Tuna byproducts as a fish-meal in tilapia aquaculture

Ecotoxicology and Environmental Safety 172 (2019) 364–372

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Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv

Tuna byproducts as a fish-meal in tilapia aquaculture a

b

c

c

T d

Kyochan Kim , Youngjin Park , Hyeong-Woo Je , Minji Seong , Jim Hyacinth Damusaru , ⁎ ⁎ Soohwan Kime, Joo-Young Jungc, , Sungchul C. Baic, a

Department of Chemical and Biomolecular Engineering, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon 34141, Republic of Korea Faculty of Biosciences and Aquaculture, Nord University, Universitetsalléen 11, 8049 Bodø, Norway Department of Marine Bio-materials and Aquaculture / Feeds & Foods Nutrition Research Center, Pukyong National University, 365 Sinseon-ro, Nam-gu, Busan 48547, Republic of Korea d Department of Fisheries, School of Maritime Studies & Technology, Solomon Islands National University, PO. Box R113, Honiara, Solomon Islands e Department of Marine Life Science, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Island 63243, Republic of Korea b c

A R T I C LE I N FO

A B S T R A C T

Keywords: Aquaculture Cadmium Fishmeal substitute Mercury Tilapia Tuna byproduct

Potentiality of the use of tuna byproducts as a fish-meal replacement on Nile tilapia (Oreochromis niloticus) was examined for 84 weeks by tracking the concentrations of cadmium and mercury in the internal organs, muscles and fish whole body through generation including their immature eggs and their larvae. The results confirmed that the tuna byproducts can be used as a fish-meal substitute in tilapia aquaculture, because their acceptable ranges for cadmium and mercury consequently did not exceed the food safety values (both < 0.5 mg kg−1), despite their proportional increases in the fish body. The use of tuna byproducts as a protein source is expected to reduce the cost of feed with other fishmeal substitutes in tilapia aquaculture. However, fish (flounder) indiscriminately consuming tuna byproduct feed were prohibited and recalls of sales were issued by the government (July 2018, Republic of Korea), as the threshold for mercury in the fish bodies had been exceeded (0.6–0.8 mg kg−1). Further study of the use of tuna byproducts as fishmeal replacements for other species in aquaculture is needed, as concentration ratios can vary depending on the species.

1. Introduction Throughout the history of humankind, there has been a populationdriven and technology-supported expansion of the use of the world’s oceans as sources of protein. Humans directly consume two-thirds of this protein, the remainder being utilized as fodder including fish byproducts (Cashion et al., 2017; Merino et al., 2012; Watson et al., 2015). Such fish byproducts (solid and liquid wastes), generally mixes of head, bones, viscera, gills, dark muscle, tail, fin and skin, are a potential source of high-value-added components conventionally employed to produce fish oil, fishmeal, fertilizer, and fish silage, including profitable bioactive compounds for human consumables (i.e., bioactive peptides, oligosaccharides, fatty acids, enzymes, water-soluble minerals, biopolymers and pharmaceutical applications) (Choudhury and Bublitz, 1996; Choudhury and Gogoi, 1995; Guérard, 2007; Kim and Mendis, 2006). Tuna, widely distributed throughout tropical and temperate waters, is an important contributor to food security and income in both developed and developing countries. Catches of commercially important tuna-like species such as skipjack (Katsuwonus pelamis), yellowfin (Thunnus albacares), bigeye (T. obesus) and albacore (T. alalunga)

⁎

amounted to almost 7.7 million tons (4.6% of global total capture fishery and aquaculture production: 167.2 million tons) (FAO, 2016; Gamarro et al., 2013; Pons et al., 2017) in 2014. The solid wastes generated by the tuna canning industry, which can be as high as 65% of the original material, also have been utilized, especially as high-value fish byproducts (Gamarro et al., 2013; Guerard et al., 2002). However, caution is required in the use of tuna byproducts, as tuna and tuna-like species, unlike other fish, accumulate large amounts of heavy metals, especially cadmium and mercury (methyl-mercury), in their organs and muscles. These toxins exert damaging effects such as minamata (MOE, 2002; Normile, 2013) and itai-itai (Morrow, 2010; Nogawa et al., 2004) disease, and can be exceptionally harmful to humans. In some instances, tuna catches with total heavy metal contents exceeding the maximum limits recommended by the FAO/WHO have been banned from human consumption (Voegborlo et al., 1999; WHO, 1972). For this reason, certain tuna byproducts are earmarked not for direct utilization (i.e., as oil, hydrolysate and flavor powders for cooking juice, and as enzymes) but rather for indirect utilization (i.e., as tuna meal and silage for cattle/poultry/pet food manufacturers), protein hydrolysate being a potential source of bioactive peptides in aquaculture

Corresponding authors. E-mail addresses: [email protected] (J.-Y. Jung), [email protected] (S.C. Bai).

https://doi.org/10.1016/j.ecoenv.2019.01.107 Received 22 October 2018; Received in revised form 29 January 2019; Accepted 30 January 2019 0147-6513/ © 2019 Elsevier Inc. All rights reserved.

