This study was conducted to examine the supplementary effects of tuna hydrolysate (TH) and shrimp hydrolysate (SH) as squid-liver powder (SLP) replacers in a high soybean meal diet for Pacific white shrimp (Litopenaeus vannamei). A diet containing 4.49% SLP was regarded as the control diet and two other diets were prepared by supplementing 1.14% tuna hydrolysate (TH) and 0.94% shrimp hydrolysate (SH) (designated as SLP, TH and SH, respectively). Five replicate groups of shrimp (initial mean body weight, 0.35 ± 0.002 g) were fed one of the experimental diets for 52 days. Final body weight and weight gain of shrimp fed SH and TH diets were significantly higher than those of shrimp fed SLP diet (p < 0.05). Feed conversion ratio was lower in SH group compared to that of shrimp fed other diets. Total antioxidant capacity and catalase activity were significantly higher in TH or SH group than SLP group (p < 0.05). Hemolymph glucose and triglyceride levels of shrimp fed SLP were significantly lower than those of shrimp fed TH and SH (p < 0.05). Shrimp-fed TH or SH exhibited significantly higher carcass lipid composition than shrimp-fed SLP (p < 0.05). Dry matter and protein digestibility were significantly higher in SH diet (p < 0.05). The findings in this study indicate that SH and TH can be used as beneficial feed supplements or ingredients that could replace SLP in L. vannamei diet. Optimum inclusion level of SH would be approximately 1% to completely replace SLP in L. vannamei diet containing high level of soybean meal.

1 INTRODUCTION

Pacific white shrimp (Litopenaeus vannamei) is an omnivorous species. The inclusion of marine protein sources such as fish meal (FM), shrimp meal and squid meal in their diet is necessary to enhance feed utilization efficiency in commercial aquaculture (Bauer et al., 2012; Moss et al., 2018; Suárez et al., 2009; Tacon & Barg, 1998).

Squid meal, squid-liver powder (SLP) and viscera meal from the processing of squid or cuttlefish are generally used as feed attractants in fish and shrimp diets (Suresh & Nates, 2011), thus enhancing the growth and feed utilization of these animals (Navarro et al., 2020). The growth of Japanese seabass (Lateolabrax japonicus) was reported to be enhanced by dietary supplementation of squid viscera meal compared to the growth of those fed a high-FM diet (Mai et al., 2006). Cruz-Suárez et al. (1989) found that squid extract had a positive impact on growth, feed utilization and nutrient availability in Kuruma prawn (Penaeus japonicus). Dietary squid meal enhanced the growth of giant tiger prawn (Penaeus monodon) (Smith et al., 2005). The growth performance and digestive enzyme activity of L. vannamei were increased when squid meal supplementation comprised 9% of crude protein in their diet but decreased when the supplementation exceeded 15% of crude protein (Córdova-Murueta, & García-Carreño, 2002). Similarly, high levels of dietary squid products were reported to suppress shrimp growth (Smith et al., 2005). In addition, long-term consumption of squid products may result in cadmium accumulation in animal tissues (Mai et al., 2006).

Tuna hydrolysate (TH) is produced from processing tuna wastes (viscera, head or frame) which are rich sources of protein and contain well-balanced amino acid profiles. Waste production volume for fish largely depends on the processing method. Canned tuna production typically generates 50%–70% of raw material as solid waste (Saidi et al., 2014). Therefore, different types of processing waste are available to produce TH (Cheng et al., 2015; Guerard et al., 2002; Nguyen et al., 2012). Hydrolysates of tuna liver was reported to possess antioxidant and antihypertensive properties and may thereby provide health benefits when administered as a dietary supplement or feed ingredient (Je et al., 2009). The protein hydrolysates of tuna frame or dark muscle tissue were also reported to be beneficial due to their nutraceutical and pharmaceutical activities against hypertension-associated diseases (Lee et al., 2010; Qian et al., 2007). TH also exhibits functional properties (whipping, gelling and texturing) as a food ingredient (Herpandi et al., 2011). Therefore, TH can be used as a protein source in fish and shrimp diets due to its excellent properties in addition to being a valuable protein and amino acid source. In a previous study (Khosravi et al., 2015), we found that TH improved growth, feed utilization, health status, diet digestibility and disease resistance of red seabream (Pagrus major). In shrimp, growth performance was improved by dietary supplementation of tuna head hydrolysate (Nguyen et al., 2012). Hernández et al. (2011) found that tuna byproduct hydrolysates enhanced the palatability of shrimp feed and improved protein digestibility and amino acid availability. Moreover, the authors observed that the growth performance of shrimp increased after a 6-week feeding trial.

Shrimp hydrolysates (SH) are produced from shrimp processing waste which accounts for 35%–45% of raw materials as inedible wastes (Kandra et al., 2012; Shahidi & Synowiecki, 1991). A shrimp head meal was tested as a protein ingredient in a low-FM diet for shrimp (Liu et al., 2011; Ye et al., 2011). Several studies have reported that SH supplementation improved the growth performance, feed efficiency, diet digestibility and innate immune responses in fish species, including Nile tilapia (Oreochromis niloticus) (Leal et al., 2010; Plascencia-Jatomea et al., 2002), olive flounder (Paralichthys olivaceus) (Gunathilaka et al., 2020; Khosravi et al., 2018) red seabream (Bui et al., 2014; Khosravi et al., 2015), cobia (Rachycentron canadum) (Costa-Bomfim et al., 2017) and European sea bass (Dicentrarchus labrax) (Gisbert et al., 2018); however, to the best of our knowledge, no studies have been conducted on SH supplementation in shrimp diets. Therefore, this study was designed to evaluate the supplementary effects of TH and SH as SLP replacers in diets containing a high level of soybean meal on growth performance, feed utilization, antioxidant capacity, innate immunity and diet digestibility of L. vannamei.

2 MATERIALS AND METHODS

2.1 Experimental design and diet preparation

Three experimental diets were formulated to contain 33.3% crude protein and 17.4 kJ g⁻¹ energy. A diet containing 4.49% SLP (dry matter basis) was regarded as a control diet and the other two diets were prepared by supplementing 1.14% TH and 0.94% SH. TH and SH were provided by DIANA AQUA (Aquaculture Division of DIANA, Member of SYMRISE Group, Elven, France). Soybean meal was used as a main protein source in the diets. All dry ingredients were thoroughly mixed in a mixer (NVM-14; Daeyung) after adding soybean oil, fish oil and distilled water. Then, the mixed dough was pelleted in 2 mm size with a pellet machine (SP-50; Gumgang ENG). The pellets were subsequently dried at 25°C for 8 h and then stored at −20°C. Molecular weight distribution and nutrient composition of SLP, TH and SH are shown in Table 1. Diet formulation and chemical composition are shown in Tables 2 and 3.

