Dietary replacement of fish meal by defatted and fermented soybean meals with taurine supplementation for pompano fish: effects on growth performance, nutrient digestibility, and biological parameters in a long-term feeding period

Abstract

A 16-wk growth trial was conducted to examine the effects of dietary replacement of fish meal by defatted soybean meal (SBM) and fermented soybean meal (FSBM) with taurine supplementation on growth performance, nutrient apparent digestibility coefficient (ADC) and biological parameters of pompano fish. The FSBM was produced by fermenting SBM with Lactobacillus spp. Seven isonitrogenous and isoenergetic diets were formulated to replace 35% or 50% of fish meal by SBM or FSBM with taurine supplementation. The diets are denoted as follows: FM, SBM35, SBM35T, FSBM35T, SBM50, SBM50T, and FSBM50T. The FM (the basal diet) contained fish meal as a main source of dietary protein. Taurine was supplemented to SBM35T, FSBM35T, SBM50T, and FSBM50T at the level of 15 g/kg diet. Pompano juveniles with an initial body weight (BW) of 80 g reared in floating net cages were fed the experimental diets twice daily for 16 wk. Results showed that the final BW, weight gain, and feed conversion ratio of fish fed SBM35 and SBM50 were significantly lower than those of fish fed FM (P < 0.05), indicating that the replacement of fish meal by SBM at the rate of 35% in the diet is excessive for pompano. Supplementation of taurine to the SBM-included diets significantly increased growth performance and feed utilization (P < 0.05); however, these diets did not restore the performance back to a level equivalent to that of fish offered the basal diet. Meanwhile, fish fed FSBM35T had comparable growth and feed performances to those fed FM. Hematocrit values, total biliary bile acid levels, whole body lipid contents, and tissue taurine concentrations of fish fed SBM35 and SBM50 were the lowest among the treatments, but these parameters were improved by taurine supplementation and FSBM inclusion in the diet. Taurine supplementation increased lipid ADC, and SBM fermentation slightly enhanced both lipid and protein ADCs of the fish. These findings suggest that the combination of FSBM and taurine supplementation is an effective way to improve growth performance, nutrient digestibility, and biological parameters, and that FSBM with taurine supplementation can replace 35% of fish meal in pompano diets without any negative effects on growth and feed performances in a long-term feeding period.

Introduction

Fish meal is commonly used as the major source of protein in aquafeeds, but its limited supply and the global aquaculture expansion have led to an increasing demand for alternative ingredients to replace fish meal (Olsen et al., 2012; Hua et al., 2019). Defatted soybean meal (SBM) has been considered to be one of the most promising alternative to fish meal because of its high protein content and cost-effectiveness (Storebakken et al., 2000; Porter and Jones, 2003). However, anti-nutritional factors (ANFs) in SBM, such as glycinin, β-conglycinin, trypsin inhibitors, raffinose and stachyose, saponins, lectins, and phytate, negatively affect growth performance, feed utilization, and physiological conditions of aquatic animals, especially in carnivorous fish species (Van den Ingh et al., 1996; Refstie et al., 1998; Francis et al., 2001; Krogdahl et al., 2003; Iwashita et al., 2008a). Fermentation has been suggested as an economical and effective method to eliminate ANFs and improve the nutritional value of SBM. Lactic acid fermentation reportedly reduces the amount of ANFs such as oligosaccharides, soy antigens, and trypsin inhibitors in SBM (Refstie et al., 2005). Fermentation using Aspergillus oryzae can break down β-conglycinin, the major antigenic protein in soybean, into smaller peptides (Hong et al., 2004; Feng et al., 2007a, 2007b). Some studies have demonstrated that feeding of fermented SBM (FSBM) can improve growth performance, feed utilization, and physiological conditions in some fish species such as rainbow trout (Yamamoto et al., 2010; Choi et al., 2020), black sea bream (Azarm and Lee, 2014), hybrid striped bass (Rombensoa et al., 2013), yellowtail (Nguyen et al., 2013), Florida pompano (Novriadi et al., 2018), yellow croaker (Wang et al., 2019), and largemouth bass (He et al., 2020).

In addition to ANFs, the deficiency of essential nutrients is another obstacle in using SBM in fish feeds. Taurine, 2-aminoethanesulfonic acid, has important roles in numerous physiological functions including bile acid synthesis, membrane stabilization, osmoregulation, and anti-oxidation (Huxtable, 1992). Although taurine plays such critical roles, its content in SBM is scarce (Olli et al., 1995; Yamamoto et al., 1998). Therefore, taurine has been suggested as an essential nutrient in fish (Takagi et al., 2008; Lim et al., 2013; Salze and Davis, 2015), and the positive effects of dietary taurine supplementation reportedly improve hematocrit value, bile acid level, and growth and feed performances in carnivorous fish fed SBM-based diets (Takagi et al., 2006, 2010; Chatzifotis et al., 2010; Yun et al., 2012; Han et al., 2014; Khaoian et al., 2014). In a previous study, feeding FSBM was found to improve growth performance, nutrient apparent digestibility coefficient (ADC), and digestive physiological conditions of yellowtail fish. Moreover, these parameters were further elevated by the supplementation of taurine in the diet (Nguyen et al., 2013). These findings suggest that using FSBM with taurine supplementation may effectively improve the growth and feed performances of fish fed a soybean protein-based diet.