Ecotoxicology and Environmental Safety 172 (2019) 364–372

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(Gamarro et al., 2013). In aquaculture systems, fish feeds account for the highest operating costs, protein being the most expensive diet; and the highest-cost and most conventional protein source of fish feeds is fish meal (Munguti et al., 2012; Tacon, 1993). Research for development of a fish-meal substitute that can reduce feed costs has considered other, animalprotein sources (i.e., meat meal, meat and bone meal, blood meal, poultry-byproduct meal, feather meal and insect meal) or plant-protein sources (i.e., soybean meal, cotton-seed meal, gluten meals and oilseed plant byproducts such as sunflower seeds, rapeseeds, sesame seeds, etc.) (Biswas et al., 2017; Cai et al., 2017; Cummins et al., 2017; GonzálezRodríguez et al., 2016; Kirimi et al., 2016; Moutinho et al., 2017; Ngugi et al., 2017; Sun et al., 2016; Wang et al., 2017) or fish byproducts, due to its advantageous amino acid profile and essential-fats-enriched oils. Several studies utilizing tuna byproducts of relatively low protein contents (but variable depending on the manufacturing process (Gamarro et al., 2013)) have been also carried out in aquaculture (Chotikachinda et al., 2018; Ezquerra et al., 1999, 1998, 1997a, 1997b; Goddard et al., 2008; Goytortúa-Bores et al., 2006; Gümüş et al., 2011, 2009; Hernández et al., 2014, 2011, 2013; Hernández and OlveraNovoa, 2017; Hernandez et al., 2004; Jeon et al., 2014; Kim et al., 2014, 2018; Oncul et al., 2018; Saïdi et al., 2010; Sookying et al., 2013; Tekinay et al., 2009; Terrazas-Fierro et al., 2010; Uyan et al., 2006; Villarreal et al., 2006), due to cheapness compared with conventional fish byproducts (anchovy, herring, menhaden, salmon, white fish (NRC, 2011)). However, the data are considered to be insufficient for rationalization or generalization of the safety of using tuna byproducts, for two reasons: the lack of information on heavy metals that can accumulate in the human body (only tuna cans have been studied (Ababneh and Al-Momani, 2013; Abolghait and Garbaj, 2015; Afonso et al., 2015; Alcala-Orozco et al., 2017; Andayesh et al., 2012, 2015; Aya-Ay et al., 2012; Burger and Gochfeld, 2004; Cappon and Smith, 1982; Dabeka et al., 2014; de Paiva et al., 2017; Emami Khansari et al., 2005; Ganjavi et al., 2010; Gerstenberger et al., 2010; Hashemi-Moghaddam et al., 2011; Higham and Tomkins, 1993; Hospido et al., 2006; Hosseini et al., 2015; Ikem and Egiebor, 2005; Inasmasu et al., 1986; Kumar, 2018; Mahalakshmi, 2012; Mol, 2011; Okyere et al., 2015; Pappalardo et al., 2017; Pourjafar et al., 2014; Rahimi and Behzadnia, 2011; Rahimi et al., 2010; Rasmussen and Morrissey, 2007; Ruelas-Inzunza et al., 2011; Russo et al., 2013; Saidi et al., 2013; Shim et al., 2004; Sobhanardakani, 2017; Tuzen and Soylak, 2007; Vieira et al., 2017; Voegborlo et al., 1999)), and the short evaluation periods of the relevant studies. In the present study, we examined the potentiality of the use of tuna byproducts as a fish-meal replacement by tracking the concentrations of cadmium and mercury in the fish body, internal organs and muscle through generation (second-generation fish, G2) including their immature eggs (G2) and larvae (third generation, G3, 10 days post hatching), and determined the effects on growth performance as an insertion experiment. The present study aims to identify the concentration of heavy metals (cadmium and mercury). Nile tilapia (Oreochromis niloticus), one of the most cultivated freshwater fish in the world and fastest-growing aquaculture products, was used as the subject animal. Fish also contain other heavy metals such as arsenic and lead, in concentrations 10 times higher than that of mercury; however, because most arsenic forms are readily excreted in urine, and lead’s sources, such as mineral salts and bone meal, are widespread (Bugdahl and Jan, 1975; Dorea, 2004; Juresa and Blanusa, 2003; Vahter, 1994), they were not considered in this study.

Table 1 Formulation of tuna byproduct diets (TBM 40% and 70%) and proximate chemical compositions of tuna byproduct meal (TBM) and experimental diets (C.F, TBM 40% and 70%). Ingredient TBM

a

Experimental diets C.Fb

TBM 40%

TBM 70%

– – – – – –

400 270 260 30 20 20

700 – 260 – 20 20

−1

Ingredients (g kg ) Tuna by product meala (TBM) Soybean mealc Wheat flourd fish oile Vitamin premixf Mineral premixg Proximate analysis (%)h Dry matter Crude protein Crude lipid Ash

