and air dried for 3 days. The dried feeds were hydrolysis. In the case of squid gut and muscle, high endogenous proteolytic activity has been reported (Sugiyama et al. 1989; Leblanc and Gill 1982;Rodger Table 1 Formulation and proximate composition of five et al. 1984) and during chopping, the tissues become experimental diets (% of dry matter basis) hydrolyzed, rendering it richer in free essential amino Ingredients Diets acids (Lian et al. 2005). Hydrolyzed fish by-products (% in diet) CON TBB TBB TBB TBB 12.5 25 37.5 50 from Alaskan fisheries have been evaluated for re- Fishmeal 50 43.75 37.50 31.25 25.00 placement of menhaden FM in Litopenaeus vannamei En. H.B 0.00 5.82 11.64 17.46 23.27 diets (Forster et al. 2011). Replacement of FM in aqua feeds with inexpensive protein sources, such as unex- Blood meal 2.90 2.90 2.90 2.90 2.90 ploited by-products which are regionally or locally Soybean meal 3.50 3.50 3.50 3.50 3.50 available, may be a great opportunity for sustainable Wheat gluten meal 7.9 7.9 7.9 7.9 7.9 resource utilization. Cornstarch 0.00 0.6 1.18 1.78 2.39 Rainbow trout, Oncorhynchus mykiss, is one of most Wheat flour 20.00 20.00 20.00 20.00 20.00 popular fish species around the world, due to its Soybean oil 7.80 7.80 7.80 7.80 7.80 excellent meat quality (Vehviläinen et al. 2008). It is also one of the most studied species and is widely used for Fish oil 3.37 3.02 2.68 2.33 1.98 research in many fields such as carcinogenesis, toxicology, Cellulose 0.53 0.71 0.90 1.08 1.26 immunology, ecology, physiology, and nutrition (Thor- Vitamin premix 2.00 2.00 2.0 2.00 2.00 gaard et al. 2002;Cowey 1992; Boyle et al. 2013;Berthelot Mineral premix 2.00 2.00 2.0 2.00 2.00 et al. 2014). Global rainbow trout production from aqua- Total 100 100 100 100 100 culture has grown tremendously and has reached Proximate analysis (% of DM) 814,090 metric tons as of 2016 (FAO 2018). For Repub- lic of Korea, rainbow trout is also one of the commer- Moisture 4.93 5.72 6.17 7.22 7.30 cially important freshwater species with 3358 metric Protein 50.22 48.71 48.34 47.95 46.81 tons of production in 2017; ranking third among fresh- Lipid 13.71 12.75 14.89 14.25 13.61 water species nationally (KOSTAT 2018). Numerous Ash 9.79 9.59 9.49 9.11 9.05 studies have been conducted on FM replacement in TBB12.5 tuna backbone by-products at 12.5% FM replacement (Samhae Company, rainbow trout (Hauptman et al. 2014). However, to our Gyeongiu, South Korea) knowledge, no study has been conducted using enzy- TBB25 tuna backbone by-products at 25% FM replacement (Samhae Company, Gyeongiu, South Korea) matically hydrolyzed tuna by-products for replacing FM TBB37.5 tuna backbone by-products at 37.5% FM replacement (Samhae Company, in the diet of juvenile rainbow trout. Based on the re- Gyeongiu, South Korea) TBB50 tuna backbone by-products at 50% FM replacement sultsobtainedinpreviousstudies,the aimof thisstudy CON control diet (the basal diet) is to partially replace FM with enzymatically hydrolyzed b En. H.B enzymatic hydrolyzed by-products (Samhae Company, Gyeongiu, tuna by-products in order to examine the effects on South Korea) Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 3 of 8 sieved and packaged in zip-lock bags, labeled and stored factor (CF). Blood samples were collected from the cau- at − 20 °C until the feeding trial. dal vein of the fish with 1 ml syringes. Serum samples obtained from blood on clotting by centrifugation at Experimental fish and feeding conditions 5000×g for 10 min and stored at − 70 °C for the analysis The feeding trial was conducted in the Department of of the activities of lysozyme and superoxide dismutase Marine Bio-Materials and Aquaculture and Feeds and (SOD). A turbid metric assay was used for the measure- Foods Nutrition Centre, Pukyong National University ment of lysozyme activity of blood serum using the (PKNU), Busan, Republic of Korea. Experimental rain- method by Hultmark (1980) with slightly modifications. −1 bow trout fry were collected from a local rainbow trout Micrococcus lysodeikticus (0.75 mg ml ) was suspended farm named Ihwajeong Fish Farm, Sangju city, Korea. in sodium phosphate buffer (0.1 M, pH 6.4), then 200 μl Before starting of the feeding trial, all fishes were fed of suspension was placed in each well of 96-well plates with the basal diet two times in a day to acclimatize and after that 20 μl of test serum was added. After incu- them to the laboratory experimental conditions for bation, the reduction in absorbance of the samples was 2 weeks. Feeding trial was done using an indoor recorded at 570 nm at room temperature for 0 and semi-recirculation system with 15 tanks of 50 L water 60 min in a micro plate reader (UVM 340, Biochrom, holding capacity receiving constant filtered freshwater Cambridge, UK). One unit of lysozyme activity was −1 −1. flow at a rate of 2 L min from the central tank. Half of regarded as a reduction in absorbance of 0.001 min the water was exchanged everyday by pumping filtered Activity of SOD was measured according to the per- fresh water to the central tank. Supplementary continu- centage of reaction inhibition rate of the enzyme with ous aeration facility provided to maintain required dis- WST-1 (water-soluble tetrazolium dye) substrate and solved oxygen (D.O) and by using water heaters, xanthine oxidase using an SOD Assay Kit (Enzo temperature always maintained at 14.0 ± 0.1 °C through- ADI-900-157, Enzo Life Sciences, Inc.) in accordance out the experimental period. Four hundred eighty fishes with manufacturer’s instructions. Each endpoint assay with an average weight of 4.87 ± 0.05 g (mean ± SD) were was monitored by absorbance at 450 nm (the absorbance weighed and distributed as 20 fish/tank randomly into wavelength for the colored product of WST-1 reaction the 15 experimental indoor tanks. Three tanks were ran- with superoxide) after 20 min of reaction time at 37 °C. domly selected for each one of the experimental diet. In The inhibition percentage was normalized by mg of pro- this way, 15 tanks are randomly assigned for 5 dietary tein and showed as SOD activity units. Serum portions treatments and marked the tanks. Feeding was done two were also used for the biochemical parameters analysis times daily (09:00 A.M. and 05:00 P.M.). Feed amount of total protein (TP) of plasma, glutamic oxaloacetic adjusted ranged from 3 to 4% according to the wet body transaminase (GOT), glutamic pyruvic transaminase weight in the beginning and at the end of feeding trial (GPT), and glucose activities determined using the com- respectively for 7 weeks. Two hours after feeding, all mercial clinical kits