The pompano Trachinotus blochii (Lacepède, 1801), also known as the silver pompano is a carnivorous marine fish species, distributed mainly in the Indo-Pacific region (Kapoor et al., 2002). It is one of the most preferred high-value species for mariculture due to its fast growth rate, good meat quality, and high market demand (Othman, 2008). To date, there have been no studies to replace fish meal by SBM or FSBM and to supplement taurine in pompano feeds. Therefore, the present study was conducted to examine the effects of dietary replacement of fish meal by SBM and FSBM with taurine supplementation growth performance, nutrient ADC, and biological parameters for pompano fish in a 16-wk feeding period.

Materials and Methods

A protocol of this experiment was reviewed and approved by the Institutional Animal Care and Use Committee at Research Institute for Aquaculture No. 1 (Tuson, Bacninh, Vietnam). The experiment was carried out at The National Broodstock Center for Mariculture Species (Catba, Haiphong, Vietnam).

Animals, diets and experimental design

The pompano juveniles provided by The National Broodstock Center for Mariculture Species were acclimatized to the experimental conditions for 2 wk by feeding with the FMD before the start of the feeding trial. One hundred pompano juveniles with an initial body weight (BW) of 80 g were allocated to each of the 21 floating net cages (2.5 m × 2.5 m × 3 m), resulting in triplicate net cages per dietary treatment. The fish were fed to satiation with the experimental diets twice each day, 7 d/wk, and for 16 wk. Water temperature, dissolved oxygen concentration, salinity, and pH were monitored daily, which ranged between 25.2 and 28.6 °C, 5.4 and 6.2 mg/L, 29.4 and 33.7 ppt, and 7.9 and 8.3, respectively.

The SBM (de-hulled and solvent-extracted SBM; crude protein [CP] 49%) and FSBM (CP, 50%) were provided by Evershining Ingredient Co., Ltd. (Bangkhuntain, Bangkok, Thailand). The FSBM was produced by fermenting SBM with Lactobacillus spp., and the concentrations of ANFs in these meals are presented in Table 1. The exact production process of the FSBM has not been disclosed. Seven isonitrogenous and isoenergetic diets were formulated to replace 35% or 50% of fish meal by SBM or FSBM with taurine supplementation. The diets were denoted as follows: FM, SBM35, SBM35T, FSBM35T, SBM50, SBM50T, and FSBM50T (Table 2). The FM (the basal diet) contained fish meal as a main source of dietary protein. Taurine was supplemented to SBM35T, FSBM35T, SBM50T, and FSBM50T at the level of 15 g/kg diet, according to a previous study (Nguyen et al., 2013). dl-methionine (5 g/kg diet) was also supplemented to all SBM- and FSBM-included diets. Chromium oxide (5 g/kg diet) was added to all the experimental diets as a marker to estimate nutrient ADC. All the ingredients of the experimental diets were finely ground and well mixed, then extruded to floating pellets by a pellet extruder (Evolum Plus, Clextral Co. Ltd., Firminy, France) at De Heus Co., Ltd. (Longho, Vinhlong, Vietnam). Dried pellets of each treatment were kept separately in polyethylene bags and stored at –20 °C. The amino acid composition of the experimental diets is presented in Table 3.

Table 1.

Anti-nutritional factors in SBM and FSBM¹

	Concentration
Anti-nutritional factors	SBM	FSBM
Glycinin (ppm)	> 40,000	2
β-conglycinin (ppm)	> 20,000	<1
Lectins (ppm)	100 to 300	0.6
Oligosaccharides (%)	6 to 8	1

¹ Data were provided by Evershining Ingredient Co., Ltd. (Bangkhuntain).

Table 2.

Formulation and proximate composition of the experimental diets

	FM	SBM35	SBM35T	FSBM35T	SBM50	SBM50T	FSBM50T
Ingredients (g/kg)
Fish meal1	660	429	429	429	330	330	330
Soybean meal2	0	300	300	0	420	420	0
Fermented soybean meal3	0	0	0	300	0	0	420
Corn gluten meal4	50	50	50	50	50	50	50
Wheat flour5	90	50	50	50	50	50	50
Pollock liver oil6	55	75	75	75	85	85	85
Cellulose7	105	51	36	36	20	5	5
Vitamin and mineral mixture8	15	15	15	15	15	15	15
Calcium phosphate9	10	10	10	10	10	10	10
Soy lecithin10	10	10	10	10	10	10	10
dl-methionine11	0	5	5	5	5	5	5
Chromium oxide12	5	5	5	5	5	5	5
Taurine11	0	0	15	15	0	15	15
Proximate composition and taurine content (g/kg, dry matter basis)
CP	460	455	453	457	452	454	455
Crude lipid	127	125	124	125	123	121	124
Ash	126	108	110	106	94	87	90
Taurine	3.2	2.0	16.6	16.8	1.3	16.3	16.0

¹Menhaden fish meal (CP 65%), Omega Protein Inc., Reedville, VA.