92.9 68.3 12.06 17.4

91.2 52.13 7.84 13.0

90.7 44.82 9.47 10.8

91.3 50.64 9.23 12.4

a

Tuna by product meal: Ottogi SF Co. Ltd., Republic of Korea. Commercial feed containing 52% protein and 8% lipid, Republic of Korea. c Soybean meal: CJ CheilJedang Corporation, Republic of Korea (crude protein, 54%; crude lipid, 3.78%; ash, 7.02%). d Wheat flour: Goyang, Republic of Korea. e Feed oil for seawater fish: Ewha Oil & Fat Industial Co. Ltd, Republic of Korea. f Contains (as mg kg−1 in diets): Ascorbic acid, 300; dl-Calcium pantothenate, 150; Choline bitate, 3000; Inositol, 150; Menadion, 6; Niacin, 150; Pyridoxine·HCl, 15; Rivoflavin, 30; Thiamine mononitrate, 15; dl-α-Tocopherol acetate, 201; Retinyl acetate, 6; Biotin, 1.5; Folic acid, 5.4; Cobalamin, 0.06. g Contains (as mg kg−1 in diets): NaCl, 437.4; MgSO4·7H2O, 1379.8; ZnSO4·7H2O, 226.4; Fe-Citrate, 299; MnSO4, 0.016; FeSO4, 0.0378; CuSO4, 0.00033; Calciumiodate, 0.0006; MgO, 0.00135; NaSeO3, 0.00025. h Dry matter basis. b

Use Committee (IACUC) of Pukyong National University. 2.1. Experimental diets (tuna byproduct meal, TBM) Tuna byproduct meal (TBM, Ottogi SF Co. Ltd., Republic of Korea) containing 68.3% protein and 12.06% lipid was utilized as a replacement for fishmeal (TBM 40% and 70%, respectively) (Table 1). This tuna byproduct meal along with soybean meal was used as the protein source, and wheat flour and soybean oil were used as the carbohydrate and lipid sources, respectively. The relevant preparation steps were as follows: ⑴ 50%-humidity feed dough for each diet was covered with aluminum foil (Samjin Co., Republic of Korea); ⑵ the diets were heattreated in a convection oven (DAIHAN Scientific Co. Ltd., Republic of Korea) for 30 min at 100 °C; ⑶ they were then dried over the course of 24 h, at 20 °C in an air-conditioned room, to an approximately 8.6 – 9.2% moisture level; ⑷ the diets were well mixed with a blender (Charmingart Co. Ltd., Republic of Korea), ⑸ pelletized by a pelletextruder (Baokyong Commercial Co., Republic of Korea), and ⑹ finally stored at − 20 °C until use. 2.2. Fish and rearing conditions Six hundred and thirty-two (632) juvenile tilapia (initial body weight, 10.2 g, first-generation fish, G1) obtained from a local fish farm (Changnyeong, Republic of Korea) were distributed between two 2400 L plastic tanks (water volume: 2000 L). A commercial diet containing 52% protein and 8% lipid was supplied for G1, and the fish were fed three times daily (9:00, 13:00, 17:00) by satiation for 41 weeks until they reached a body weight over 500 g, and a selection process was conducted every eight weeks for intensive breeding. To produce second-generation fish (G2), 100 fish of G1 randomly selected (220 – 280 g; male 30, female 70) during rearing G1 were distributed to another, 2400 L plastic tank (same volume as first two tanks: 2000 L)

2. Materials and methods In general, the analyses were performed with a minimum of triplicates. Commercial feed-fed fish (C.F, Table 1) from storage tank were used for relative comparisons of the fish body composition. The experimental protocol was followed by the Institutional Animal Care and 365

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was placed in a teflon bomb with 10 mL of nitric acid (60 – 61%) added, and was reacted at room temperature for 150 min. The Teflon decomposer was sealed and heated at 150 °C for 600 min on a heating plate until it became a yellowish clear solution. The solution was evaporated to a concentration of 1 mL of nitric acid at 100 °C., followed by dissolution in 2% nitric acid, filtration and purification (100 mL), after which it was used as a pretreatment sample for analysis.

within which an autotrophic biofloc technology (ABFT) system utilizing microalgae (Jung et al., 2017) was maintained; concentration of Chlorella vulgaris for inoculum was 0.025 g L−1 under a 16-h light, 8-h dark photoperiod cycle at 28 °C, fish were fed 3 times at a rate of 1 – 2% of wet body weight per day, and on the 15th day, larvae (G3) carefully collected were distributed into six 150 L plastic tanks (water volume: 100 L). Commercial crumble feed containing 42% protein and 7% lipid (Frippak Ultra, Myung Sun, Republic of Korea) was provided for 5 weeks until the larvae (G2) weighed 11 g. For the main, tuna-byproduct-diet experiment (TBM 40% and 70%), 240 juvenile (G2) fish randomly selected from the 150 L tanks were distributed evenly between another two 2400 L plastic tanks (same volume, 120 fish in each tank) and reared for 38 weeks at a rate of 2 – 3% for 21 weeks (< 200 g) and 0.87 – 0.91% for 17 weeks ( > 200 g) of wet body weight per day until they reached a body weight of over 500 g including selection process one time for intensive breeding. Each tank was controlled by our circulating filtration system: the water was 30% replaced daily; constant aeration was provided by air stones placed on the bottom of the tanks to maintain the oxygen level; the water temperature was maintained between 25.1 and 25.4 °C under a 16-h light, 8-h dark photoperiod cycle.