TABLE 1. Molecular weight distribution and nutrient composition of squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH) (from product technical data sheets)

	SLP	TH	SH
Molecular weight (Dalton, % wet basis)
>30,000	–	0.00	0.01
20,000–30,000	–	0.19	0.02
10,000–20,000	–	0.27	0.08
5000–10,000	–	0.48	0.59
1000–5000	–	5.27	6.69
500–1000	–	6.77	7.67
<500	–	87.0	85.0
Proximate composition
Dry matter, DM (%)	89.7	28.6	94.0
Protein (% DM)	52.4	43.8	71.3
Lipid (% DM)	24.9	11.1	8.91
Ash (% DM)	9.47	26.6	13.6
Soluble protein (% total protein)	–	90.2	90.8
Fatty acids
Total omega-3 (% lipid)	2.90	1.16	1.34
Total omega-6 (% lipid)	0.60	0.14	1.84
EPA (% lipid)	1.56	0.21	0.49
DHA (% lipid)	1.56	0.95	0.60
Essential amino acids (products, % wet basis)
Arginine	5.38	0.54	4.33
Histidine	1.18	0.69	1.47
Isoleucin	1.99	0.52	2.87
Leucine	4.82	0.89	4.50
Lysine	6.36	0.63	4.31
Methionine	1.40	0.30	1.33
Phenylalanine	2.60	0.52	3.06
Threonine	2.99	0.49	2.58
Valine	2.77	0.59	3.51

TABLE 2. Formulation of the three experimental diets for Pacific white shrimp (Litopenaeus vannamei) (%, dry matter)

Ingredients	SLP	TH	SH
Tuna meal (55% CP)	9.10	9.10	9.10
Squid-liver powder	4.49
Tuna hydrolysate		1.14
Shrimp hydrolysate			0.94
Wheat gluten	4.50	4.50	4.50
Soybean meal	45.1	48.6	48.3
Wheat flour	16.0	16.0	16.0
Starch	7.18	6.48	6.94
Soybean oil	2.00	2.00	2.00
Fish oil	2.38	3.06	3.11
Lecithin	1.00	1.00	1.00
Mineral premix¹	2.00	2.00	2.00
Vitamin premix²	1.00	1.00	1.00
Cholesterol	0.04	0.08	0.07
Choline chloride	1.00	1.00	1.00
Monocalcium phosphate	3.00	3.00	3.00
Guar gum	1.00	1.00	1.00
Proximate composition (%, dry matter)
Crude protein	32.9	33.6	33.8
Crude lipid	8.00	7.90	8.00
Ash	6.20	6.40	6.70
Dry matter	92.8	93.2	93.2

Note: Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).
¹ Mineral premix (1 kg) contains 80 g MgSO₄·7H₂O, 370 g NaH₂PO₄·2H₂O, 130 g KCl, 40 g Ferric citrate, 20 g ZnSO₄·7H₂O, 356.64 g Ca-lactate, 0.2 g CuCl₂, 0.15 g AlCl₃·6H₂O, 0.01 g Na₂Se₂O₃, 2 g MnSO₄·H₂O and 1 g CoCl₂·6H₂O.
² Vitamin premix (1 kg) contains 121.2 g L-ascorbic acid, 18.8 g DL-α tocopheryl acetate, 2.7 g thiamin hydrochloride, 9.1 g riboflavin, 1.8 g pyridoxine hydrochloride, 36.4 g niacin, 12.7 g Ca-D-pantothenate, 181.8 g myo-inositol, 0.27 g D-biotin, 0.68 g folic acid, 18.2 g p-aminobenzoic acid, 1.8 g menadione, 0.73 g retinyl acetate, 0.003 g cholecalciferol, 0.003 g cyanocobalamin and 593.814 g starch.

TABLE 3. Amino acid composition (%, dry matter) of the three experimental diets for Pacific white shrimp (Litopenaeus vannamei)

	SLP	TH	SH
Essential amino acids
Threonine	1.33	1.31	1.23
Valine	1.73	1.71	1.61
Isoleucine	1.60	1.59	1.49
Leucine	2.65	2.65	2.48
Phenylalanine	1.76	1.78	1.66
Histidine	1.19	1.15	1.07
Lysine	1.18	1.14	1.08
Arginine	1.45	1.34	1.27
Non-essential amino acids
Aspartic acid	3.68	3.60	3.34
Serine	1.69	1.64	1.53
Glutamic acid	7.39	7.28	6.84
Proline	2.19	2.48	2.50
Glycine	1.69	1.67	1.58
Alanine	1.61	1.54	1.46
Tyrosine	1.02	1.08	1.00

Note: Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).

2.2 Shrimp and feeding trial

The experimental shrimp was fed a commercial diet for 2 weeks to be acclimated to the experimental facilities. Then, the shrimp (average body weight, 0.35 ± 0.002 g) was randomly distributed into 120 L capacity 15 acrylic tanks at a density of 25 shrimp per tank. Tanks were filled with filtered seawater and aerated to keep sufficient level of dissolved oxygen. Water temperature was kept at 28–30°C during the feeding trial. Five replicate groups of shrimp were fed one of the experimental diets at a ratio of 6%–16% body weight (four times a day, 08:30, 12:00, 16:00 and 19:30 h) for 52 days. The rearing water was exchanged by 90% every 3 days. During the feeding trial, water quality was maintained within a standard range for L. vannamei as follows: temperature (28–31°C), pH (7.38–7.64), dissolved oxygen (6.70–7.37 mg L⁻¹) and ammonia (0.03–0.10 mg L⁻¹). Photoperiod was scheduled for 12:12 h light/dark by fluorescent light. Experimental protocols for the experiment followed the guidelines of the Institutional Animal Care and Use Committee of Jeju National University.

2.3 Sample collection

All the shrimps in each tank were individually weighed for calculation of growth parameters and survival rate. Four shrimps per tank (20 shrimp per dietary treatment) were randomly captured and placed in ice water for 5 min to anaesthetise before hemolymph sampling. Hemolymph were taken from the ventral sinus with 1 ml syringes (25gauge needle) containing 400 μl of precooled (4°C) anticoagulant Alsever's solution (A3551; Sigma-Aldrich). The diluted hemolymph from each shrimp was kept and analysed separately. Anticoagulant-hemolymph was used to determine nitroblue-tetrazolium (NBT) activity. The remaining anticoagulant-hemolymph mixture was centrifuged at 800 g for 20 min at 4°C. The supernatant was separated and stored at −70°C for innate immune response analyses. Another three shrimps per tank were captured and stored for the analysis of carcass proximate composition.

2.4 Sample analyses

Analysis of moisture and ash contents were performed using standard procedures (AOAC, 1995). Moisture content was measured by heating samples at 125°C for 4 h in a dry oven. Ash content was measured by burning the samples at 500°C in a muffle furnace for 8 h. Crude protein levels were measured according to the Kjeldahl method with an automated Kjeltec Analyser (Kjeltec™ 2300; FOSS Analytical). Crude lipid levels in diets and carcass were analysed after extraction with chloroform/methanol mixture (2:1; v/v) according to Folch et al. (1957). The antiprotease activity was measured according to Ellis (1990) with slight modifications as applied by Magnadóttir et al. (1999). Activity of serum catalase enzyme was analysed using a kit (K773-100; Biovision). Total antioxidant capacity (TAC) was also determined using a kit (CS0790; Sigma-Aldrich). Phenoloxidase (PO) activity was measured according to Hernández-López et al. (1996). Production of oxidative radical during respiratory burst was measured by NBT assay according to Song and Hsieh (1994) with slight modifications (Zhang et al., 2013). Levels of cholesterol, glucose, triglyceride and total protein were determined using a blood analyser (SLIM; SEAC).