of Fuji DRI-CHEM 3500i, Fuji Photo tanks were siphoned to remove fecal matter and uneaten Film Ltd., Tokyo, Japan. feeds daily. Mortality would check daily, dead fish imme- From each tank, three fish were collected and pooled diately removed and weighed, and required feed together according to the fish fed with different experi- amounts for the tanks adjusted according to the mental diets; homogenized and freeze-dried at − 80 °C remaining body weight of fish in the tanks. Dead fish for analysis. Proximate compositions of the experimental was not replaced during the experiment. Total weight of fish and the basal diet were determined according to fish in each tank was determined at 4th week for adjust standard procedures of AOAC (2005) in duplicates. Both the amount of diet for feeding. Before each checking, samples were dried at 105 °C to a constant weight to de- fish were starved for 24 h to avoid inclusion of ingested termine moisture content. Determination of ash content feed in the measurements of fish body weight as well as was done by incineration in a muffle furnace at 550 °C to minimize stress. for 3.5 h, crude lipid was determined by the Soxhlet ex- traction using Soxtec system 1046 (Tecator AB, Foss, Sample collection and analysis Hoganas, Sweden) and crude protein by the Kjedahl After completion of the feeding trial, all fish were method (N × 6.25) after acid digestion. Laboratory ana- counted and weighed in each tank to calculate weight lyses were done at the Feeds and Foods Nutrition Re- gain (WG), specific growth rate (SGR), feed efficiency search Centre (FFNRC) at Yongdang campus of PKNU, (FE), protein efficiency ratio (PER), and survival rate Republic of Korea. (SR). From each tank, three fish were randomly selected, measurement of length, weight, and dissected to obtain Statistical analysis visceral mass and liver to calculate hepatosomatic indi- After completion of all laboratory analysis, all data were ces (HSI), viscerosomatic indices (VSI), and condition analyzed by the one-way analysis of variance (ANOVA) Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 4 of 8 using SAS Program, Version 9.1 (SAS Institute, Cary, Non-specific immune responses NC, USA) to test for the effects of the different dietary Non-specific immune responses based on lysozyme and experimental treatments. A least significant difference superoxide dismutase (SOD) activities of juvenile rain- (LSD) test was used to compare the means of significant bow trout fed with five different experimental diets for effect. Effects of treatments were considered significant 7 weeks are summarized in Table 3. In lysozyme activity at confidence level of P < 0.05. For each treatment, mean and superoxide dismutase, no significant differences and SD were also calculated. were found among the fish fed every experimental groups (P< 0.05). Results Whole body proximate analysis Growth performances Whole body proximate compositions of juvenile rainbow Growth performances of juvenile rainbow trout, Onco- trout fed with five different experimental diets for rhynchus mykiss, based on weight gain (WG), specific 7 weeks are summarized in Table 4. Moisture of fish fed growth rate (SGR), feed efficiency (FE), protein efficiency TBB diet was significantly higher than CON, TBB , 37.5 12.5 ratio (PER), and survival rate (SR) fed with five different TBB , and TBB diets. No significant differences were 25 50 experimental diets for 7 weeks are summarized in Table 2. found among the fish fed CON, TBB , TBB , and 12.5 25 After completion of feeding trial, WG, SGR, FE, and PER TBB diets. Crude protein of fish fed CON showed no of fish fed CON was significantly higher than fish fed significant differences among the fish fed every diets. TBB diet (P< 0.05). But there were no significant differ- But fish fed TBB , TBB , and TBB diets were sig- 12.5 25 50 ences (P> 0.05) between fish fed TBB ,TBB ,and nificantly higher than fish fed TBB diet. No signifi- 12.5 25 37.5 TBB diets. Broken-line model analysis on the basis of cant difference was founded in crude lipid and crude ash 37.5 WG indicated that the minimum dietary level of enzym- among the fish fed every diets. atic hydrolyzed of tuna backbone by-product to replace fishmeal could be up to 29.7% in rainbow trout (Fig. 1). Hematological parameters Survival rate varied from 91.67 to 95.67%, but no signifi- Hematological parameters of blood serum in juvenile cant difference (P> 0.05) was found among fish fed with rainbow trout fed with five different experimental diets all dietary treatments. There was no significant difference for 7 weeks are summarized in Table 5. Total protein of in hepatosomatic index (HSI). Viscerosomatic index (VSI) fish fed CON showed no significant differences of fish fed TBB was significantly higher than fish fed (P> 0.05) among the fish fed all the experimental diets. 37.5 TBB diet. But no significant difference was found among But fish fed TBB diet was significantly higher 12.5 the fish fed CON, TBB ,and TBB diets. CF of CON (P< 0.05) than TBB and TBB diets. GOT of fish fed 12.5 25 37.5 50 was significantly higher than TBB and TBB diets. But TBB , TBB , and TBB diets was significantly higher 12 50 25 37.5 50 no significant difference was found among the fish fed (P< 0.05) than fish fed CON diet. But fish fed CON and TBB and TBB diets. TBB diets showed no significant differences 25 37.5 12.5 Table 2 Growth performances of juvenile rainbow trout fed with five experimental diets for 7 weeks Diets CON TBB TBB TBB TBB 12.5 25 37.5 50 1 a ab ab ab b WG 259 ± 14.9 250 ± 17.4 243 ± 17.7 239 ± 29.0 225 ± 8.82 2 a ab ab ab b SGR 2.13 ± 0.07 2.09 ± 0.08 2.05 ± 0.09 2.03 ± 0.14 1.96 ± 0.05 3 a ab ab ab b FE 133 ± 6.14 131 ± 6.34 127 ± 1.30 125 ± 2.82 125 ± 1.88 4 a ab ab ab b PER 2.76 ± 0.12 2.70 ± 0.12 2.63 ± 0.03 2.62 ± 0.05 2.59 ± 0.04 5 ns HSI 1.07 ± 0.50 0.91 ± 0.15 0.98 ± 0.12 1.03 ± 0.15 1.00 ± 0.13 6 ab ab ab a b VSI 6.58 ± 0.67 7.01 ± 0.60 6.87 ± 1.13 7.26 ± 0.99 6.35 ± 0.53 7 a bc ab ab c CF 1.07 ± 0.08 0.98 ± 0.09 1.04 ± 0.08 0.98 ± 0.06 0.90 ± 0.06 8 ns SR 93.3 ± 7.64 91.7 ± 5.77 91.7 ± 7.64 93.3 ± 11.6 95.7 ± 2.89 Values are means from triplicate groups of fish (n = 3) where values in each row with different superscripts are significantly different (P < 0.05) Weight gain (WG) = (final weight − initial weight) × 100/initial weight Specific growth rate (SGR; %/day) = (ln final weight − ln initial weight) × 100/d Feed efficiency (FE; %) = wet WG (g) × 100/dry feed intake (g) Protein efficiency ratio (PER) = wet weight gain/protein intake Hepatosomatic index (HSI; %) = (liver weight/body weight) × 100 Viscerosomatic