2.7. Mercury analysis The total mercury concentration in the samples (internal organs, muscle, whole body, immature eggs yolk and fry) was measured by automatic direct mercury analyzer (DMA-80, Milestone, Italy, > ppb) (Lin et al., 2010). In the DMA-80, the sample (0.1 g) was run through an initial drying step at 300 °C and then decomposed at 850 °C. The resulting Hg vapor was trapped on a gold amalgamator and subsequently desorbed for quantitation. The released Hg vapor was measured by atomic absorption spectrophotometry at a wavelength (k) 253.70 nm. 2.8. Statistical Analysis After confirming the normality and homogeneity of variance, all of the data were analyzed by one-way ANOVA (Statistix 3.1; AnalyticalSoftware, St. Paul, MN, USA) to test the effects of the treatments. When a significant treatment effect was observed, an LSD test was applied to compare the means. The treatment effects were considered at the 5% level of significance (P < 0.05). Broken-line linear regression analysis was applied to predict further accumulation of total mercury in muscle of tilapia with size of more than 500 g.

2.3. Proximate composition analysis A proximate composition analysis was performed using the standard AOAC methods (AOAC, 1995). Preparatorily, samples were freeze-dried for 48 h. The moisture contents were determined by means of a dry oven at 105 °C, and the ash contents by combustion at 550 °C. The crude protein was analyzed by the Kjedahl method, and the crude lipid was analyzed by soxhlet extraction using the soxhlet system 1046 (Tacator AB, Sweden) (Folch et al., 1956).

3. Results and discussion

2.4. Amino acid analysis

3.1. Evaluations of tuna byproducts as fish meal

Samples of tilapia were freeze-dried for amino acid (AA) analysis (Li et al., 2013). A total of 0.02 g of samples was hydrolyzed with 15 mL of 6 N HCl at 110 °C for 24 h. The hydrolyzed samples in distilled water within a 50 mL flask were evaporated and recovered in sodium citrate buffer (0.2 N, pH 2.2). After filtration (0.2 µm), the samples were analyzed with ninhydrin at 570 nm and 440 nm using a S433 amino acid analyzer (Sykam, Gilching, Germany, > ppm). For methionine and cystine hydrolysis, performic acid was used in place of 6 N HCl.

The growth performance and feed efficiency data on tilapia fed with either of two tuna byproduct diets (TBM 40% and 70%) are provided in Table 2. According to the results of this study, the overall values of weight gain (WG), feed efficiency ratio (FE), protein efficiency ratio (PER), and specific growth rate (SGR) were not significantly different Table 2 Growth performance and feed efficiency of tilapia fed with tuna byproduct diets (TBM 40% and 70%) at the end of the 21 weeks (< 200 g) and 17 weeks (> 200 g) experiments. Values are means from triplicate groups of fish where the values with different superscripts are significantly different (P < 0.05).

2.5. Fatty acid methyl ester analysis Freeze-dried muscle powder was treated with chloroform/methanol (2:1, v/v), and lipids were determined using the modified Folch method (Folch et al., 1956). Methanol and sulfuric acid were added and then incubated at 100 °C for 20 min for fatty acid methyl ester (FAME) conversion. Heptadecanoic acid was used as an internal standard. The organic phase was separated by 0.3 M NaOH, then recovered with centrifugation at 4000 rpm for 10 min. FAMEs were measured by gas chromatography (HP 6890, Agilent, USA, > ppm) with a flame-ionized detector. The FAME content was calculated as follows:

Initial mean weight (g fish−1) Initial number (fish tank−1) Final mean weight (g fish−1) WG (%)1 FE (%)2 PER3 SGR (%/day)4 Survival (%)5

FAME content(%, w/w) weightofFAMEobtainedaftertransesterification = × 100 weightoffishwholebody

Fish size < 200 g (21 weeks)

Fish size > 200 g (17 weeks)

TBM 40%

TBM 70%

TBM 40%

TBM 70%

11.0

11.1

227.8

217.7

120

120

50

50

192.7

195.0

397.8

1645.5 121.1 2.60 1.95 100

1650.5 122.6 2.18 1.95 100

74.7 88.4 1.89 0.47 100

b b b b

b

441.0

a

102.6 a 116.0 a 2.06 a 0.59 a 100

1 Weight gain (WG, %) = (final weight – initial weight) × 100 / initial weight. 2 Feed efficiency ratio (FE, %) = (wet weight gain / dry feed intake) × 100. 3 Protein efficiency ratio (PER) = wet weight gain / protein intake. 4 Specific growth rate (SGR, %/day) = (loge final weight - loge initial weight) × 100 / days. 5 Survival rate (%) = (initial total fish – dead fish) × 100 / initial total fish.

2.6. Cadmium analysis The total cadmium concentration in the samples (internal organs, muscle, whole body, immature eggs yolk and fry) was measured by inductively coupled plasma mass spectrometry (ICP-MS, Perkin-Elmer Optima 2000DV, Shelton, CT 06484 USA, > ppm). The sample (1 g) 366

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Table 3 Whole-body proximate composition of tilapia fed with commercial feed (C.F) and tuna-by product diets (TBM 40% and 70%) at different sizes of tilapia (%) 200 g C.F Moisture Crude protein Crude lipid Ash

300 g

2

40% b

70% b

C.F d

72.93 15.73 c 5.11 d 4.58 b

73.44 15.95 b 5.94 a 4.67 c

400 g

71.06 15.21 b 5.93 b 4.50 c

40% b

70% c

73.64 15.32 d 5.30 c 5.31 b

72.07 16.84 a 5.61 b 4.02 d

40% a

75.12 14.94 c 5.02 c 4.67 b

.