²De-hulled and solvent-extracted soybean meal (CP 49%), Evershining Ingredient Co., Ltd., Bangkhuntain.

³Soybean meal fermented by Lactobacillus spp. (CP 50%), Evershining Ingredient Co., Ltd.

⁴Pangoo Biotech Hebei Co.,Ltd., Cangzhou, Hebei, China.

⁵Global retail JSC., Badinh, Hanoi, Vietnam.

⁶Pesquera pacific star S.A., Calle Ruta, Puerto Montt, Chile.

⁷Shanghai Richem International Co., Ltd., Shanghai, China.

⁸Hinter Biotechnology Group Co., Ltd., Zhuhai, Guangdong, China. Vitamin and mineral mixture (IU or mg/kg mixture): thiamine HNO₃, 1,030; riboflavin, 3,070; pyridoxine HCl, 1,390; cyanocobalamin, 8.1; vitamin C (l-ascorbate-2-monophosphate), 18,100; vitamin A acetate, 485,000; vitamin D₃ (cholecalciferol), 172,000; vitamin E (dl-α-tocopherol acetate, 7,010; vitamin K₃ (menadione sodium bisulfite), 1,850; folic acid, 550; nicotinamide, 5,200; d-calcium pantothenate, 4250; d-biotin, 16.5; inositol, 15,400; ZnSO₄, 2,700; MnSO₄, 1,730; CuSO₄, 1,310; FeSO₄, 6,250; CoSO₄, 156; potassium iodide, 175; sodium selenate, 38.1.

⁹Dairy Vietnam Co., Ltd., Hoankiem, Hanoi, Vietnam.

¹⁰Fuji Oil Asia Pte Ltd., Tanhung, Ho Chi Minh city, Vietnam.

¹¹TRInternational, Inc., Seattle, WA.

¹²Sigma-Aldrich Corp., St. Louis, MO.

Table 3.

Amino acid composition of the experimental diets (g/kg, dry matter basis)

	FM	SBM35	SBM35T	FSBM35T	SBM50	SBM50T	FSBM50T
Essential amino acids
Arginine	31.2	30.8	30.7	30.6	30.4	30.3	30.1
Histidine	15.5	15.8	15.9	15.5	15.7	15.6	15.5
Isoleucine	20.8	20.6	20.7	20.5	20.3	20.4	20.3
Leucine	38.8	37.5	37.7	37.6	36.9	36.7	36.8
Lysine	35.6	32.2	32.3	32.0	29.8	28.7	28.5
Methionine	17.5	18.4	18.3	18.2	16.8	16.7	16.8
Phenylalanine	24.4	23.8	23.9	23.7	23.3	23.4	23.1
Threonine	25.6	24.5	24.4	24.3	23.7	23.8	23.5
Tryptophan	6.4	6.8	6.8	6.7	7.1	7.0	7.2
Valine	22.6	22.3	22.4	22.2	21.7	21.8	21.7
Non-essential amino acids
Alanine	31.5	30.7	30.9	30.6	29.5	29.5	29.7
Aspartic acid	42.5	43.3	43.5	43.6	44.2	44.1	44.4
Cystine	49.3	52.2	52.3	52.6	54.5	54.7	54.8
Glutamic acid	67.4	71.6	71.4	71.9	73.2	73.3	73.5
Glycine	31.3	29.1	29.0	29.3	27.7	27.5	27.4
Proline	24.5	24.3	24.3	24.5	24.6	24.7	24.8
Serine	20.2	20.7	20.7	20.6	20.9	20.8	20.7
Tyrosine	15.8	16.7	16.8	16.6	17.7	17.9	18.1

Sampling and analytical methods

At the end of the feeding trial, all fish were measured the final BW after fasted for 48 hr. In addition to these measurements, 8 fish per net cage were collected. Three whole fish were used for proximate analysis. Blood samples were taken from the other 5 fish by heparinized syringes from the caudal vein. Aliquots of the blood samples were used for hematocrit determination by capillary centrifugation, and the remainder was centrifuged (10,000 rpm for 10 min) to obtain plasma. Next, these fish were dissected to collect the liver, gallbladder, and dorsal muscle. The dorsal muscle was taken from below the dorsal fin to above the lateral line area. After collecting these samples, the remaining fish continued to be fed the experimental diets, and feces were collected by stripping at 5 hr after feeding. All the samples were maintained at –20 °C until analysis.