2.5 Estimation of apparent digestibility coefficients

Diets for the digestibility test were prepared to contain 1% chromium oxide (Cr₂O₃) (Sigma-Aldrich) as an inert indicator. Another set of shrimp was stocked into three 240 L capacity tanks at a density of 40–50 shrimp per tank. Shrimp were fed at 08:30 h and culture water was exchanged removing any debris on the bottom of tanks 30 min after the feeding. Faecal samples were collected three times a day by siphoning from each tank (11:30, 15:00 and 18:30 h). Collected faeces from each tank were frozen at −20°C until analyses after removing the water with a filter paper. Chromium oxide content in both diets and faecal samples was analysed by Divakaran et al. (2002). Apparent digestibility coefficients (ADCs) were calculated according to the method described by Cho et al. (1982).

2.6 Statistical analysis

Experimental diets were assigned using a completely randomized design. Data were analysed by one-way analysis of variance (ANOVA) after arcsine transformation in spss version 20.0 (SPSS). The differences in mean values were compared using Duncan's multiple range test at the 5% significance level (p < 0.05).

3 RESULTS

Growth performance, feed utilization and survival of shrimp are provided in Table 4. Final body weight (FBW) and weight gain of shrimp-fed SH diet were significantly higher than those of shrimp-fed SLP or TH diet (p < 0.05). TH group also exhibited significantly higher FBW than SLP group. Feed conversion ratio was significantly lower in SH group than TH group (p < 0.05). Protein efficiency ratio of shrimp-fed SH diet was significantly higher than that of shrimp-fed TH diet. Survival rate was not significantly influenced by the dietary treatments although numerically higher survival was found in TH and SH groups than SLP group (p > 0.05).

TABLE 4. Growth performance and feed utilization of Pacific white shrimp (Litopenaeus vannamei) fed the three experimental diets for 52 days

	SLP	TH	SH
IBW¹	0.35 ± 0.00	0.35 ± 0.00	0.35 ± 0.00
FBW (g)²	4.92 ± 0.17^c	5.18 ± 0.22^b	5.54 ± 0.12^a
WG (%)³	1301 ± 61.6^b	1381 ± 59.0^b	1476 ± 27.1^a
FCR⁴	1.84 ± 0.12^ab	1.90 ± 0.10^a	1.74 ± 0.05^b
PER⁵	1.53 ± 0.09^ab	1.47 ± 0.06^b	1.70 ± 0.05^a
Survival rate (%)	79.2 ± 5.93	86.4 ± 2.19	85.6 ± 5.37

Note: Values are mean of five replicates groups and presented as mean ± standard deviation. Values with different superscripts in the same row are significantly different (p < 0.05). Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).
¹ Initial body weight (g).
² Final mean body weight (g).
³ Weight gain (%) = 100 × (FBW − initial mean body weight)/initial mean body weight.
⁴ Feed conversion ratio = dry feed fed (g)/wet weight gain (g).
⁵ Protein efficiency ratio = wet weight gain /total protein given.

The carcass proximate composition is shown in Table 5. Shrimp-fed TH and SH diets exhibited significantly higher carcass lipid level than shrimp-fed SLP diet (p < 0.05). Carcass protein, ash and dry matter were not affected by the dietary treatments. Amino acid compositions of shrimp carcass (Table 6) were not also affected by the dietary treatments.

TABLE 5. Carcass composition (%, dry matter) of Pacific white shrimp (Litopenaeus vannamei) fed the three experimental diets for 52 days

	SLP	TH	SH
Dry matter	24.7 ± 0.04	24.3 ± 0.49	24.6 ± 0.06
Ash	13.3 ± 0.07	13.3 ± 0.21	13.0 ± 1.25
Protein	74.2 ± 0.46	75.5 ± 0.17	76.3 ± 0.81
Lipid	3.78 ± 0.16^b	5.03 ± 0.03^a	5.58 ± 0.14^a

Note: Values are mean of five replicate groups and presented as mean ± standard deviation. Values with different superscripts in the same row are significantly different (p < 0.05). Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).

TABLE 6. Amino acid composition (% in sample) for carcass of Pacific white shrimp (Litopenaeus vannamei) fed the three experimental diets for 52 days

	SLP	TH	SH
Essential amino acids
Threonine	3.12	3.02	3.07
Valine	3.76	3.77	3.82
Isoleucine	3.72	3.73	3.82
Leucine	6.29	6.20	6.37
Phenylalanine	3.47	3.39	3.52
Histidine	2.38	2.34	2.33
Lysine	6.92	6.75	6.96
Arginine	9.43	9.30	9.59
Non-essential amino acids
Aspartic acid	8.89	8.83	9.08
Serine	2.99	2.82	2.88
Glutamic acid	14.2	14.0	14.4
Proline	5.14	5.28	4.89
Glycine	7.74	7.77	8.17
Alanine	3.34	3.19	3.33
Tyrosine	2.59	2.47	2.55

Note: Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).

The results of innate immunity, antioxidant enzyme activity and hemolymph biochemical parameters are provided in Table 7. TAC and catalase activity were significantly higher in shrimp-fed TH and SH diets compared to those of shrimp-fed SLP diet, while SH group had significantly higher catalase activity than TH group (p < 0.05). TAC of shrimp-fed TH diet was not significantly different compared to that of SH group. No significant difference in NBT (p > 0.05), PO (p > 0.05) and antiprotease (p > 0.05) activities were observed among all the groups. Glucose level of shrimp-fed SLP diet was significantly lower than that of shrimp-fed TH and SH diets (p < 0.05). Triglyceride level was significantly lower in SLP or TH group than SH group (p < 0.05). No significant differences in total protein and cholesterol levels were observed among all the groups (p > 0.05).

TABLE 7. Innate immune, antioxidant capacity and hemolymph biochemical parameters of Pacific white shrimp (Litopenaeus vannamei) fed the three experimental diets for 52 days

	SLP	TH	SH
NBT¹	2.36 ± 0.82	1.95 ± 0.85	2.38 ± 1.00
PO²	0.13 ± 0.03	0.13 ± 0.01	0.12 ± 0.02
Antiprotease³	36.5 ± 2.37	40.7 ± 4.01	39.6 ± 1.94
GPx⁴	32.7 ± 6.75	28.7 ± 7.39	28.1 ± 2.88
TAC⁵	1.04 ± 0.05^b	1.24 ± 0.05^a	1.26 ± 0.10^a
Catalase⁶	0.96 ± 0.01^c	1.20 ± 0.04^b	1.35 ± 0.05^a
Glucose (mg dl⁻¹)	207 ± 6.25^b	276 ± 29.8^a	300 ± 8.42^a
Triglyceride (mg dl⁻¹)	16.0 ± 2.60^b	17.6 ± 2.04^b	21.2 ± 1.29^a
Total protein (g dl⁻¹)	1.74 ± 0.54	2.15 ± 0.35	2.20 ± 0.61
Total cholesterol (mg dl⁻¹)	7.92 ± 0.70	7.35 ± 1.51	7.45 ± 1.41

Note: Values are mean of five replicate groups and presented as mean ± standard deviation. Values with different superscripts in the same row are significantly different (p < 0.05). Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).
¹ Nitro blue tetrazolium; phagocytic activity (absorbance).
² Phenoloxidase activity (absorbance).
³ Antiprotease activity (% inhibition).
⁴ Glutathione peroxidase activity (mU ml⁻¹).
⁵ Total antioxidant capacity (μmol ml⁻¹).
⁶ Catalase activity (mU ml⁻¹).