500 g

C.F a

1,3

70% d

74.43 15.76 c 5.59 b 4.34 d

C.F b

71.34 15.67 c 5.75 a 5.86 a

40% c

72.20 15.13 bc 6.16 a 5.64 a

70% a

72.04 16.94 a 4.72 d 5.55 a

71.77 c 16.67 a 5.87 b 4.69 b

73.57 15.89 b 5.30 c 4.27 c

1

Wet weight basis. Commercial feed containing 52% protein and 8% lipid, Republic of Korea. 3 Statistical analysis was performed by weight comparison within each diets. Values are means from triplicate groups of fish where the values with different superscripts are significantly different (P < 0.05). 2

levels of tuna byproduct diets are provided below (Table 4). Consistently with previous studies on the use of tuna byproduct meal as fish meal in aquaculture (Goddard et al., 2008; Hernández et al., 2011, 2013; Jung et al., 2016; Saïdi et al., 2010; Uyan et al., 2006), our results indicated high contents of arginine, leucine, lysine, aspartic acid, glutamine, glycine and alanine in TBM. The dominant amino acids in the whole-body weights of the tilapia fed with the tuna byproduct diet (TBM 70%, 200–500 g fish, Table 4 and S1) were the same as those for TBM (ingredient); however, after rearing, the contents of methionine, glycine and cysteine were increased whereas those of histidine, isoleucine, leucine, phenylalanine, threonine, valine and tyrosine were decreased. The fatty acids compositions in the tuna byproduct diets (% g−1) and in the muscles of the tilapia fed with commercial feed and different levels of tuna byproduct diets (% total fatty acids−1) are provided below (Table 5). High contents of palmitic acid (C16:0), oleic acid (C18:1n9) and docosahexaenoic acid (C22:6n3, DHA) were detected in the TBM, which results is similar to those of previous studies on the use of tuna byproduct meal in aquaculture (de Oliveira et al., 2016; Gopakumar and Nair, 1972; Howe et al., 2002; Li et al., 2017; Mourente et al., 2002; Muhamad and Mohamad, 2012; Nakamura et al., 2007; Suseno, 2015; Wheeler and Morrissey, 2003). The dominant fatty acids

between the two diets (< 200 g, Table 2) even though the protein content (Table 1) of the TBM 70% (50.64%) diet was higher than that of the 40% diet (44.82%). This supports the Recommended (Estimated) Dietary Protein Level (%) in Diets according to Fish Weight theory’s contention (NRC, 2011) that the correlation between fish growth and protein content in diet is not always proportional (44.82% at TBM 40% in the present study). Contrastingly, in growth above that weight (> 200 g, Table 2), the values of WG, FE, PER, and SGR were significantly different (higher) for the TBM 70% than for the TBM 40% diet, which will be reasonable to be interpreted in terms of fish growth rate (according to the types or properties of proteins affecting digestibility) rather than in terms of protein content. The total protein and lipid contents in the tilapia whole body (200 – 500 g) ranged from 14.94 to 16.94 and from 4.72% to 6.16%, respectively (Table 3). The protein / lipid content ranges for each group were 15.32 – 16.94 / 4.72 – 5.94% with commercial feed, 15.67 – 16.84 / 5.11 – 5.75% with TBM 40% (mixed with tuna byproduct meal and soybean meal), and 14.94 – 16.67 / 5.02 – 6.16% with TBM 70%, which values were within the ranges of other studies (> 200 g, Nile tilapia) (El‐Sayed, 1998; Mugo-Bundi et al., 2015; Ngugi et al., 2017). The amino acids compositions of the ingredients, diets and wholebody weights of the tilapia fed with commercial feed and different

Table 4 Amino acids compositions of tuna byproduct meal (TBM), experimental diets (C.F, TBM 40% and 70%) and whole body of tilapia fed with commercial feed (C.F) and tuna-by product diets (TBM 40% and 70%) for different sizes of tilapia (%)1,3. Ingredient

200 g

2

C.F

40%

70%

C.F

4.10 2.84 3.19 5.15 5.36 0.37 0.92 2.88 4.75 3.15 3.61

3.89 2.37 2.41 4.19 4.45 1.25 2.36 2.44 3.91 2.29 2.92

3.10 1.69 2.24 3.62 3.28 0.94 1.08 2.14 3.53 2.04 2.47

3.54 2.18 2.80 4.55 4.51 0.24 0.71 2.48 4.26 2.63 3.18

3.83 1.64 2.33 4.03 4.46 1.56 2.73 2.20 3.81 2.49 2.60

b

6.39 2.63 8.65 3.23 4.35 4.40 1.87 0.55

5.85 2.39 8.77 3.22 3.81 3.47 1.47 1.11

4.75 2.01 7.92 2.59 2.71 2.67 1.39 0.79

5.56 2.27 8.37 3.14 3.46 3.63 1.78 0.47

5.76 2.30 8.16 3.16 4.90 3.81 1.60 1.17

b

TBM Essential amino acids Arginine Histidine Isoleucine Leucine Lysine Methionine Methionine + cysteine Phenylalanine Phenylalanine + tyrosine Threonine Valine Non-essential amino acids Aspartic acid Serine Glutamic acid Proline Glycine Alanine Tyrosine Cysteine