index (VSI; %) = (visceral weight/body weight) × 100 7 3 Condition factor (CF) = {fish weight (g)/fish length (cm) } × 100 Survival (SR; %) = (total fish-dead fish) × 100/total fish Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 5 of 8 y = -1.12x + 281 R² = 1 29.7 0 10203040506070 of FM replaced by TBB Fig. 1 Broken line regression analysis of weight gain in rainbow trout fed experimental diets at different TBB levels (P> 0.05). GPT of fish fed TBB was significantly reducing growth performance and body composition. higher (P< 0.05) than the other diets. But no significant Feed utilization performance parameters such as FE and difference (P> 0.05) was observed among fish fed CON, PER were also influenced by dietary treatments in this TBB , TBB , TBB and TBB . study. FE and PER were both similar in fish fed the 12.5 25 37.5 50 CON diet and those of fish fed diets replacing up to Discussion 37.5% of fish meal with tuna backbone by-product. In this study, enzymatically hydrolyzed tuna backbone Higher replacement levels (TBB ) decreased FE and by-product was used in different levels in experimental PER in rainbow trout. This indicates that up to 37.5% of diets to partially replace commercially used fish meal FM replacement by tuna backbone by-product did not (FM). After completion of the feeding trial, weight gain negatively influence feed utilization performance of rain- (WG) and specific growth rate (SGR) of fish fed the bow trout. These results were consistent with the obser- 37.5% replacement diets with tuna backbone by-product vations in studies that used combinations of various were not significantly different from the FM fed fish. Al- protein sources in the diets of rainbow trout (Jo et al. though, 50% replacement of FM with tuna backbone 2016; Bureau et al. 2000). Similar studies on rainbow by-product reduced both the WG and SGR. This indi- trout have also reported that partially hydrolyzed ingre- cates that enzymatic hydrolyzed tuna backbone dients have higher nutritional value because of higher by-product containing diets can partially replace FM but up to at a certain level. In a relevant study by Mendoza Table 4 Whole body proximate composition of juvenile et al. (2001), it was reported that using enzymatic hydro- rainbow trout fed with five experimental diets for 7 weeks lyzed and co-extruded feather meal with soya-bean meal (% dry matter basis) in practical diets for the pacific-white shrimp (Litope- Diets naeus vannamei) can replace up to 20% of FM without CON TBB TBB TBB TBB 12.5 25 37.5 50 1 b b b a b Mo 78.3 ± 0.11 77.2 ± 0.58 78.3 ± 0.22 79.1 ± 0.32 78.3 ± 0.47 2 ab a a b a Table 3 Non-specific immune responses of juvenile rainbow trout CP 14.6 ± 0.45 15.1 ± 0.25 15.1 ± 0.02 14.4 ± 0.07 15.2 ± 0.56 fed with five experimental diets for 7 weeks 3 ns CL 4.80 ± 0.75 5.06 ± 0.52 5.26 ± 0.06 4.60 ± 0.20 4.93 ± 0.44 Diets 4 ns As 1.94 ± 0.10 2.06 ± 0.10 1.96 ± 0.10 1.92 ± 0.05 2.10 ± 0.16 CON TBB TBB TBB TBB 12 25 37 50 Values are means from triplicate groups of fish (n = 3) where in each row with 1 ns Lys 1.35 ± 0.30 1.58 ± 0.32 1.60 ± 0.28 1.64 ± 0.37 1.24 ± 0.05 different superscripts values are significantly different (P < 0.05) Mo moisture content of whole body composition of juvenile rainbow trout in 2 ns SOD 80.9 ± 8.27 79.0 ± 7.76 80.6 ± 4.09 76.4 ± 2.02 83.6 ± 7.07 different diets Values are means from triplicate groups of fish (n = 3) where in each row with CP crude protein present under different dietary treatments different superscripts values are significantly different (P < 0.05) CL crude lipid, present in whole body proximate composition of juvenile Lysozyme (U/l) rainbow trout after feeding trial 2 4 Superoxide dismutase (% inhibition) As ash content of whole body proximate composition of fish in different diets Weight gain ( ) Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 6 of 8 Table 5 Hematological parameters of juvenile rainbow trout fed with five experimental diets for 7 weeks Diets CONT TBB TBB TBB TBB 12.5 25 37.5 50 1 ns GL 105 ± 6.51 112 ± 8.19 113 ± 3.00 111.3 ± 6.03 107 ± 9.17 2 ab a ab b b TP 3.60 ± 0.10 3.73 ± 0.23 3.40 ± 0.26 3.30 ± 0.10 3.33 ± 0.25 3 c bc ab a ab GOT 402 ± 39.1 452 ± 26.0 517 ± 16.2 530 ± 52.9 509 ± 44.5 4 b b b b a GPT 8.00 ± 3.61 8.67 ± 2.08 10.3 ± 2.31 10.0 ± 1.73 18.7 ± 2.52 Values are means from triplicate groups of fish (n = 3) where in each row with different superscripts values are significantly different (P < 0.05) GL glucose (mg/dl) TP total protein (g/dl) GOT glutamic glutamic oxaloacetic transaminase (U/l) GPT glutamic pyruvic transaminase (U/l): levels of free amino acids. This makes these ingredients (O ) dismutation into molecular oxygen (O ) and 2- 2 more digestible and fish can utilize the ingredients more hydrogen peroxide (H O ) (Shao et al. 2010). This will 2 2 efficiently that will results in higher growth and feed support a significant defense system against oxidative utilization performances (Dong et al. 1993; Hardy 2002). damage. Findings of the present study did not show any The hepatosomatic index (HSI) was not changed in fish significant differences in lysozyme or SOD activities in fed all the experimental diets. Although, viscerosomatic all the experimental fish. This shows that even 50% re- index (VSI) and condition factor (CF) were lower in fish placement of FM with tuna backbone by-product does fed the TBB50 diet compared to those of fish fed the not influence the innate immunity of rainbow trout. This CON diet. HIS, VSI, and CF are good representatives for could be attributed to standard experimental conditions health, general well-being, and feed quality (Ighwela et while tuna backbone by-product was providing sufficient al. 2014). These parameter showed that until 37.5% re- protein with well-balanced amino acids to support the placement of FM with tuna backbone by-product has no immune system (Sullivan 2008; Jo et al. 2016). negative effects on rainbow trout organosomatic health. Serum parameters as well as hematological activities These results were similar with previous studies using are good indicators of health status of any organism and tuna by-products as a protein source for rainbow trout can vary with temperature, season, and nutritional status (Samuelsen et al. 2001; Caballero et al. 2002; Tekinay et (Blaxhall 1972). They are suitable indicators for evaluat- al. 2009). Noteworthy, in this study, we observed more ing the health, stress level, and physiological welfare of than 90% survival for all experimental groups that could fish (Simide et al. 2016). Serum glucose is a stress indi- be related to standard rearing condition and