The ADCs for dry matter (ADCd), protein (ADCp), lipids (ADCl) and amino acids (ADCa) are shown in Tables 8 and 9. SH Diet exhibited significantly higher ADCd than TH diet (p < 0.05). ADCp was significantly higher in SH diet compared to that of TH and SLP groups (p < 0.05). ADCl was not significantly different among the treatments (p > 0.05).

TABLE 8. Apparent digestibility coefficients (%, ADC) for dry matter, protein, and lipid of the experimental diets for Pacific white shrimp (Litopenaeus vannamei)

	SLP	TH	SH
ADCd (%)¹	83.2 ± 0.20^ab	82.2 ± 0.32^b	84.3 ± 2.73^a
ADCp (%)²	90.4 ± 0.11^b	91.1 ± 0.16^b	92.4 ± 1.32^a
ADCl (%)³	89.1 ± 0.13	89.8 ± 0.18	89.7 ± 1.79

Note: Values are mean of five replicate groups and presented as mean ± standard deviation. Values with different superscripts in the same row are significantly different (p < 0.05). Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).
¹ Apparent digestibility coefficient of dry matter.
² Apparent digestibility coefficient of protein.
³ Apparent digestibility coefficient of lipid.

TABLE 9. Apparent digestibility coefficients (%, ADC) for the amino acid of the experimental diets for Pacific white shrimp (Litopenaeus vannamei)

	SLP	TH	SH
Essential amino acids
Threonine	96.1 ± 0.2	96.5 ± 0.1	96.6 ± 0.0
Valine	95.6 ± 0.2	96.0 ± 0.2	96.2 ± 0.2
Isoleucine	96.7 ± 0.2	97.0 ± 0.1	97.1 ± 0.2
Leucine	94.5 ± 0.3	95.3 ± 0.2	95.4 ± 0.2
Phenylalanine	96.3 ± 0.1	96.8 ± 0.1	96.9 ± 0.1
Histidine	95.6 ± 1.7	96.2 ± 0.0	96.5 ± 0.6
Lysine	96.7 ± 0.1	96.9 ± 0.1	97.1 ± 0.1
Arginine	96.4 ± 0.1	96.8 ± 0.1	96.7 ± 0.1
Non-essential amino acids
Aspartic acid	92.5 ± 0.1	93.3 ± 0.3	93.5 ± 0.1
Serine	96.4 ± 0.4	96.7 ± 0.1	96.8 ± 0.1
Glutamic acid	90.1 ± 0.4	90.9 ± 0.3	91.2 ± 0.1
Proline	96.7 ± 0.2	96.8 ± 0.3	96.4 ± 0.2
Glycine	94.8 ± 0.1	95.2 ± 0.2	94.4 ± 0.7
Alanine	95.9 ± 1.1	96.4 ± 1.0	96.2 ± 1.0
Tyrosine	97.5 ± 0.2	97.9 ± 0.1	98.0 ± 0.1

Note: Ingredients are abbreviated as: squid-liver powder (SLP), tuna hydrolysate (TH) and shrimp hydrolysate (SH).

4 DISCUSSION

Our results indicated that the dietary inclusion of SH improved the growth performance and feed utilization of shrimp. SH has been reported to improve the growth, immunity, digestibility, palatability and health status of fish (Gunathilaka et al., 2020; Khosravi et al., 2015, 2018; Leal et al., 2010; Leduc et al., 2018; Plascencia-Jatomea et al., 2002). SH contains astaxanthin which is known to have growth-stimulating effects for fish (Cheng et al., 2018; Kalinowski et al., 2011; Li et al., 2014, 2018; Lim et al., 2018; Xie et al., 2017) and shrimps (Chuchird et al., 2015; Niu et al., 2009; Paibulkichakul et al., 2008). Dietary supplementation of low-molecular weight peptides was reported to enhance the growth performance of fish and shrimp (Gyan et al., 2020; Lugo et al., 2013; Teshima et al., 2004). Therefore, the presence of low-molecular weight peptides in SH might explain the improved growth performance of shrimp-fed SH diet. The growth of shrimp-fed TH diet followed a similar trend, although the positive effect of TH was not as high as that for SH. In a previous study, we observed that TH improved growth performance of red seabream (Khosravi et al., 2015). TH supplementation in a fish meal free diet for barramundi (Lates calcarifer) was recommended to promote growth performance (Siddik et al., 2019). Dietary TH was also reported to improve the growth performance of shrimp (Hernández et al., 2011; Nguyen et al., 2012). The authors in the studies hypothesized that the high level of digestible protein in TH might explain the improved shrimp growth. Accordingly, in the present study, the highly digestible, low-molecular-weight peptides in SH and TH might account for the improved growth of shrimp.

Catalase is important to maintain cellular redox balance by eliminating hydrogen peroxide (He et al., 2017; Hwang et al., 2020). Catalase action also accelerates the functions of the innate immune system (Ji et al., 2009). In this study, shrimp-fed TH or SH diets exhibited higher catalase activity including TAC. Therefore, supplementation of approximately 1% TH or SH (in wet basis) could be an effective substitute for SLP in diet for shrimp. Squid byproduct ingredients or additives in diets were also reported to improve the immunity of fish and other animals (Estruch et al., 2018; Liu et al., 2011; Murakawa et al., 2007). Unlike squid byproducts, TH and SH contain low-molecular weight compounds including peptides and free amino acids (Table 9). Several low-molecular weight peptides have been identified in SH showing antimicrobial properties (Robert et al., 2014). Gyan et al. (2020) reported that antioxidant activities in L. vannamei was enhanced by including antimicrobial peptides in their diets. Liao et al. (2019) also found that antioxidant activity in L. vannamei was enhanced after feeding them a diet containing antimicrobial polypeptides. Peptides and amino acids possess radical scavenging activity (Elias et al., 2008; Mendis et al., 2005; Wu et al., 2003). Therefore, the peptides present in TH or SH might have enhanced the hemolymph antioxidant capacity of L. vannamei, as reflected by the significantly higher TAC and catalase activity in shrimp-fed TH or SH diets compared to those in the SLP group.

The increased level of glucose in hemolymph of shrimp-fed TH or SH is debatable because it is difficult to identify the exact mechanism for the increase in this study. Racotta and Palacios (1998) reported that the hemolymph glucose level of L. vannamei was increased in response to stress. This parameter has also been shown to increase in response to hemolymph nitrate levels (Yildiz & Benli, 2004). Gutiérrez et al. (2007) observed that hemolymph glucose level was increased when shrimp were injected with insulin-like growth factor- I (IGF-I). In the present study, we did not observe retarded growth or any abnormality in the tested parameters. Therefore, we assumed that the shrimp were not stressed and that the increased glucose level might be associated with the increased IGF-I level in hemolymph since IGF-I is known to increase energy metabolism in animals (Jung et al., 2013). Hemolymph triglyceride level was significantly higher in shrimp-fed SH diet than in shrimp-fed SLP diet. Mercier et al. (2006) observed a reduced triglyceride level in L. vannamei that were subjected to handling stress. Triglyceride and glucose levels in crustacean hemolymph may also change during moulting (Ciaramella et al., 2014; Galindo et al., 2009). Nutrient availability is also an important factor that affects hemolymph biochemistry in crustaceans (Stuck et al., 1996). Thus, further studies are needed to investigate the effects of marine protein hydrolysates on hemolymph biochemical parameters of shrimp.