Experimental diet

300 g 40%

b

b

a

a

ab b c b b a

70%

3.63 1.95 2.25 3.83 4.61 1.39 2.49 2.10 3.49 2.45 2.54

a

5.24 2.22 7.75 3.16 4.00 3.44 1.39 1.10

a

a a a a

a a a a a

a a

c bc

C.F

3.39 1.79 2.09 3.61 4.31 1.36 2.42 1.97 3.24 2.32 2.39

b

4.93 2.09 7.36 2.94 3.99 3.36 1.27 1.06

b

1

a b b b ab a b b b b

b b

c b b

400 g 40%

4.06 1.76 2.37 4.06 4.44 1.55 2.70 2.22 3.65 2.58 2.67

a

6.22 2.38 8.27 3.67 5.70 4.08 1.43 1.15

a

ab

b

ab

ab

a ab ab a ab b

70%

3.78 1.74 2.16 3.76 4.55 1.42 2.47 2.06 3.37 2.44 2.46

a

5.23 2.24 7.79 3.25 5.06 3.77 1.31 1.05

a

b a a a

a a ab a a

a a

a a

C.F

4.01 1.81 2.43 4.12 5.00 1.50 2.61 2.23 3.77 2.60 2.67

a

5.62 2.33 8.61 3.22 4.67 3.87 1.55 1.12

a

a a a a a a a a a a

a a

ab a a

500 g 40%

3.89 1.73 2.28 3.91 4.28 1.52 2.63 2.12 3.45 2.51 2.58

b

5.93 2.23 8.09 3.44 5.47 3.91 1.33 1.12

ab

ab

b

ab

b

b b b a ab bc

70%

3.68 1.67 2.14 3.62 4.34 1.36 2.39 2.02 3.30 2.32 2.43

a

4.98 2.07 7.57 3.23 4.88 3.62 1.27 1.04

a

bc a b a

ab ab b a a

ab a

a ab

C.F

3.48 1.55 1.98 3.38 4.03 1.34 2.37 1.85 3.08 2.13 2.24

b

4.61 1.98 7.09 3.01 4.89 3.48 1.23 1.04

b

b b c b ab ab b bc c b

b bc

a b bc

40%

4.14 1.86 2.31 3.98 4.87 1.43 2.46 2.22 3.47 2.47 2.64

a

6.14 2.30 8.40 3.80 5.78 4.10 1.25 1.02

a

a

a

b

b

ab a a a a c

70%

3.42 1.54 1.86 3.21 3.94 1.30 2.25 1.79 3.01 2.05 2.16

b

4.44 1.93 6.68 3.10 4.62 3.28 1.22 0.95

b

c b c b

b b c b b

b b

b c

3.37 1.66 1.94 3.22 4.14 1.19 2.10 1.83 2.93 2.16 2.23

b

4.60 1.95 6.90 2.99 4.50 3.30 1.10 0.91

b

ab b c b b b b c bc b

b c

b b c

Dry matter basis. Commercial feed containing 52% protein and 8% lipid, Republic of Korea. 3 Statistical analysis was performed by weight comparison within each diets. Values are means from triplicate groups of fish where the values with different superscripts are significantly different (P < 0.05). 2

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Table 5 Fatty acids compositions of tuna byproduct diets (TBM 40% and 70%), tuna byproduct meal (TBM) and muscles of tilapia fed with commercial feed (C.F) and tuna-by product diets (TBM 40% and 70%) for different sizes of tilapia (%) 7. Experimental diet1

Ingredient2

Tilapia muscle

b

200 g 40% C14:0 C16:0 C16:1 C18:0 C18:1n9 C18:2n6 C18:3n3 C20:4n6 C20:5n3 C22:6n3 Others SFA4 MUFA5 PUFA6

0.13 1.25 0.16 0.41 0.90 1.12 0.12 – 0.11 0.63 0.77 2.20 1.06 1.98

70% 0.15 1.23 0.18 0.44 0.65 0.31 – – 0.13 0.97 0.33 1.94 0.84 1.11

TBM 3.86 27.95 5.58 9.80 14.76 0.60 – 2.16 3.91 23.21 8.17 41.61 20.34 29.88

C.F3

300 g 40%

b

2.00 23.83 c 4.89 b 10.60 c 19.07 b 10.89 b – – – 13.99 c 14.79 a 36.45 b 23.96 b 24.88 c

70% a

3.09 28.44 a 4.73 a 9.32 a 22.96 a 9.94 d – – – 11.27 d 10.25 b 40.85 a 27.69 a 21.21 c

C.F c

1.97 28.34 a 6.48 a 8.41 ab 24.95 a 5.17 d – – – 13.75 b 10.93 a 38.72 a 31.43 a 18.92 c