feed. Whole cator of fish and stress hormone which is associated with body proximate composition of rainbow trout fed the cortisol, mobilize and increase glucose production in experimental diets did not show any specific trend in blood serum to cope with the required energy produced the present study. Whereas crude lipid and ash were by a stressor (Wallace et al. 1994). Total protein of same for all fish fed the experimental diets and there blood serum is also considered a strong natural response were no significant differences in crude protein between in fish (Reverter et al. 2014) and assessments can reflect the CON and other experimental groups. Some studies nutritional levels. (Acharya and Mohanty 2014). In the have reported a trend in which whole body moisture present study, glucose content of serum did not show content shows opposite values compared to protein con- any significant differences in fish fed all the experimental tent in rainbow trout, O. mykiss (Jo et al. 2016); kuruma diets. There were also no differences in serum total pro- shrimp, Marsupenaeus japonicas (Bulbul et al. 2016); tein level of fish fed the CON diet and those of fish fed and Australian short-finned eel, Aaustralis australis the other diets. Glutamic oxaloacetic transaminase (Engin and Carter 2005). (GOT) and glutamic pyruvic transaminase (GPT) which Non-specific immune responses are the basic mechan- are enzymes or proteins mostly found in liver cells and ism of defense system in fish and play a vital role in the rising levels in blood serum indicate damage or inflam- obtained immune response and homeostasis by a system mation of liver cells (Giannini et al. 2005). In the present of receptor proteins (Srivastava and Pandey 2015; Halver study, the GOT level showed an increasing trend with and Hardy 2002; Reverter et al. 2014; Uribe et al. 2011). higher FM replacement levels. While fish fed diets Lysozyme activity is an important humoral indicator of TBB ,TBB , and TBB had a higher GOT compared 25 37.5 50 non-specific immunity in fish and one of the important to fish fed the CON diet. Serum GPT also showed higher enzymes of defensive mechanism that protects the host levels for fish fed the TBB diet compared to all other (Ellis 1999; Jo et al. 2016). On the other hand, SOD is a experimental fish. An increase in GOT and GPT could metalloenzyme that catalyzes the superoxide radical be attributed to the addition of alternative protein Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 7 of 8 sources in fish diets because of various dynamics such as Received: 11 November 2018 Accepted: 4 January 2019 reduction in FM content, tolerance of anti-nutritional factors, digestibility, and palatability problems (Jo et al. References 2016; National Research Council, NRC 2011). Acharya G, Mohanty PK. Comparative haematological and serum biochemical analysis of catfishes Clariasbatrachus (Linnaeus, 1758) and Heteropneustes fossilis (Bloch, 1794) with respect to sex. J Entomol Zool Stud. 2014;2:191–7. Conclusions Anderson AD, Alam MS, Watanabe WO, Carroll PM, Wedegaertner TC, Dowd MK. Full replacement of menhaden fish meal protein by low-gossypol Considering growth performances, non-specific immune cottonseed flour protein in the diet of juvenile black sea bass, Centropristis responses, other relevant parameters in CON, and other striata. Aquaculture. 2016;464:618–28. diets which included tuna backbone by-products for FM AOAC. 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Funding Caballero MJ, Obach A, Rosenlund G, Montero D, Gisvold M, Izquierdo MS. This research work was supported by the Pukyong National University Research Impact of different dietary lipid sources on growth, lipid digestibility, tissue Fund in 2017 (C-D-2017-0333). fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture. 2002;214:253–71. Cho JH, Kim IH. Fish meal-nutritive value. J Anim Physiol An N. 2011;95:685–92. Availability of data and materials Cowey CB. Nutrition: estimating requirements of rainbow trout. Aquaculture. Please contact author for data requests. 1992;100:177–89. Dong FM, Hardy RW, Haard NF, Barrows FT, Rasco BA, Fairgrieve WT, Forster IP. Authors’ contributions Chemical composition and digestibility of poultry by-product meals for JB designed, conducted the experiment, and wrote the paper. MDAKA salmon diets. Aquaculture. 1993;116:149–58. conducted feeding trial. SW design and conducted some parts of the Ellis AE. 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Effects of enzymatically hydrolyzed fish by-products in diet of juvenile rainbow trout (Oncorhynchus mykiss)

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Springer Journals
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Copyright © 2019 by The Author(s)
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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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2234-1757
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10.1186/s41240-019-0117-4
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Abstract

Five experimental diets were formulated to evaluate the effects of dietary enzymatically hydrolyzed tuna by-product on growth, non-specific immune responses, and hematology of juvenile rainbow trout (Oncorhynchus mykiss). A basal diet with 50% of fishmeal was used as control (CON) and four other diets replaced 12.5% (TBB ), 25% (TBB ), 37.5% 12.5 25 (TBB ), and 50% (TBB ) of fish meal in the CON diet. Juvenile rainbow trout (4.87 ± 0.05 g) were randomly distributed 37.5 50 into 15 tanks (50 L) and fed 3–4% of wet body weight two times a day. At the end of 7 weeks of feeding trial, weight gain, specific growth rate, feed efficiency, and protein efficiency ratio of fish fed CON diet were significantly higher than those of fish fed TB diet (P< 0.05). But there were no significant differences among fish fed CON, TBB ,TBB ,and 50 12.5 25 TBB diets (P> 0.05). There were no significant differences in GPT levels among fish fed CON, TBB ,TBB ,and 37.5 12.5 25 TBB diets. Also, there were no significant differences in lysozyme, superoxide dismutase, glucose, and total protein 37.5 levels in all experimental diet (P> 0.05). The broken-line analysis indicated that the minimum dietary level of enzymatically hydrolyzed tuna by-product to replace fishmeal could be 29.7% in rainbow trout. These results indicated that the optimum level of dietary enzymatically hydrolyzed tuna by-product could replace greater than 29.7% but less than 37.5% of fishmeal in juvenile rainbow trout diet. Keywords: Rainbow trout, Enzymatic hydrolysis, Growth performance, Immune