Plasma constituents were quantified using a commercial automatic analyzer (Architect c16000, Abbott, IL). Bile juice was diluted with distilled water at a ratio of 1:1200 and was then used for total bile acid-level quantification using a commercial assay kit (MAK309, Sigma-Aldrich, St. Louis, MO). Taurine in the liver, muscle, and experimental diets was extracted with 70% perchloric acid, and its concentrations were determined with o-phthalaldehyde prelabeling high-performance liquid chromatography (HPLC, LC-20A, Shimadzu Corp., Japan), according to the method of Hopkins et al. (1989). Amino acids of the experimental diets were liberated from the protein by hydrolysis with 6 N HCl for 24 hr at 110 °C and quantified using an automatic amino acid analyzer (Hitachi, Tokyo, Japan). The proximate compositions of the experimental diets, whole body, and the digestibility marker were analyzed according to the Association of Official Analytical Chemists standard methods (AOAC, 2005). The ADC (%) was calculated as $100\times [1-({\mathrm{I}}_{\mathrm{d}\mathrm{i}\mathrm{e}\mathrm{t}}/{\mathrm{I}}_{\mathrm{f}\mathrm{e}\mathrm{c}\mathrm{e}\mathrm{s}}\times {\mathrm{N}}_{\mathrm{f}\mathrm{e}\mathrm{c}\mathrm{e}\mathrm{s}}/{\mathrm{N}}_{\mathrm{d}\mathrm{i}\mathrm{e}\mathrm{t}})]$, where I_diet and I_feces represent the concentrations of inert marker (chromium oxide) in the diet and feces, and N_diet and N_feces represent the concentrations of nutrients in the diet and feces, respectively.

Statistical analysis

Data were analyzed using 1-way analysis of variance. Statistical differences between groups were assessed using the Tukey–Kramer test, and significance was based on a 5% level of probability.

Results

Growth performance and feed utilization

The growth performance and feed utilization of pompano fed the experimental diets are shown in Table 4. The final BW and weight gain (WG) of fish in the SBM35, SBM35T, SBM50, SBM50T, and FSBM50T groups were significantly lower than those in the FM group (P < 0.05). Meanwhile, there were no significant differences in growth performance between the FSBM35T and FM groups. Fish fed SBM- and FSBM-included diets resulted in significantly higher feed conversion ratio (FCR) values than those fed FM (P < 0.05), except the FSBM35T group. Taurine supplementation in the diet significantly improved growth performance and FCR at both 35% and 50% fish meal replacement levels (P < 0.05). The test diets did not significantly alter feed intake and survival rate of the experimental fish after 16-wk feeding.

Table 4.

Growth performance and feed utilization of pompano fed the experimental diets for 16 wk

	Mean BW (g)
Dietary groups	Initial	Final	WG2 (%)	Feed intake3 (%BW/d)	FCR4	Survival (%)
FM	82.4 ± 0.3	673.2 ± 4.2d	717.0 ± 15.7d	2.90 ± 0.07	2.08 ± 0.01a	97.0 ± 4.2
SBM35	82.7 ± 0.6	612.7 ± 11.3b	640.8 ± 18.9b	3.05 ± 0.06	2.24 ± 0.01c	97.5 ± 2.1
SBM35T	82.3 ± 0.4	637.4 ± 8.5c	674.5 ± 12.6c	2.96 ± 0.12	2.15 ± 0.04b	98.0 ± 1.4
FSBM35T	82.8 ± 0.8	661.8 ± 14.8cd	699.5 ± 25.3cd	2.91 ± 0.08	2.09 ± 0.02a	95.5 ± 2.1
SBM50	82.2 ± 1.0	564.0 ± 9.9a	586.1 ± 1.4a	3.13 ± 0.06	2.35 ± 0.01d	95.0 ± 2.8
SBM50T	82.5 ± 0.8	590.6 ± 4.9b	616.0 ± 21.1b	3.06 ± 0.02	2.27 ± 0.001c	95.0 ± 4.2
FSBM50T	82.4 ± 0.6	608.9 ± 12.0b	639.0 ± 9.4b	2.98 ± 0.13	2.19 ± 0.09b	94.5 ± 0.7

¹Values are presented as means ± standard deviations of triplicates. The values in the same column with different superscripts are significantly different (P < 0.05).