400 g 40%

c

1.22 26.34 a 2.75 c 12.02 b 18.95 b 9.69 c – – – 16.25 b 12.78 c 39.58 a 21.70 c 25.94 b

– 24.30 c 3.78 b 9.23 a 21.29 b 13.32 b – – – 15.99 a 12.09 a 33.53 c 25.07 c 29.31 a

70%

C.F ab

2.99 24.49 d 5.96 b 7.17 c 25.11 a 11.96 a – 0.63 b – 12.95 c 8.74 c 34.65 c 31.07 b 25.54 a

500 g 40%

a

3.64 24.69 bc 5.49 a 9.23 d 21.17 a 11.57 a – – – 11.79 d 12.74 c 37.56 b 26.66 a 23.36 d

70% b

1.85 25.44 b 4.56 a 9.11 a 22.46 a 12.59 c – – – 14.08 c 9.91 b 36.40 b 27.02 b 26.67 b

C.F b

2.86 25.66 c 5.64 b 8.19 b 23.91 b 8.20 c – 0.74 b – 14.82 a 9.98 b 36.71 b 29.55 c 23.76 b

– 25.51 ab – 13.48 a 14.08 c 8.46 d – – – 24.25 a 14.22 b 38.99 a 14.08 d 32.71 a

40%

70% c

1.14 25.04 b 4.77 a 8.04 b 22.76 a 14.05 a – – – 15.14 b 9.06 c 34.22 c 27.53 ab 29.19 a

3.21 a 26.50 b 5.71 b 8.67 a 25.49 a 9.73 b – 1.31 a – 12.79 c 6.59 d 38.38 a 31.20 ab 23.83 b

1

Dry matter basis. % of total fatty acids. 3 Commercial feed containing 52% protein and 8% lipid, Republic of Korea. 4 Saturated fatty acid. 5 Monounsaturated fatty acid. 6 Polyunsaturated fatty acid. 7 Statistical analysis was performed by weight comparison within each diets. Values are means from triplicate groups of fish where the values with different superscripts are significantly different (P < 0.05). 2

in the muscles of the tilapia fed with the tuna byproduct diet (TBM 70%, 200 – 500 g fish, Table 5 and S2) were the same as those for TBM, but after rearing, the contents of the other fatty acids were increased, except for arachidonic acid (C20:4n6, ARA), eicosapentaenoic acid (C20:5n3, EPA) and docosahexaenoic acid (C22:6n3, DHA). The detection of arachidonic acid (C20:4n6, ARA, > 300 g), along with the explosive increase in linolenic acid (C18:2n6), the non-detection of eicosapentaenoic acid (C20:5n3, EPA) and the changes in the fatty acid distribution (SFA > MUFA > PUFA, after rearing) relative to TBM (SFA > PUFA > MUFA, ingredient) are interesting results (Table 5 and S2). The concentrations of total cadmium and mercury in the ingredients, diets and internal organs, muscles, whole body, immature eggs, and larvae of tilapia fed with different levels of tuna-by product diets are listed (Table 6). Both cadmium and mercury were detected in all of the experimental groups, and the accumulation rate increased in proportion to tilapia size. Cadmium in tilapia was the most concentrated in the internal (internal organs > muscle), as earlier studies have reported (Abdel-Tawwab and Wafeek, 2014; Ekpo et al., 2008; Etesin and Benson, 2007; Kargın and Çoğun, 1999; Pelgrom et al., 1995; Rashed, 2001) and its concentration ratio was from 0.023 to 0.247 mg kg−1. However, mercury, unlike cadmium, was found to be the most concentrated in the muscles (muscle > internal organs) and its concentration ratio was from 0.033 to 0.127 mg kg−1. On this basis, it was confirmed that the primary use of tuna byproducts as a fish-meal substitute is possible, as the concentration of cadmium and mercury (precisely methyl mercury, less than 60% of total mercury concentrations (Carbonell et al., 2009; Drevnick and Sandheinrich, 2003; Harris et al., 2003; Jagtap et al., 2011)) in the fish body did not exceed the limit for heavy metals in fish (both < 0.5 mg kg−1) (Nauen, 1983). Considering that the maximum weight of tilapia is 4.323 kg, the corresponding mercury content levels (muscle/fillet) are 0.464 (TBM 40%) and 0.697 (TBM 70%) mg kg−1, respectively (Fig. 1). However, these figures are likely to be significantly lower, considering that the market size of tilapia ranges from 250 g (0.06 – 0.09 mg kg−1) to 450 g (0.08 – 0.152 mg kg−1). These are also safe levels compared to those of other commercial aquatic products; scorpionfish (0.233 mg kg−1),

Table 6 Concentrations of cadmium and mercury in tuna byproduct meal (TBM) and experimental diets (TBM 40% and 70%) as well as internal organs, muscles, whole body, immature eggs, and larvae of tilapia fed with TBM 40% and 70% 5.