SLP, TH, and SH diets showed comparable DM digestibility regardless of their soybean-meal level suggesting that SLP in shrimp diets can be replaced with TH or SH at the levels tested in this study without sacrificing diet digestibility. SH was reported to improve intestinal morphology and diet digestibility in fish (Khosravi et al., 2015, 2018; Leduc et al., 2018). According to the studies, high level of dietary low-molecular weight compounds, peptides and soluble nitrogen level was the reasons for the improved diet digestibility. Gunathilaka et al. (2020) reported that diet digestibility and nutrient absorption can be enhanced by dietary supplementation of SH for olive flounder. Ravallec-Plé and Van Wormhoudt (2003) reported that peptides produced by hydrolyzing shrimp heads can induce enzyme secretion in animal cells. According to Hernández et al. (2011), high levels of digestible protein in TH were responsible for improved protein digestibility in shrimp. Soluble nitrogen levels were higher in SH and TH than in SLP, perhaps explaining the improved digestibility of SH and TH diets in the present study. Moreover, Córdova-Murueta and García-Carreño (2002) observed that fish and krill hydrolysates increased the gut enzyme activity of P. vannamei to a greater extent than squid meal. They also observed high proteolytic activity in fish hydrolysates, while squid meal exhibited no proteolytic activity. These findings are consistent with those of the current study, supporting the conclusion that hydrolysates are more effective than squid meal in promoting protein digestion.

In conclusion, SLP in the shrimp diets can be totally replaced with SH or TH. The growth performance, feed utilization, diet digestibility and antioxidant capacity of L. vannamei can be effectively improved by supplementing their diet with SH rather than the traditional SLP. The optimum inclusion level of SH is approximately 1% to completely replace SLP in L. vannamei diets containing high levels of soybean meal.

AUTHOR CONTRIBUTIONS

Buddhi E. Gunathilaka participated in the feeding trial, sampling, analyses and manuscript preparation. Soohwan Kim mainly conducted the feedings and analysed the samples. Mikael Herault and Vincent Fournier designed the experiment, provided ingredients and analysed the results. Kyeong-Jun Lee organized and supervised the whole experiment and completed the manuscript.

ACKNOWLEDGEMENTS

This study was supported by AQUATIV (Aquaculture Division of DIANA, Member of SYMRISE Group), Elven, France and supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A03033553).

CONFLICT OF INTEREST

The authors declare that they have no competing financial interest or personal relationships that could have influenced this paper.

Open Research

DATA AVAILABILITY STATEMENT

The data from this study are available from the corresponding author upon reasonable request.