² $\mathrm{W}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}\mathrm{g}\mathrm{a}\mathrm{i}\mathrm{n}=100\times (\mathrm{f}\mathrm{i}\mathrm{n}\mathrm{a}\mathrm{l}\mathrm{m}\mathrm{e}\mathrm{a}\mathrm{n}\mathrm{B}\mathrm{W}-\mathrm{i}\mathrm{n}\mathrm{i}\mathrm{t}\mathrm{i}\mathrm{a}\mathrm{l}\mathrm{m}\mathrm{e}\mathrm{a}\mathrm{n}\mathrm{B}\mathrm{W})/\mathrm{i}\mathrm{n}\mathrm{i}\mathrm{t}\mathrm{i}\mathrm{a}\mathrm{l}\mathrm{m}\mathrm{e}\mathrm{a}\mathrm{n}\mathrm{B}\mathrm{W}.$

³ $\mathrm{F}\mathrm{e}\mathrm{e}\mathrm{d}\mathrm{i}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{k}\mathrm{e}=100\times \mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{g}\mathrm{d}\mathrm{r}\mathrm{y}\mathrm{f}\mathrm{e}\mathrm{e}\mathrm{d}\mathrm{i}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{k}\mathrm{e}/\left[(\mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{i}\mathrm{n}\mathrm{i}\mathrm{t}\mathrm{i}\mathrm{a}\mathrm{l}\mathrm{B}\mathrm{W}+\mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{f}\mathrm{i}\mathrm{n}\mathrm{a}\mathrm{l}\mathrm{B}\mathrm{W})/2\right]$  $/\mathrm{f}\mathrm{e}\mathrm{e}\mathrm{d}\mathrm{i}\mathrm{n}\mathrm{g}\mathrm{d}\mathrm{a}\mathrm{y}\mathrm{s}.$

⁴ $\mathrm{F}\mathrm{e}\mathrm{e}\mathrm{d}\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{v}\mathrm{e}\mathrm{r}\mathrm{s}\mathrm{i}\mathrm{o}\mathrm{n}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\left(\mathrm{F}\mathrm{C}\mathrm{R}\right)=\mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{g}\mathrm{d}\mathrm{r}\mathrm{y}\mathrm{f}\mathrm{e}\mathrm{e}\mathrm{d}\mathrm{i}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{k}\mathrm{e}/(\mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{f}\mathrm{i}\mathrm{n}\mathrm{a}\mathrm{l}\mathrm{B}\mathrm{W}-\mathrm{i}\mathrm{n}\mathrm{i}\mathrm{t}\mathrm{i}\mathrm{a}\mathrm{l}\mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{B}\mathrm{W}).$

Hematological parameters

Hematocrit values of fish fed SBM35 and SBM50 were the lowest among the treatments (Table 5), and the difference between SBM50-fed fish and FM-fed fish was significant (P < 0.05). No statistical differences in hematocrit were observed among fish fed taurine-supplemented diets and FM. Total cholesterol levels of fish fed SBM- and FSBM-included diets were significantly inferior to that of fish fed FM (P < 0.05), except the FSBM35T group. There were no statistical differences in plasma total protein, glucose, and triglyceride levels among the treatments.

Table 5.

Hematological parameters of pompano fed the experimental diets for 16 wk¹

Dietary groups	Hematocrit (%)	Total protein (g/100 mL)	Glucose (mg/100 mL)	Total cholesterol (mg/100 mL)	Triglyceride (mg/100 mL)
FM	47.6 ± 0.5bc	4.8 ± 0.5	128.4 ± 7.8	346.4 ± 12.0b	181.3 ± 13.2
SBM35	45.1 ± 0.9ab	4.2 ± 0.4	135.5 ± 8.8	307.4 ± 10.5a	177.7 ± 15.6
SBM35T	47.7 ± 0.4bc	4.7 ± 0.3	129.2 ± 10.2	300.7 ± 11.6a	175.5 ± 9.4
FSBM35T	48.8 ± 1.3c	4.9 ± 0.5	133.7 ± 7.3	321.8 ± 9.7ab	190.8 ± 22.1
SBM50	44.0 ± 0.6a	4.4 ± 0.2	127.9 ± 11.1	286.2 ± 7.8a	166.3 ± 8.4
SBM50T	47.1 ± 0.7bc	4.7 ± 0.3	136.6 ± 6.2	289.5 ± 6.5a	182.2 ± 7.5
FSBM50T	47.4 ± 0.6bc	4.3 ± 0.6	130.1 ± 8.0	298.4 ± 17.3a	170.8 ± 14.1

¹Values are presented as means ± standard deviations of triplicates each containing 5 fish. The values in the same column with different superscripts are significantly different (P < 0.05).

Biological parameters of the liver and gallbladder

Biological parameters of the liver and gallbladder are presented in Table 6. The experimental diets had no influence on hepatosomatic index (HSI) and gallbladdersomatic index (GBSI) among the treatment groups. Total biliary bile acid level of fish fed SBM50 was significantly lower than those of fish fed taurine-supplemented diets and fish fed FM (P < 0.05). This parameter did not differ among fish fed SBM35T, FSBM35T, SBM50T, FSBM50T, and FM.

Table 6.