response, Tuna by-products Background increase. According to a recent report, the global pro- Fish meal (FM) is the one of the most important ingredi- duction of fish meal has decreased by about 1.1 million ents used in aquafeed. FM is a high-quality source of tons compared to the production in 2000 (IFFO 2018). protein and is desirable for its rich essential amino acids Tremendous price increases for FM together with envir- profile (Cho and Kim 2011; Anderson et al. 2016) as well onmental concerns have forced the aquaculture industry as for its vitamin and mineral content (IFOMA 2000). to find alternative protein sources for aquafeed formula- Typically, FM (66% crude protein) is the preferred tion. As a result, at this moment, the replacement of FM source of protein in aquafeed formulation, yet the cost in aqua feeds is one of the most pressing issues facing of FM is continually increasing (Tomas et al. 2005; the industry. Conversely, alternative protein sources can Anderson et al. 2016;FAO 2018). It is to be noted that relieve this problem by lowering the cost of feed, redu- the world demand of FM increased by only about 27% cing the amount of dependence on wild fish, and poten- during the past two decades, while FM output by the tially reduces the nutrient levels in effluent waste (Van major FM-producing countries actually decreased. Be- Weerd et al. 1999; Papatryphon and Soares Jr. 2001; cause of the limited supply of FM coupled with its in- Masumoto et al. 2001). However, for most species, there is creasing demand, the cost of producing fish is likely to a limit on amount of FM that can be replaced by alterna- tive protein sources without causing negative effects on the health and physiology of the fish. Therefore, a new * Correspondence: scbai@pknu.ac.kr feed ingredient that is both cheaper and free from disease Department of Marine Bio-Materials and Aquaculture/Feeds and Foods is highly desirable. Therefore, fishery by-products could Nutrition Research Center (FFNRC), Pukyong National University, 599-1 Daeyeon 3-Dong, Busan 608-737, Republic of Korea be a possible solution. Uyan et al. (2006)reported that 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. Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 2 of 8 tuna muscle by-product powder is a promising feed ingre- growth and non-specific immune responses in juvenile dient to replace 50% FM protein without reduction in the rainbow trout. growth performance of olive flounder. Enzymatic hydrolysis is a process by which enzymes Materials and methods facilitate the cleavage of chemical bonds by water, play- Experimental design and diets ing a pivotal role in the digestion of food (Nielsang et al. A basal diet was formulated containing crude protein 2005). This process makes it possible to improve the nu- 50.22%, crude lipid 13.71%, ash 9.79%, and moisture tritive value of individual feed ingredients (PER, digest- 4.93%; without inclusion of enzymatically hydrolyzed ibility and FCR). Moreover, the moisture contents of the tuna backbone by-products, used as control diet (CON) ingredients remain almost the same, varying only by 2.5 and four other experimental diets were formulated using ± 4.4%, maintaining typical parameters for storage of in- enzymatically hydrolyzed tuna backbone by-products. gredients. Lastly, an important benefit of extrusion after TBB , TBB , TBB , and TBB diet were formulated enzymatic hydrolysis is the sterilization of the ingredi- 12.5 25 37.5 50 with hydrolyzed tuna by-products level of 12.5%, 25%, ents. Enzymatic hydrolyzed by-products are now 37.5%, and 50% replacement of FM respectively (Table 1). widely used to modify or improve protein quality and The ingredients were grounded into powder form using a their digestibility (Panyam and Kilara 1996; Liaset et grinding machine and sieved before inclusion of ingredi- al. 2000;Je etal. 2007; Baek and Cadwallader 1995; ents. The resultant mixtures become pelletized with a pel- Nielsang et al. 2005). Nevertheless, the presence of let machine with no heating using a module of 2-mm endogenous enzymes in by-products may induce auto diameter and air dried for 3 days. The dried feeds were hydrolysis. In the case of squid gut and muscle, high endogenous proteolytic activity has been reported (Sugiyama et al. 1989; Leblanc and Gill 1982;Rodger Table 1 Formulation and proximate composition of five et al. 1984) and during chopping, the tissues become experimental diets (% of dry matter basis) hydrolyzed, rendering it richer in free essential amino Ingredients Diets acids (Lian et al. 2005). Hydrolyzed fish by-products (% in diet) CON TBB TBB TBB TBB 12.5 25 37.5 50 from Alaskan fisheries have been evaluated for re- Fishmeal 50 43.75 37.50 31.25 25.00 placement of menhaden FM in Litopenaeus vannamei En. H.B 0.00 5.82 11.64 17.46 23.27 diets (Forster et al. 2011). Replacement of FM in aqua feeds with inexpensive protein sources, such as unex- Blood meal 2.90 2.90 2.90 2.90 2.90 ploited by-products which are regionally or locally Soybean meal 3.50 3.50 3.50 3.50 3.50 available, may be a great opportunity for sustainable Wheat gluten meal 7.9 7.9 7.9 7.9 7.9 resource utilization. Cornstarch 0.00 0.6 1.18 1.78 2.39 Rainbow trout, Oncorhynchus mykiss, is one of most Wheat flour 20.00 20.00 20.00 20.00 20.00 popular fish species around the world, due to its Soybean oil 7.80 7.80 7.80 7.80 7.80 excellent meat quality (Vehviläinen et al. 2008). It is also one of the most studied species and is widely used for Fish oil 3.37 3.02 2.68 2.33 1.98 research in many fields such as carcinogenesis, toxicology, Cellulose 0.53 0.71 0.90 1.08 1.26 immunology, ecology, physiology, and nutrition (Thor- Vitamin premix 2.00 2.00 2.0 2.00 2.00 gaard et al. 2002;Cowey 1992; Boyle et al. 2013;Berthelot Mineral premix 2.00 2.00 2.0 2.00 2.00 et al. 2014). Global rainbow trout production from aqua- Total 100 100 100 100 100 culture has grown tremendously and has reached Proximate analysis (% of DM) 814,090 metric tons as of 2016 (FAO 2018). For Repub- lic of Korea, rainbow trout is also one of the commer- Moisture 4.93 5.72 6.17 7.22 7.30 cially important freshwater species with 3358 metric Protein 50.22 48.71 48.34 47.95 46.81 tons of production in 2017; ranking third among fresh- Lipid 13.71 12.75 14.89 14.25 13.61 water species nationally (KOSTAT 2018). Numerous Ash 9.79 9.59 9.49 9.11 9.05 studies have been conducted on FM replacement in TBB12.5 tuna backbone by-products at 12.5% FM replacement (Samhae Company, rainbow trout (Hauptman et al. 2014). However, to our Gyeongiu, South Korea) knowledge, no study has been conducted using enzy- TBB25 tuna