REFERENCES

AOAC. (1995). Official methods of analysis of the Association of Official Analytical Chemists International ( 16th ed.). Association of Official Analytical Chemists.
Google Scholar
Bauer, W., Prentice-Hernandez, C., Tesser, M. B., Wasielesky, W., & Poersch, L. H. S. (2012). Substitution of fishmeal with microbial floc meal and soy protein concentrate in diets for the pacific white shrimp (Litopenaeus vannamei). Aquaculture, 342–343(1), 112–116. https://doi.org/10.1016/j.aquaculture.2012.02.023
10.1016/j.aquaculture.2012.02.023
CAS Web of Science® Google Scholar
Bui, H. T. D., Khosravi, S., Fournier, V., Herault, M., & Lee, K. J. (2014). Growth performance, feed utilization, innate immunity, digestibility and disease resistance of juvenile red seabream (Pagrus major) fed diets supplemented with protein hydrolysates. Aquaculture, 418–419, 11–16. https://doi.org/10.1016/j.aquaculture.2013.09.046
10.1016/j.aquaculture.2013.09.046
CAS Web of Science® Google Scholar
Cheng, C. H., Guo, Z. X., Ye, C. X., & Wang, A. L. (2018). Effect of dietary astaxanthin on the growth performance, non-specific immunity, and antioxidant capacity of pufferfish (Takifugu obscurus) under high temperature stress. Fish Physiology and Biochemistry, 44(1), 209–218. https://doi.org/10.1007/s10695-017-0425-5
10.1007/s10695-017-0425-5
CAS PubMed Web of Science® Google Scholar
Cheng, M. L., Wang, H. C., Hsu, K. C., & Hwang, J. S. (2015). Anti-inflammatory peptides from enzymatic hydrolysates of tuna cooking juice. Food and Agricultural Immunology, 26, 770–781. https://doi.org/10.1080/09540105.2015.1036352
10.1080/09540105.2015.1036352
CAS Web of Science® Google Scholar
Cho, C. Y., Slinger, S. J., & Bayley, H. S. (1982). Bioenergetics of salmonid fishes: Energy intake, expenditure and productivity. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 73, 25–41. https://doi.org/10.1016/0305-0491(82)90198-5
10.1016/0305-0491(82)90198-5
Web of Science® Google Scholar
Chuchird, N., Rorkwiree, P., & Rairat, T. (2015). Effect of dietary formic acid and astaxanthin on the survival and growth of Pacific white shrimp (Litopenaeus vannamei) and their resistance to Vibrio parahaemolyticus. SpringerPlus, 4(1), 1–12. https://doi.org/10.1186/s40064-015-1234-x
10.1186/s40064?015?1234?x
CAS PubMed Google Scholar
Ciaramella, M. A., Battison, A. L., & Horney, B. (2014). Measurement of tissue lipid reserves in the American lobster (Homarus americanus): Hemolymph metabolites as potential biomarkers of nutritional status. Journal of Crustacean Biology, 34(5), 629–638. https://doi.org/10.1163/1937240X-00002262
10.1163/1937240X?00002262
Web of Science® Google Scholar
Córdova-Murueta, J. H., & García-Carreño, F. L. (2002). Nutritive value of squid and hydrolyzed protein supplement in shrimp feed. Aquaculture, 210(1–4), 371–384. https://doi.org/10.1016/S0044-8486(02)00011-X
10.1016/S0044‐8486(02)00011‐X
CAS Web of Science® Google Scholar
Costa-Bomfim, C. N., Silva, V. A., Bezerra, R. S., Druzian, J. I., & Cavalli, R. O. (2017). Growth, feed efficiency and body composition of juvenile cobia (Rachycentron canadum Linnaeus, 1766) fed increasing dietary levels of shrimp protein hydrolysate. Aquaculture Research, 48(4), 1759–1766. https://doi.org/10.1111/are.13013
10.1111/are.13013
CAS Web of Science® Google Scholar
Cruz-Suárez, L. E., Guillaume, J., & Van Wormhoudt, A. (1989). Effect of squid extracts on time course appearance of glucose and free amino acids in haemolymph in Penaeus japonicus after feeding: Preliminary results. Aquaculture, 76(1–2), 57–65. https://doi.org/10.1016/0044-8486(89)90251-2
10.1016/0044?8486(89)90251?2
Google Scholar
Divakaran, S., Obaldo, L. G., & Forster, I. P. (2002). Note on the methods for determination of chromic oxide in shrimp feeds. Journal of Agricultural and Food Chemistry, 50(3), 464–467. https://doi.org/10.1021/jf011112s
10.1021/jf011112s
CAS PubMed Web of Science® Google Scholar
Elias, R. J., Kellerby, S. S., & Decker, E. A. (2008). Antioxidant activity of proteins and peptides. Critical Reviews in Food Science and Nutrition, 48(5), 430–441. https://doi.org/10.1080/10408390701425615
10.1080/10408390701425615
CAS PubMed Web of Science® Google Scholar
Ellis, A. E. (1990). Serum antiprotease in fish. In J. S. Stolen, T. C. Fletcher, D. P. Anderson, W. B. Roberson, & W. B. Muiswinkel (Eds.), Techniques in fish immunology (pp. 95–99). SOS Publication.
Google Scholar
Estruch, G., Collado, M. C., Monge-Ortiz, R., Tomás-Vidal, A., Jover-Cerdá, M., Peñaranda, D. S., & Martínez-Llorens, S. (2018). Long-term feeding with high plant protein based diets in gilthead seabream (Sparus aurata, L.) leads to changes in the inflammatory and immune related gene expression at intestinal level. BMC Veterinary Research, 14(1), 1–15. https://doi.org/10.1186/s12917-018-1626-6
10.1186/s12917?018?1626?6
PubMed Web of Science® Google Scholar
Folch, J., Lees, M., & Stanley, G. S. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226(1), 497–509.
10.1016/S0021-9258(18)64849-5
CAS PubMed Web of Science® Google Scholar
Galindo, C., Gaxiola, G., Cuzon, G., & Chiappa-Carrara, X. (2009). Physiological and biochemical variations during the molt cycle in juvenile Litopenaeus vannamei under laboratory conditions. Journal of Crustacean Biology, 29(4), 544–549. https://doi.org/10.1651/08-3094.1
10.1651/08?3094.1
Web of Science® Google Scholar
Gisbert, E., Fournier, V., Solovyev, M., Skalli, A., & Andree, K. B. (2018). Diets containing shrimp protein hydrolysates provided protection to European sea bass (Dicentrarchus labrax) affected by a Vibrio pelagius natural infection outbreak. Aquaculture, 495, 136–143. https://doi.org/10.1016/j.aquaculture.2018.04.051
10.1016/j.aquaculture.2018.04.051
CAS Web of Science® Google Scholar
Guerard, F., Guimas, L., & Binet, A. (2002). Production of tuna waste hydrolysates by a commercial neutral protease preparation. Journal of Molecular Catalysis B: Enzymatic, 19(20), 489–498. https://doi.org/10.1016/S1381-1177(02)00203-5
10.1016/S1381?1177(02)00203?5
Google Scholar
Gunathilaka, B. E., Khosravi, S., Herault, M., Fournier, V., Lee, C., Jeong, J., & Lee, K. (2020). Evaluation of shrimp or tilapia protein hydrolysate at graded dosages in low fish meal diet for olive flounder (Paralichthys olivaceus). Aquaculture Nutrition, 26(5), 1592–1603. https://doi.org/10.1111/anu.13105
10.1111/anu.13105
CAS Web of Science® Google Scholar
Gutiérrez, A., Nieto, J., Pozo, F., Stern, S., & Schoofs, L. (2007). Effect of insulin/IGF-I like peptides on glucose metabolism in the white shrimp (Penaeus vannamei). General and Comparative Endocrinology, 153(1–3), 170–175.
10.1016/j.ygcen.2007.04.014
CAS PubMed Web of Science® Google Scholar
Gyan, W. R., Yang, Q., Tan, B., Jan, S. S., Jiang, L., Chi, S., & Shuang, Z. (2020). Effects of antimicrobial peptides on growth, feed utilization, serum biochemical indices and disease resistance of juvenile shrimp, Litopenaeus vannamei. Aquaculture Research, 51(3), 1222–1231. https://doi.org/10.1111/are.14473
10.1111/are.14473
CAS Web of Science® Google Scholar
He, L., He, T., Farrar, S., Ji, L., Liu, T., & Ma, X. (2017). Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cellular Physiology and Biochemistry, 44, 532–553. https://doi.org/10.1159/000485089