Biological parameters of the liver and gallbladder of pompano fed the experimental diets for 16 wk¹

Dietary groups	HSI2 (%)	GBSI3 (%)	Total biliary bile acid (mmol/L)
FM	1.30 ± 0.3	0.18 ± 0.01	316.5 ± 11.0b
SBM35	1.26 ± 0.4	0.17 ± 0.02	288.7 ± 14.6ab
SBM35T	1.29 ± 0.3	0.20 ± 0.02	296.8 ± 11.2b
FSBM35T	1.31 ± 0.4	0.19 ± 0.01	308.7 ± 10.9b
SBM50	1.22 ± 0.3	0.17 ± 0.01	255.4 ± 5.7a
SBM50T	1.27 ± 0.2	0.20 ± 0.03	290.5 ± 17.3b
FSBM50T	1.28 ± 0.3	0.18 ± 0.01	302.6 ± 8.6b

¹Values are presented means ± standard deviations of triplicates each containing 5 fish. The values in the same column with different superscripts are significantly different (P < 0.05).

² $\mathrm{H}\mathrm{e}\mathrm{p}\mathrm{a}\mathrm{t}\mathrm{o}\mathrm{s}\mathrm{o}\mathrm{m}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{c}\mathrm{i}\mathrm{n}\mathrm{d}\mathrm{e}\mathrm{x}\left(\mathrm{H}\mathrm{S}\mathrm{I}\right)=100\times \mathrm{i}\mathrm{n}\mathrm{d}\mathrm{i}\mathrm{v}\mathrm{i}\mathrm{d}\mathrm{u}\mathrm{a}\mathrm{l}\mathrm{l}\mathrm{i}\mathrm{v}\mathrm{e}\mathrm{r}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}/\mathrm{w}\mathrm{e}\mathrm{t}\mathrm{B}\mathrm{W}.$

³ $\mathrm{G}\mathrm{a}\mathrm{l}\mathrm{l}\mathrm{b}\mathrm{l}\mathrm{a}\mathrm{d}\mathrm{d}\mathrm{e}\mathrm{r}\mathrm{s}\mathrm{o}\mathrm{m}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{c}\mathrm{i}\mathrm{n}\mathrm{d}\mathrm{e}\mathrm{x}\left(\mathrm{G}\mathrm{B}\mathrm{S}\mathrm{I}\right)=100\times \mathrm{i}\mathrm{n}\mathrm{d}\mathrm{i}\mathrm{v}\mathrm{i}\mathrm{d}\mathrm{u}\mathrm{a}\mathrm{l}\mathrm{g}\mathrm{a}\mathrm{l}\mathrm{l}\mathrm{b}\mathrm{l}\mathrm{a}\mathrm{d}\mathrm{d}\mathrm{e}\mathrm{r}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}/\mathrm{w}\mathrm{e}\mathrm{t}\mathrm{B}\mathrm{W}.$

Proximate composition of the whole body

As presented in Table 7, fish fed SBM50 had the lowest crude lipid content of the whole body, and the significant difference was observed between this experimental group and the FM-, SBMT35-, and FSBMT35 experimental groups (P < 0.05). There were no statistical differences in whole body lipid content among fish fed SBM35, SBM35T, FSBM35T, SBM50T, FSBM50T, and FM. The experimental diets did not significantly alter the whole body moisture, CP, and ash contents of the fish.

Table 7.

Proximate composition of whole body of pompano fed the experimental diets for 16 wk (%)¹

Dietary groups	Moisture	CP	Crude lipid	Ash
FM	62.3 ± 2.2	15.7 ± 0.7	16.2 ± 0.9b	2.4 ± 0.6
SBM35	64.0 ± 0.6	14.1 ± 1.2	14.6 ± 1.3ab	2.2 ± 0.5
SBM35T	63.2 ± 1.4	16.0 ± 0.8	15.8 ± 0.7b	2.6 ± 0.2
FSBM35T	63.9 ± 2.7	15.9 ± 1.5	16.4 ± 1.1b	2.3 ± 0.7
SBM50	64.2 ± 2.4	15.8 ± 0.5	12.5 ± 1.0a	2.4 ± 0.4
SBM50T	64.7 ± 1.9	16.3 ± 1.1	14.8 ± 0.8ab	2.0 ± 0.5
FSBM50T	62.3 ± 2.2	16.5 ± 0.9	14.5 ± 0.5ab	2.7 ± 0.8

¹Values are presented as means ± standard deviations of triplicates each containing 3 fish. The values in the same column with different superscripts are significantly different (P < 0.05).

Taurine concentrations in the liver and muscle

As shown in Figure 1, the liver and muscle taurine concentrations were significantly lower in fish fed SBM35 and SBM50 compared with those fed FM (P < 0.05). Fish fed SBM35T, FSBM35T, SBM50T, and FSBM50T resulted in similar tissue taurine concentrations, and they were significantly higher than those of fish fed FM.