backbone by-products at 25% FM replacement (Samhae Company, Gyeongiu, South Korea) matically hydrolyzed tuna by-products for replacing FM TBB37.5 tuna backbone by-products at 37.5% FM replacement (Samhae Company, in the diet of juvenile rainbow trout. Based on the re- Gyeongiu, South Korea) TBB50 tuna backbone by-products at 50% FM replacement sultsobtainedinpreviousstudies,the aimof thisstudy CON control diet (the basal diet) is to partially replace FM with enzymatically hydrolyzed b En. H.B enzymatic hydrolyzed by-products (Samhae Company, Gyeongiu, tuna by-products in order to examine the effects on South Korea) Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 3 of 8 sieved and packaged in zip-lock bags, labeled and stored factor (CF). Blood samples were collected from the cau- at − 20 °C until the feeding trial. dal vein of the fish with 1 ml syringes. Serum samples obtained from blood on clotting by centrifugation at Experimental fish and feeding conditions 5000×g for 10 min and stored at − 70 °C for the analysis The feeding trial was conducted in the Department of of the activities of lysozyme and superoxide dismutase Marine Bio-Materials and Aquaculture and Feeds and (SOD). A turbid metric assay was used for the measure- Foods Nutrition Centre, Pukyong National University ment of lysozyme activity of blood serum using the (PKNU), Busan, Republic of Korea. Experimental rain- method by Hultmark (1980) with slightly modifications. −1 bow trout fry were collected from a local rainbow trout Micrococcus lysodeikticus (0.75 mg ml ) was suspended farm named Ihwajeong Fish Farm, Sangju city, Korea. in sodium phosphate buffer (0.1 M, pH 6.4), then 200 μl Before starting of the feeding trial, all fishes were fed of suspension was placed in each well of 96-well plates with the basal diet two times in a day to acclimatize and after that 20 μl of test serum was added. After incu- them to the laboratory experimental conditions for bation, the reduction in absorbance of the samples was 2 weeks. Feeding trial was done using an indoor recorded at 570 nm at room temperature for 0 and semi-recirculation system with 15 tanks of 50 L water 60 min in a micro plate reader (UVM 340, Biochrom, holding capacity receiving constant filtered freshwater Cambridge, UK). One unit of lysozyme activity was −1 −1. flow at a rate of 2 L min from the central tank. Half of regarded as a reduction in absorbance of 0.001 min the water was exchanged everyday by pumping filtered Activity of SOD was measured according to the per- fresh water to the central tank. Supplementary continu- centage of reaction inhibition rate of the enzyme with ous aeration facility provided to maintain required dis- WST-1 (water-soluble tetrazolium dye) substrate and solved oxygen (D.O) and by using water heaters, xanthine oxidase using an SOD Assay Kit (Enzo temperature always maintained at 14.0 ± 0.1 °C through- ADI-900-157, Enzo Life Sciences, Inc.) in accordance out the experimental period. Four hundred eighty fishes with manufacturer’s instructions. Each endpoint assay with an average weight of 4.87 ± 0.05 g (mean ± SD) were was monitored by absorbance at 450 nm (the absorbance weighed and distributed as 20 fish/tank randomly into wavelength for the colored product of WST-1 reaction the 15 experimental indoor tanks. Three tanks were ran- with superoxide) after 20 min of reaction time at 37 °C. domly selected for each one of the experimental diet. In The inhibition percentage was normalized by mg of pro- this way, 15 tanks are randomly assigned for 5 dietary tein and showed as SOD activity units. Serum portions treatments and marked the tanks. Feeding was done two were also used for the biochemical parameters analysis times daily (09:00 A.M. and 05:00 P.M.). Feed amount of total protein (TP) of plasma, glutamic oxaloacetic adjusted ranged from 3 to 4% according to the wet body transaminase (GOT), glutamic pyruvic transaminase weight in the beginning and at the end of feeding trial (GPT), and glucose activities determined using the com- respectively for 7 weeks. Two hours after feeding, all mercial clinical kits of Fuji DRI-CHEM 3500i, Fuji Photo tanks were siphoned to remove fecal matter and uneaten Film Ltd., Tokyo, Japan. feeds daily. Mortality would check daily, dead fish imme- From each tank, three fish were collected and pooled diately removed and weighed, and required feed together according to the fish fed with different experi- amounts for the tanks adjusted according to the mental diets; homogenized and freeze-dried at − 80 °C remaining body weight of fish in the tanks. Dead fish for analysis. Proximate compositions of the experimental was not replaced during the experiment. Total weight of fish and the basal diet were determined according to fish in each tank was determined at 4th week for adjust standard procedures of AOAC (2005) in duplicates. Both the amount of diet for feeding. Before each checking, samples were dried at 105 °C to a constant weight to de- fish were starved for 24 h to avoid inclusion of ingested termine moisture content. Determination of ash content feed in the measurements of fish body weight as well as was done by incineration in a muffle furnace at 550 °C to minimize stress. for 3.5 h, crude lipid was determined by the Soxhlet ex- traction using Soxtec system 1046 (Tecator AB, Foss, Sample collection and analysis Hoganas, Sweden) and crude protein by the Kjedahl After completion of the feeding trial, all fish were method (N × 6.25) after acid digestion. Laboratory ana- counted and weighed in each tank to calculate weight lyses were done at the Feeds and Foods Nutrition Re- gain (WG), specific growth rate (SGR), feed efficiency search Centre (FFNRC) at Yongdang campus of PKNU, (FE), protein efficiency ratio (PER), and survival rate Republic of Korea. (SR). From each tank, three fish were randomly selected, measurement of length, weight, and dissected to obtain Statistical analysis visceral mass and liver to calculate hepatosomatic indi- After completion of all laboratory analysis, all data were ces (HSI), viscerosomatic indices (VSI), and condition analyzed by the one-way analysis of variance (ANOVA) Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 4 of 8 using SAS Program, Version 9.1 (SAS Institute, Cary, Non-specific immune responses NC, USA) to test for the effects of the different dietary Non-specific immune responses based on lysozyme and experimental treatments. A least significant difference superoxide dismutase (SOD) activities of juvenile rain- (LSD) test was used to compare the means of significant bow trout fed with five different experimental