10.1159/000485089
PubMed Web of Science® Google Scholar
Hernández, C., Olvera-Novoa, M. A., Smith, D. M., Hardy, R. W., & Gonzalez-Rodriguez, B. (2011). Enhancement of shrimp (Litopenaeus vannamei) diets based on terrestrial protein sources via the inclusion of tuna by-product protein hydrolysates. Aquaculture, 317, 117–123. https://doi.org/10.1016/j.aquaculture.2011.03.041
10.1016/j.aquaculture.2011.03.041
CAS Web of Science® Google Scholar
Hernández-López, J., Gollas-Galván, T., & Vargas-Albores, F. (1996). Activation of the prophenoloxidase system of the brown shrimp (Penaeus californiensis Holmes). Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 113(1), 61–66. https://doi.org/10.1016/0742-8413(95)02033-0
10.1016/0742-8413(95)02033-0
Web of Science® Google Scholar
Herpandi, H. N., Rosma, A., & Wan Nadiah, W. A. (2011). The tuna fishing industry: A new outlook on fish protein hydrolysates. Comprehensive Reviews in Food Science and Food Safety, 10(4), 195–207. https://doi.org/10.1111/j.1541-4337.2011.00155.x
10.1111/j.1541?4337.2011.00155.x
CAS Web of Science® Google Scholar
Hwang, I., Uddin, M. J., Pak, E. S., Kang, H., Jin, E. J., Jo, S., & Ha, H. (2020). The impaired redox balance in peroxisomes of catalase knockout mice accelerates nonalcoholic fatty liver disease through endoplasmic reticulum stress. Free Radical Biology and Medicine, 148, 22–32.
10.1016/j.freeradbiomed.2019.12.025
CAS PubMed Web of Science® Google Scholar
Je, J. Y., Lee, K. H., Lee, M. H., & Ahn, C. B. (2009). Antioxidant and antihypertensive protein hydrolysates produced from tuna liver by enzymatic hydrolysis. Food Research International, 42(9), 1266–1272. https://doi.org/10.1016/j.foodres.2009.06.013
10.1016/j.foodres.2009.06.013
CAS Web of Science® Google Scholar
Ji, P. F., Yao, C. L., & Wang, Z. Y. (2009). Immune response and gene expression in shrimp (Litopenaeus vannamei) hemocytes and hepatopancreas against some pathogen-associated molecular patterns. Fish & Shellfish Immunology, 27(4), 563–570. https://doi.org/10.1016/j.fsi.2009.08.001
10.1016/j.fsi.2009.08.001
CAS PubMed Web of Science® Google Scholar
Jung, H., Lyons, R. E., Hurwood, D. A., & Mather, P. B. (2013). Genes and growth performance in crustacean species: A review of relevant genomic studies in crustaceans and other taxa. Reviews in Aquaculture, 5(2), 77–110. https://doi.org/10.1111/raq.12005
10.1111/raq.12005
Web of Science® Google Scholar
Kalinowski, C. T., Robaina, L. E., & Izquierdo, M. S. (2011). Effect of dietary astaxanthin on the growth performance, lipid composition and post-mortem skin colouration of red porgy (Pagrus pagrus). Aquaculture International, 19(5), 811–823. https://doi.org/10.1007/s10499-010-9401-0
10.1007/s10499?010?9401?0
CAS Web of Science® Google Scholar
Kandra, P., Challa, M. M., & Jyothi, H. K. P. (2012). Efficient use of shrimp waste: Present and future trends. Applied Microbiology and Biotechnology, 93, 17–29. https://doi.org/10.1007/s00253-011-3651-2
10.1007/s00253?011?3651?2
CAS PubMed Web of Science® Google Scholar
Khosravi, S., Bui, H. T. D., Herault, M., Fournier, V., Kim, K. D., Lee, B. J., & Lee, K. J. (2018). Supplementation of protein hydrolysates to a low-fishmeal diet improves growth and health status of juvenile olive flounder, Paralichthys olivaceus. Journal of the World Aquaculture Society, 49(5), 897–911. https://doi.org/10.1111/jwas.12436
10.1111/jwas.12436
CAS Web of Science® Google Scholar
Khosravi, S., Bui, H. T. D., Rahimnejad, S., Herault, M., Fournier, V., Kim, S. S., & Lee, K. J. (2015). Dietary supplementation of marine protein hydrolysates in fish-meal based diets for red sea bream (Pagrus major) and olive flounder (Paralichthys olivaceus). Aquaculture, 435, 371–376. https://doi.org/10.1016/j.aquaculture.2014.10.019
10.1016/j.aquaculture.2014.10.019
CAS Web of Science® Google Scholar
Leal, A. L. G., de Castro, P. F., de Lima, J. P. V., de Souza Correia, E., & de Souza Bezerra, R. (2010). Use of shrimp protein hydrolysate in Nile tilapia (Oreochromis niloticus, L.) feeds. Aquaculture International, 18(4), 635–646. https://doi.org/10.1007/s10499-009-9284-0
10.1007/s10499-009-9284-0
Web of Science® Google Scholar
Leduc, A., Hervy, M., Rangama, J., Delépée, R., Fournier, V., & Henry, J. (2018). Shrimp by-product hydrolysate induces intestinal myotropic activity in European seabass (Dicentrarchus labrax). Aquaculture, 497, 380–388. https://doi.org/10.1016/j.aquaculture.2018.08.009
10.1016/j.aquaculture.2018.08.009
CAS Web of Science® Google Scholar
Lee, S. H., Qian, Z. J., & Kim, S. K. (2010). A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysate and its antihypertensive effect in spontaneously hypertensive rats. Food Chemistry, 118(1), 96–102. https://doi.org/10.1016/j.foodchem.2009.04.086
10.1016/j.foodchem.2009.04.086
CAS Web of Science® Google Scholar
Li, F., Huang, S., Lu, X., Wang, J., Lin, M., An, Y., & Cai, M. (2018). Effects of dietary supplementation with algal astaxanthin on growth, pigmentation, and antioxidant capacity of the blood parrot (Cichlasoma citrinellum × Cichlasoma synspilum). Journal of Oceanology and Limnology, 36(5), 1851–1859. https://doi.org/10.1007/s00343-019-7172-7
10.1007/s00343-019-7172-7
CAS Web of Science® Google Scholar
Li, M., Wu, W., Zhou, P., Xie, F., Zhou, Q., & Mai, K. (2014). Comparison effect of dietary astaxanthin and Haematococcus pluvialis on growth performance, antioxidant status and immune response of large yellow croaker Pseudosciaena crocea. Aquaculture, 434, 227–232. https://doi.org/10.1016/j.aquaculture.2014.08.022
10.1016/j.aquaculture.2014.08.022
CAS Web of Science® Google Scholar
Liao, X.-Z., Hu, S.-K., Wang, B., Qin, H.-P., Zhao, J.-C., He, Z.-H., Chen, X.-Y., Liu, Y.-S., Qu, P., Sun, C.-B., & Zhang, S. (2019). Dietary supplementation with polypeptides improved growth performance, antibacterial immune and intestinal microbiota structure of Litopenaeus vannamei. Fish & Shellfish Immunology, 92, 480–488. https://doi.org/10.1016/j.fsi.2019.06.033
10.1016/j.fsi.2019.06.033
CAS PubMed Web of Science® Google Scholar
Lim, K. C., Yusoff, F. M., Shariff, M., & Kamarudin, M. S. (2018). Astaxanthin as feed supplement in aquatic animals. Reviews in Aquaculture, 10(3), 738–773. https://doi.org/10.1111/raq.12200
10.1111/raq.12200
Web of Science® Google Scholar
Liu, H., Luo, P., Chen, S., & Shang, J. (2011). Effects of squid ink on growth performance, antioxidant functions and immunity in growing broiler chickens. Asian-Australasian Journal of Animal Sciences, 24(12), 1752–1756. https://doi.org/10.5713/ajas.2011.11128
10.5713/ajas.2011.11128
CAS Web of Science® Google Scholar
Lugo, J. M., Carpio, Y., Morales, R., Rodríguez-Ramos, T., Ramos, L., & Estrada, M. P. (2013). First report of the pituitary adenylate cyclase activating polypeptide (PACAP) in crustaceans: Conservation of its functions as growth promoting factor and immunomodulator in the white shrimp (Litopenaeus vannamei). Fish & Shellfish Immunology, 35(6), 1788–1796. https://doi.org/10.1016/j.fsi.2013.08.028
10.1016/j.fsi.2013.08.028
CAS PubMed Web of Science® Google Scholar