Figure 1.

Taurine concentrations in the liver and muscle of pompano fed the experimental diets. Values are presented as means ± standard deviations of triplicates each containing 5 fish. Bars assigned with different superscripts within each tissue denote significant differences (P < 0.05).

ADCs of protein and lipid

Protein ADC of fish fed SBM50 and SBM50T was the lowest among the treatments (Figure 2), and the differences were significant when comparing the 2 aforementioned fish groups and FM-fed fish (P < 0.05). FSBM inclusion in the diet tended to increase protein ADC, and the protein ADC of FSBM35T-fed fish was similar to that of FM-fed fish. Lipid ADC of fish fed SBM35 and SBM50 was significantly inferior to that of fish fed FM (P < 0.05). Dietary taurine supplementation increased lipid ADC compared with none-dietary taurine supplementation, and the lipid ADC in fish fed SBM35T and FSBM35T was comparable to that in fish fed FM.

Figure 2.

Protein and lipid ADCs of pompano fed the experimental diets. Values are presented as means ± standard deviations of triplicates. Bars assigned with different superscripts within each nutrient ADC denote significant differences (P < 0.05).

Discussion

In the present study, the final BW and WG of fish fed SBM35 were significantly lower than those of fish fed FM after 16-wk feeding (Table 4). In addition, SBM35-fed fish resulted in a significantly higher FCR value than FM-fed fish. These results indicate that the replacement of fish meal by SBM in the absence of taurine at the rate of 35% in the diet is excessive for pompano in a long-term feeding period. Supplementation of taurine to SBM-included diets significantly improved the growth and FCR of the fish; however, these diets did not restore the performances of the fish back to a level equivalent to that of fish offered the basal diet. On the other hand, the final BW, WG, and FCR of fish fed FSBM35T were comparable to those of fish fed FM. These observations suggest that taurine supplementation is beneficial to growth performance and feed utilization of pompano fed a SBM-based diet, and FSBM with taurine supplementation can replace 35% of fish meal in pompano diets without any detrimental effects on growth and feed performances in a long-term feeding period.

The improvement of nutritional quality of SBM by fermentation depends on microorganisms and fermentation conditions (Yamamoto et al., 2010; Nguyen et al., 2013; Wang et al., 2016). In fact, genera Lactobacillus, Bacillus, and Aspergillus are common microorganisms used for fermenting SBM (Hong et al., 2004; Shiu et al., 2015; Yuan et al., 2017; He et al., 2020). In this study, FSBM was produced by fermenting SBM with Lactobacillus spp., which resulted in the concentrations of glycinin, β-conglycinin, lectins, oligosaccharides to be reduced in comparison with SBM (Table 1). Thus, the elimination of such ANFs in the FSBM could be the factor contributing the improvements of the growth and feed performances of fish fed FSBM35T. Although the inclusion of FSBM in the diet provided benefits for the fish, the growth and FCR of FSBM50T-fed fish were inferior to those of FSBM35T- and FM-fed fish. It has been reported that the growth and feed performances of fish decrease as the dietary proportion of soybean protein increases (Krogdahl et al., 2003; Refstie et al., 2005; Wang et al., 2016; He et al., 2020). Hence, the poor performance of fish fed FSBM50T could be due to the excessive inclusion level of FSBM in the diet. The dietary lysine content in FSBM50T was relatively low compared to that in FM (Table 3), suggesting that the deficiency of this essential amino acid might be one of the reasons for low growth performance of fish fed FSBM50T. Apart from positive effects on growth and feed performances, fermentation reportedly improves the intestinal histology and microbiota in fish fed soybean protein-based diets (Refstie et al., 2005; Yamamoto et al., 2010; Wang et al., 2019; Choi et al., 2020; He et al., 2020). In the present study, morphology and microorganism population in the intestine were not examined. For this reason, further studies are required to evaluate whether FSBM benefit such parameters in pompano fish.

Anemia, which is indicated by a low hematocrit value, has been reported in carnivorous fish such as yellowtail (Takagi et al., 2006) and tiger puffer (Lim et al., 2011) when they were fed a soybean protein-based diet. In this study, fish fed SBM35 and SBM50 had lower hematocrit values than fish fed FM, and the hematocrit tended to decrease as the dietary SBM inclusion level increased (Table 5). Meanwhile, the hematocrit values of fish fed SBM35T and SBM50T were comparable to that of fish fed FM. These results, together with dietary taurine contents and tissue taurine concentrations (Table 2 and Figure 1), indicate that taurine deficiency could be a factor responsible for the anemia observed in fish fed SBM35 and SBM50. The higher hematocrit values in fish fed taurine-supplemented diets compared with fish fed SBM35 and SBM50 suggest that taurine supplementation in SBM diets is necessary to improve the anemia in pompano. This result supports an earlier report in yellowtail, where the hematocrit value of the fish was elevated by adding taurine in a soybean protein-based diet (Takagi et al., 2006).