1

Ingredient Experimental diet1 Tilapia Internal organs2,4

Muscle2

Whole body2

TBM TBM 40% TBM 70% Fish size 200 g 300 g 400 g 500 g 200 g 300 g 400 g 500 g 200 g 300 g 400 g 500 g

Immature eggs3 Larvae (10 days post hatching)3

Cadmium

Mercury

0.99 0.40 0.69 TBM 40% 0.085 a 0.100 b 0.158 c 0.170 d – – – 0.023 – – – – – 22.37

0.199 0.079 0.139 TBM 40% 0.033 a 0.038 a 0.053 b 0.064 c 0.057 a 0.075 b 0.077 b 0.089 c 0.071 c 0.054 a 0.062 b 0.058 ab 6.71 43.82

TBM 70% 0.120 a 0.147 b 0.223 c 0.247 d – – – 0.050 – – – 0.033 51.55 67.12

TBM 70% 0.038 a 0.047 b 0.056 c 0.069 d 0.084 a 0.087 a 0.108 b 0.127 c 0.056 a 0.108 c 0.075 b 0.050 a 15.05 49.28

Dry weight basis (mg kg−1). Wet weight basis (mg kg−1). 3 Wet weight basis (µg kg−1). 4 Internal organs: liver, pyloric caeca, spleen, stomach, intestine, gonad, air bladder and kidney. 5 Statistical analysis was performed by weight comparison within each diets. Values are means from triplicate groups of fish where the values with different superscripts are significantly different (P < 0.05). 1 2

weakfish (sea trout, 0.235 mg kg−1), halibut (0.241 mg kg−1), and Spanish mackerel (0.454 mg kg−1) (FDA, 2012). Therefore, the risk to humans is considered to be low, even if tuna byproducts are utilized as a fish-meal substitute in tilapia aquaculture. However, the concentrations of mercury and cadmium contained in tuna by-product feeds should always be monitored, because they can be fluid during its manufacturing process, as mentioned in the 368

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4. Conclusion The objective of this study was to identify the concentration of heavy metals (cadmium and mercury) when tuna byproducts are used as a fish-meal substitute. As a result, tuna byproducts were confirmed to be safe for use as fish meal in tilapia aquaculture, as their levels of cadmium and mercury did not exceed food safety values, despite their proportional increases in the fish body sizes. An additional experiment between commercial and tuna byproduct feed should be performed in order to confirm growth efficiency outcomes. Overall, the use of tuna byproducts as a protein source in tilapia aquaculture is expected to reduce the cost of feed products with other fishmeal substitutes. Acknowledgments This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. The authors would like to extend our sincere thanks to the Feeds & Foods Nutrition Research Center (FFNRC, Pukyong National University), Aqua-k (an aqua-feed company) and Is-tech (a software and scientific equipment company).

Fig. 1. Broken-line regression analysis based on total mercury content in muscle/fillet of Nile tilapia (Oreochromis niloticus) with different fish size fed tuna byproducts diets with TBM 40% and 70%.

introduction.

Conflict of interest statement 3.2. Safety of tuna byproducts as fish meal The authors declare they have no conflicts of interest. Tuna byproducts were confirmed safe for use as fish meal in tilapia aquaculture, because they did not affect the overall growth performance (including fish body composition), and their acceptable ranges for cadmium and mercury consequently did not exceed the food safety values, despite their proportional increases in the fish body. However, blind faith in standard values such as maximum residue levels (MRL), acceptable daily intake (ADI), estimated daily intake (EDI) or acute reference dose (ARfD) (ANVISA, 2016; CAC, 2017; FAO/ WHO, 2009) should be avoided, because the criteria are only relative indicators calibrated according to internal and external environmental factors: race, sex, age, region and time lapse. Since the onset of minamata by mercury (1956) and itai-itai by cadmium (1968) disease syndromes, research related to their potential impacts on humans has continued (Aoshima, 2016; Nishijo et al., 2017; Nogawa et al., 2017; Takahashi et al., 2017; Yorifuji and Kashima, 2016; Yorifuji et al., 2017). Studies on radionuclides resulting from the accidents at the Chernobyl (1986) and Fukushima (2011) nuclear power plants likewise are ongoing (Belharet et al., 2016; Hayama et al., 2017; Men et al., 2017; Merz et al., 2015), even after reports of results claimed to be nonthreatening to humans. Similarly, in the wake of the 2017 egg scandal involving 40 countries, studies on the fipronil insecticide (MedicalXpress, 2017; Polet, 2017) and other such chemicals (Goff et al., 2017; Hamid et al., 2017; Haque et al., 2017; Mahugija et al., 2017; Parente et al., 2017; Thompson et al., 2017) continue, notwithstanding the insistence that there is no threat to human health and that the risk to consumers is very low. Although this might seem somewhat contradictory, such studies, including the present one, are just the minimal precautions for the defense of human health and welfare. Aquaculture in modern society has been emphasized with the considerable population increase to offset shortages of aquatic products by fisheries, and the use of aquatic byproducts has been attempted as an aspect of eco-friendly and sustainable aquaculture technology currently under study (FAO, 2014). However, fish (flounder) indiscriminately grown by tuna byproduct feed were prohibited, and products have been recalled by the government (July 2018, Republic of Korea), as the safety threshold of mercury content in the fish bodies was exceeded (0.6–0.8 mg kg−1). Tuna byproducts, therefore, should be carefully utilized, and thorough monitoring, inspection and verification systems must be established and faithfully followed. Further study of the use of tuna byproducts as fishmeal replacements for other species in aquaculture is needed.

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