diets for effect. Effects of treatments were considered significant 7 weeks are summarized in Table 3. In lysozyme activity at confidence level of P < 0.05. For each treatment, mean and superoxide dismutase, no significant differences and SD were also calculated. were found among the fish fed every experimental groups (P< 0.05). Results Whole body proximate analysis Growth performances Whole body proximate compositions of juvenile rainbow Growth performances of juvenile rainbow trout, Onco- trout fed with five different experimental diets for rhynchus mykiss, based on weight gain (WG), specific 7 weeks are summarized in Table 4. Moisture of fish fed growth rate (SGR), feed efficiency (FE), protein efficiency TBB diet was significantly higher than CON, TBB , 37.5 12.5 ratio (PER), and survival rate (SR) fed with five different TBB , and TBB diets. No significant differences were 25 50 experimental diets for 7 weeks are summarized in Table 2. found among the fish fed CON, TBB , TBB , and 12.5 25 After completion of feeding trial, WG, SGR, FE, and PER TBB diets. Crude protein of fish fed CON showed no of fish fed CON was significantly higher than fish fed significant differences among the fish fed every diets. TBB diet (P< 0.05). But there were no significant differ- But fish fed TBB , TBB , and TBB diets were sig- 12.5 25 50 ences (P> 0.05) between fish fed TBB ,TBB ,and nificantly higher than fish fed TBB diet. No signifi- 12.5 25 37.5 TBB diets. Broken-line model analysis on the basis of cant difference was founded in crude lipid and crude ash 37.5 WG indicated that the minimum dietary level of enzym- among the fish fed every diets. atic hydrolyzed of tuna backbone by-product to replace fishmeal could be up to 29.7% in rainbow trout (Fig. 1). Hematological parameters Survival rate varied from 91.67 to 95.67%, but no signifi- Hematological parameters of blood serum in juvenile cant difference (P> 0.05) was found among fish fed with rainbow trout fed with five different experimental diets all dietary treatments. There was no significant difference for 7 weeks are summarized in Table 5. Total protein of in hepatosomatic index (HSI). Viscerosomatic index (VSI) fish fed CON showed no significant differences of fish fed TBB was significantly higher than fish fed (P> 0.05) among the fish fed all the experimental diets. 37.5 TBB diet. But no significant difference was found among But fish fed TBB diet was significantly higher 12.5 the fish fed CON, TBB ,and TBB diets. CF of CON (P< 0.05) than TBB and TBB diets. GOT of fish fed 12.5 25 37.5 50 was significantly higher than TBB and TBB diets. But TBB , TBB , and TBB diets was significantly higher 12 50 25 37.5 50 no significant difference was found among the fish fed (P< 0.05) than fish fed CON diet. But fish fed CON and TBB and TBB diets. TBB diets showed no significant differences 25 37.5 12.5 Table 2 Growth performances of juvenile rainbow trout fed with five experimental diets for 7 weeks Diets CON TBB TBB TBB TBB 12.5 25 37.5 50 1 a ab ab ab b WG 259 ± 14.9 250 ± 17.4 243 ± 17.7 239 ± 29.0 225 ± 8.82 2 a ab ab ab b SGR 2.13 ± 0.07 2.09 ± 0.08 2.05 ± 0.09 2.03 ± 0.14 1.96 ± 0.05 3 a ab ab ab b FE 133 ± 6.14 131 ± 6.34 127 ± 1.30 125 ± 2.82 125 ± 1.88 4 a ab ab ab b PER 2.76 ± 0.12 2.70 ± 0.12 2.63 ± 0.03 2.62 ± 0.05 2.59 ± 0.04 5 ns HSI 1.07 ± 0.50 0.91 ± 0.15 0.98 ± 0.12 1.03 ± 0.15 1.00 ± 0.13 6 ab ab ab a b VSI 6.58 ± 0.67 7.01 ± 0.60 6.87 ± 1.13 7.26 ± 0.99 6.35 ± 0.53 7 a bc ab ab c CF 1.07 ± 0.08 0.98 ± 0.09 1.04 ± 0.08 0.98 ± 0.06 0.90 ± 0.06 8 ns SR 93.3 ± 7.64 91.7 ± 5.77 91.7 ± 7.64 93.3 ± 11.6 95.7 ± 2.89 Values are means from triplicate groups of fish (n = 3) where values in each row with different superscripts are significantly different (P < 0.05) Weight gain (WG) = (final weight − initial weight) × 100/initial weight Specific growth rate (SGR; %/day) = (ln final weight − ln initial weight) × 100/d Feed efficiency (FE; %) = wet WG (g) × 100/dry feed intake (g) Protein efficiency ratio (PER) = wet weight gain/protein intake Hepatosomatic index (HSI; %) = (liver weight/body weight) × 100 Viscerosomatic index (VSI; %) = (visceral weight/body weight) × 100 7 3 Condition factor (CF) = {fish weight (g)/fish length (cm) } × 100 Survival (SR; %) = (total fish-dead fish) × 100/total fish Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 5 of 8 y = -1.12x + 281 R² = 1 29.7 0 10203040506070 of FM replaced by TBB Fig. 1 Broken line regression analysis of weight gain in rainbow trout fed experimental diets at different TBB levels (P> 0.05). GPT of fish fed TBB was significantly reducing growth performance and body composition. higher (P< 0.05) than the other diets. But no significant Feed utilization performance parameters such as FE and difference (P> 0.05) was observed among fish fed CON, PER were also influenced by dietary treatments in this TBB , TBB , TBB and TBB . study. FE and PER were both similar in fish fed the 12.5 25 37.5 50 CON diet and those of fish fed diets replacing up to Discussion 37.5% of fish meal with tuna backbone by-product. In this study, enzymatically hydrolyzed tuna backbone Higher replacement levels (TBB ) decreased FE and by-product was used in different levels in experimental PER in rainbow trout. This indicates that up to 37.5% of diets to partially replace commercially used fish meal FM replacement by tuna backbone by-product did not (FM). After completion of the feeding trial, weight gain negatively influence feed utilization performance of rain- (WG) and specific growth rate (SGR) of fish fed the bow trout. These results were consistent with the obser- 37.5% replacement diets with tuna backbone by-product vations in studies that used combinations of various were not significantly different from the FM fed fish. Al- protein sources in the diets of rainbow trout (Jo et al. though, 50% replacement of FM with tuna backbone 2016; Bureau et al. 2000). Similar studies on rainbow by-product reduced both the WG and SGR. This indi- trout have also reported that partially hydrolyzed ingre- cates that enzymatic hydrolyzed tuna backbone dients have higher nutritional value because of higher by-product containing diets can partially replace FM but up to at a certain level. In a relevant study by Mendoza Table 4 Whole body proximate composition of juvenile et al. (2001), it was reported that using enzymatic hydro- rainbow trout fed with five experimental diets for 7 weeks lyzed and co-extruded feather meal with soya-bean meal (% dry matter basis) in practical diets for the pacific-white shrimp (Litope- Diets naeus vannamei) can replace up to 20% of FM without CON TBB