Reductions in gallbladder bile acid levels have been recorded in red sea bream (Takagi et al., 2002), rainbow trout (Iwashita et al., 2008b; Yamanoto et al., 2010), and yellowtail (Nguyen et al., 2011a, 2017) fed soybean protein-based diets. In this study, we similarly found that total bile acid levels in the gallbladders of pompano fed SBM35 and SBM50 were lower than that of fish fed FM (Table 6). In contrast, gallbladder total bile acid levels were dramatically increased in fish fed taurine-supplemented diets, reaching comparable values to that of fish fed FM. Bile acids are synthesized from cholesterol in the liver and are conjugated with taurine or glycine before being stored in the gallbladder (Tuchweber et al., 1996). In carnivorous fish, the conjugation is exclusive to taurine, and taurocholic acid and taurochenodeoxycholic acid are the main bile acids (Goto et al., 1996; Kim et al., 2007). Since the dietary taurine contents in SBM35 and SBM50 were lower than that in FM, the inferior bile acid levels in the gallbladders of fish fed these 2 SBM diets could be due to the insufficient taurine supply, resulting in the poor bile acid synthesis. The deficiency of taurine supply was also supported by the low taurine concentrations in the liver and muscle tissues of SBM35- and SBM50-fed fish. Fish fed taurine-supplemented diets had higher taurine concentrations in the liver and muscle than fish fed FM. Moreover, the similar levels of total bile acid were observed among fish fed taurine-supplemented diets and FM. These results imply that the amount of taurine (15 g/kg diet) added to SBM35T, FSBM35T, SBM50T, and FSBM50T in the present study was sufficient to meet the requirement of pompano.

Low nutrient ADCs have been reported in Atlantic salmon (Olli and Krogdahl, 1995; Storebakken et al., 1995), rainbow trout (Romarheim et al., 2008), red sea bream (Biswas et al., 2007), and yellowtail (Nguyen et al., 2013) when they were fed SBM-based diets. In the present study, fish fed SBM35 and SBM50 showed lower protein and lipid ADCs than fish-fed FM, meaning that SBM reduced dietary protein and lipid digestion and absorption in pompano fish. On the other hand, fish fed SBM50T showed a significantly higher lipid ADC than fish fed SBM50. Similarly, SBM35T-fed fish had a slightly higher lipid ADC than SBM35-fed fish. These observations, together with bile acid level, imply that supplementation of taurine in the SBM diets improved dietary lipid digestion and absorption through the increase in bile acid synthesis. Some studies have demonstrated that SBM fermentation can enhance nutrient digestion and absorption (Kiers et al., 2003; Refstie et al., 2005; Feng et al., 2007b; Yamamoto et al., 2010; Nguyen et al., 2013; Yuan et al., 2017). In the current study, fish-fed FSBM-included diets slightly increased protein and lipid ADCs compared with those fed SBM-included diets. Alcohol-soluble components in SBM, which consist of oligosaccharides and lectins, have been found to prevent the secretion of bile acids and pancreatic lipases into the intestine, resulting in poor dietary lipid digestion and absorption (Nguyen et al., 2011b; 2017). In addition, glycinin and β-conglycinin of SBM reportedly reduce digestive enzyme activity, nutrient ADCs, and growth and feed performances of fish (Zhang et al., 2013; Li et al., 2017a, 2017b). Thus, the presence of such ANFs in SBM could interfere with protein and lipid digestion and absorption of pompano in the present study, though bile acid synthesis of fish fed SBM35T and SBM50T has been improved by taurine supplementation. The elimination of these ANFs through fermentation might be beneficial to nutrient digestion and absorption of fish fed FSBM35T and FSBM50T.

In conclusion, the replacement of fish meal by SBM at the rate of 35% in the diet is excessive for pompano. The fermentation of SBM with Lactobacillus spp. tended to enhance protein and lipid ADCs. Taurine supplementation improved hematocrit value, bile acid level, and lipid ADC. These positive effects could contribute to the improvements of growth performance and feed utilization. The findings of the present study suggest that the combination of FSBM and taurine supplementation may be an effective way to improve growth performance and feed utilization and that FSBM with taurine supplementation can replace 35% of fish meal in pompano diets without any adverse effects on growth and feed performances in a long-term feeding period.

Glossary

Abbreviations

ADC

apparent digestibility coefficient

ANFs

anti-nutritional factors

BW

body weight

CP

crude protein

FCR

feed conversion ratio

FSBM

fermented soybean meal

GBSI

gallbladdersomatic index

HSI

hepatosomatic index

SBM

defatted soybean meal

WG

weight gain

Funding

This study was financially supported by National Foundation for Science and Technology Development (NAFOSTED).

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.