TBB TBB TBB 12.5 25 37.5 50 1 b b b a b Mo 78.3 ± 0.11 77.2 ± 0.58 78.3 ± 0.22 79.1 ± 0.32 78.3 ± 0.47 2 ab a a b a Table 3 Non-specific immune responses of juvenile rainbow trout CP 14.6 ± 0.45 15.1 ± 0.25 15.1 ± 0.02 14.4 ± 0.07 15.2 ± 0.56 fed with five experimental diets for 7 weeks 3 ns CL 4.80 ± 0.75 5.06 ± 0.52 5.26 ± 0.06 4.60 ± 0.20 4.93 ± 0.44 Diets 4 ns As 1.94 ± 0.10 2.06 ± 0.10 1.96 ± 0.10 1.92 ± 0.05 2.10 ± 0.16 CON TBB TBB TBB TBB 12 25 37 50 Values are means from triplicate groups of fish (n = 3) where in each row with 1 ns Lys 1.35 ± 0.30 1.58 ± 0.32 1.60 ± 0.28 1.64 ± 0.37 1.24 ± 0.05 different superscripts values are significantly different (P < 0.05) Mo moisture content of whole body composition of juvenile rainbow trout in 2 ns SOD 80.9 ± 8.27 79.0 ± 7.76 80.6 ± 4.09 76.4 ± 2.02 83.6 ± 7.07 different diets Values are means from triplicate groups of fish (n = 3) where in each row with CP crude protein present under different dietary treatments different superscripts values are significantly different (P < 0.05) CL crude lipid, present in whole body proximate composition of juvenile Lysozyme (U/l) rainbow trout after feeding trial 2 4 Superoxide dismutase (% inhibition) As ash content of whole body proximate composition of fish in different diets Weight gain ( ) Bae et al. Fisheries and Aquatic Sciences (2019) 22:1 Page 6 of 8 Table 5 Hematological parameters of juvenile rainbow trout fed with five experimental diets for 7 weeks Diets CONT TBB TBB TBB TBB 12.5 25 37.5 50 1 ns GL 105 ± 6.51 112 ± 8.19 113 ± 3.00 111.3 ± 6.03 107 ± 9.17 2 ab a ab b b TP 3.60 ± 0.10 3.73 ± 0.23 3.40 ± 0.26 3.30 ± 0.10 3.33 ± 0.25 3 c bc ab a ab GOT 402 ± 39.1 452 ± 26.0 517 ± 16.2 530 ± 52.9 509 ± 44.5 4 b b b b a GPT 8.00 ± 3.61 8.67 ± 2.08 10.3 ± 2.31 10.0 ± 1.73 18.7 ± 2.52 Values are means from triplicate groups of fish (n = 3) where in each row with different superscripts values are significantly different (P < 0.05) GL glucose (mg/dl) TP total protein (g/dl) GOT glutamic glutamic oxaloacetic transaminase (U/l) GPT glutamic pyruvic transaminase (U/l): levels of free amino acids. This makes these ingredients (O ) dismutation into molecular oxygen (O ) and 2- 2 more digestible and fish can utilize the ingredients more hydrogen peroxide (H O ) (Shao et al. 2010). This will 2 2 efficiently that will results in higher growth and feed support a significant defense system against oxidative utilization performances (Dong et al. 1993; Hardy 2002). damage. Findings of the present study did not show any The hepatosomatic index (HSI) was not changed in fish significant differences in lysozyme or SOD activities in fed all the experimental diets. Although, viscerosomatic all the experimental fish. This shows that even 50% re- index (VSI) and condition factor (CF) were lower in fish placement of FM with tuna backbone by-product does fed the TBB50 diet compared to those of fish fed the not influence the innate immunity of rainbow trout. This CON diet. HIS, VSI, and CF are good representatives for could be attributed to standard experimental conditions health, general well-being, and feed quality (Ighwela et while tuna backbone by-product was providing sufficient al. 2014). These parameter showed that until 37.5% re- protein with well-balanced amino acids to support the placement of FM with tuna backbone by-product has no immune system (Sullivan 2008; Jo et al. 2016). negative effects on rainbow trout organosomatic health. Serum parameters as well as hematological activities These results were similar with previous studies using are good indicators of health status of any organism and tuna by-products as a protein source for rainbow trout can vary with temperature, season, and nutritional status (Samuelsen et al. 2001; Caballero et al. 2002; Tekinay et (Blaxhall 1972). They are suitable indicators for evaluat- al. 2009). Noteworthy, in this study, we observed more ing the health, stress level, and physiological welfare of than 90% survival for all experimental groups that could fish (Simide et al. 2016). Serum glucose is a stress indi- be related to standard rearing condition and feed. Whole cator of fish and stress hormone which is associated with body proximate composition of rainbow trout fed the cortisol, mobilize and increase glucose production in experimental diets did not show any specific trend in blood serum to cope with the required energy produced the present study. Whereas crude lipid and ash were by a stressor (Wallace et al. 1994). Total protein of same for all fish fed the experimental diets and there blood serum is also considered a strong natural response were no significant differences in crude protein between in fish (Reverter et al. 2014) and assessments can reflect the CON and other experimental groups. Some studies nutritional levels. (Acharya and Mohanty 2014). In the have reported a trend in which whole body moisture present study, glucose content of serum did not show content shows opposite values compared to protein con- any significant differences in fish fed all the experimental tent in rainbow trout, O. mykiss (Jo et al. 2016); kuruma diets. There were also no differences in serum total pro- shrimp, Marsupenaeus japonicas (Bulbul et al. 2016); tein level of fish fed the CON diet and those of fish fed and Australian short-finned eel, Aaustralis australis the other diets. Glutamic oxaloacetic transaminase (Engin and Carter 2005). (GOT) and glutamic pyruvic transaminase (GPT) which Non-specific immune responses are the basic mechan- are enzymes or proteins mostly found in liver cells and ism of defense system in fish and play a vital role in the rising levels in blood serum indicate damage or inflam- obtained immune response and homeostasis by a system mation of liver cells (Giannini et al. 2005). In the present of receptor proteins (Srivastava and Pandey 2015; Halver study, the GOT level showed an increasing trend with and Hardy 2002; Reverter et al. 2014; Uribe et al. 2011). higher FM replacement levels. While fish fed diets Lysozyme activity is an important humoral indicator of TBB ,TBB , and TBB had a higher GOT compared 25 37.5 50 non-specific immunity in fish and one of the important to fish fed the CON diet. Serum GPT also showed higher enzymes of defensive mechanism that protects the host levels for fish fed the TBB diet compared to all other (Ellis 1999; Jo et al. 2016). On the other hand, SOD is a experimental fish. An increase in GOT and GPT could metalloenzyme that catalyzes the superoxide radical be attributed to the addition of alternative protein Bae et al. 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