Magnadóttir, B., Jónsdóttir, H., Helgason, S., Björnsson, B., Jøgensen, T., & Pilström, L. (1999). Humoral immune parameters in Atlantic cod (Gadus morhua L.). II. The effects of size and gender under different environmental conditions. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 122(2), 181–188. https://doi.org/10.1016/S0305-0491(98)10157-8
10.1016/S0305?0491(98)10157?8
CAS PubMed Web of Science® Google Scholar
Mai, K., Li, H., Ai, Q., Duan, Q., Xu, W., Zhang, C., & Liufu, Z. (2006). Effects of dietary squid viscera meal on growth and cadmium accumulation in tissues of Japanese seabass, Lateolabrax japonicus (Cuvier 1828). Aquaculture Research, 37(11), 1063–1069. https://doi.org/10.1111/j.1365-2109.2006.01529.x
10.1111/j.1365?2109.2006.01529.x
CAS Web of Science® Google Scholar
Mendis, E., Rajapakse, N., & Kim, S. K. (2005). Antioxidant properties of a radical-scavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysate. Journal of Agricultural and Food Chemistry, 53(3), 581–587. https://doi.org/10.1021/jf048877v
10.1021/jf048877v
CAS PubMed Web of Science® Google Scholar
Mercier, L., Palacios, E., Campa-Córdova, Á. I., Tovar-Ramírez, D., Hernández-Herrera, R., & Racotta, I. S. (2006). Metabolic and immune responses in Pacific whiteleg shrimp (Litopenaeus vannamei) exposed to a repeated handling stress. Aquaculture, 258(1–4), 633–640. https://doi.org/10.1016/j.aquaculture.2006.04.036
10.1016/j.aquaculture.2006.04.036
Web of Science® Google Scholar
Moss, A. S., Koshio, S., Ishikawa, M., Yokoyama, S., Nhu, T. H., Dawood, M. A. O., & Wang, W. (2018). Replacement of squid and krill meal by snail meal (Buccinum striatissimum) in practical diets for juvenile of kuruma shrimp (Marsupenaeus japonicus). Aquaculture Research, 49(9), 3097–3106. https://doi.org/10.1111/are.13772
10.1111/are.13772
CAS Web of Science® Google Scholar
Murakawa, K., Fukunaga, K., Tanouchi, M., Hosokawa, M., Hossain, Z., & Takahashi, K. (2007). Therapy of myeloma in vivo using marine phospholipid in combination with Agaricus blazei Murill as an immune respond activator. Journal of Oleo Science, 56(4), 179–188. https://doi.org/10.5650/jos.56.179
10.5650/jos.56.179
CAS PubMed Google Scholar
Navarro, C., Civera, R., Arjona, O., Rivera-Perez, C., García, H. S., Hurtado-Oliva, M. Á., & Palacios, E. (2020). Stress response and lipid composition in shrimp (Litopenaeus vannamei) fed diets enriched with squid or scallop viscera meal. Aquaculture Research, 51(4), 1602–1622. https://doi.org/10.1111/are.14508
10.1111/are.14508
CAS Web of Science® Google Scholar
Nguyen, H. T. M., Pérez-Gálvez, R., & Bergé, J. P. (2012). Effect of diets containing tuna head hydrolysates on the survival and growth of shrimp (Penaeus vannamei). Aquaculture, 324–325, 127–134. https://doi.org/10.1016/j.aquaculture.2011.11.014
10.1016/j.aquaculture.2011.11.014
CAS Web of Science® Google Scholar
Niu, J., Tian, L. X., Liu, Y. J., Yang, H. J., Ye, C. X., Gao, W., & Mai, K. S. (2009). Effect of dietary astaxanthin on growth, survival, and stress tolerance of postlarval shrimp, Litopenaeus vannamei. Journal of the World Aquaculture Society, 40(6), 795–802. https://doi.org/10.1111/j.1749-7345.2009.00300.x
10.1111/j.1749?7345.2009.00300.x
Web of Science® Google Scholar
Paibulkichakul, C., Piyatiratitivorakul, S., Sorgeloos, P., & Menasveta, P. (2008). Improved maturation of pond-reared, black tiger shrimp (Penaeus monodon) using fish oil and astaxanthin feed supplements. Aquaculture, 282(1–4), 83–89.
10.1016/j.aquaculture.2008.06.006
CAS Web of Science® Google Scholar
Plascencia-Jatomea, M., Olvera-Novoa, M. A., Arredondo-Figueroa, J. L., Hall, G. M., & Shirai, K. (2002). Feasibility of fishmeal replacement by shrimp head silage protein hydrolysate in Nile tilapia (Oreochromis niloticus L) diets. Journal of the Science of Food and Agriculture, 82(7), 753–759. https://doi.org/10.1002/jsfa.1092
10.1002/jsfa.1092
CAS Web of Science® Google Scholar
Qian, Z. J., Je, J. Y., & Kim, S. K. (2007). Antihypertensive effect of angiotensin I converting enzyme-inhibitory peptide from hydrolysates of bigeye tuna dark muscle, Thunnus obesus. Journal of Agricultural and Food Chemistry, 55(21), 8398–8403. https://doi.org/10.1021/jf0710635
10.1021/jf0710635
CAS PubMed Web of Science® Google Scholar
Racotta, I. S., & Palacios, E. (1998). Hemolymph metabolic variables in response to experimental manipulation stress and serotonin injection in Penaeus vannamei. Journal of the World Aquaculture Society, 29(3), 351–356. https://doi.org/10.1111/j.1749-7345.1998.tb00658.x
10.1111/j.1749?7345.1998.tb00658.x
Web of Science® Google Scholar
Ravallec-Plé, R., & Van Wormhoudt, A. (2003). Secretagogue activities in cod (Gadus morhua) and shrimp (Penaeus aztecus) extracts and alcalase hydrolysates determined in AR4-2J pancreatic tumour cells. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 134(4), 669–679. https://doi.org/10.1016/S1096-4959(03)00026-5
10.1016/S1096?4959(03)00026?5
CAS PubMed Web of Science® Google Scholar
Robert, M., Zatylny-Gaudin, C., Fournier, V., Corre, E., Le Corguillé, G., Bernay, B., & Henry, J. (2014). Transcriptomic and peptidomic analysis of protein hydrolysates from the white shrimp (L. vannamei). Journal of Biotechnology, 186, 30–37. https://doi.org/10.1016/j.jbiotec.2014.06.020
10.1016/j.jbiotec.2014.06.020
CAS PubMed Web of Science® Google Scholar
Saidi, S., Deratani, A., Belleville, M. P., & Amar, R. B. (2014). Production and fractionation of tuna by-product protein hydrolysate by ultrafiltration and nanofiltration: Impact on interesting peptides fractions and nutritional properties. Food Research International, 65, 453–461. https://doi.org/10.1016/j.foodres.2014.04.026
10.1016/j.foodres.2014.04.026
CAS Web of Science® Google Scholar
Shahidi, F., & Synowiecki, J. (1991). Isolation and characterization of nutrients and value-added products from snow crab (Chinoecetes opilio) and shrimp (Pandalus Borealis) processing discards. Journal of Agricultural and Food Chemistry, 39(8), 1527–1532. https://doi.org/10.1021/jf00008a032
10.1021/jf00008a032
CAS Web of Science® Google Scholar
Siddik, M. A. B., Howieson, J., & Fotedar, R. (2019). Beneficial effects of tuna hydrolysate in poultry by-product meal diets on growth, immune response, intestinal health and disease resistance to Vibrio harveyi in juvenile barramundi, Lates calcarifer. Fish & Shellfish Immunology, 89, 61–70. https://doi.org/10.1016/j.fsi.2019.03.042
10.1016/j.fsi.2019.03.042
CAS PubMed Web of Science® Google Scholar
Smith, D. M., Tabrett, S. J., Barclay, M. C., & Irvin, S. J. (2005). The efficacy of ingredients included in shrimp feeds to stimulate intake. Aquaculture Nutrition, 11(4), 263–272. https://doi.org/10.1111/j.1365-2095.2005.00349.x
10.1111/j.1365?2095.2005.00349.x
CAS Web of Science® Google Scholar
Song, Y. L., & Hsieh, Y. T. (1994). Immunostimulation of tiger shrimp (Penaeus monodon) hemocytes for generation of microbicidal substances: Analysis of reactive oxygen species. Developmental & Comparative Immunology, 18(3), 201–209.
10.1016/0145-305X(94)90012-4
CAS PubMed Web of Science® Google Scholar
Stuck, K. C., Watts, S. A., & Wang, S. Y. (1996). Biochemical responses during starvation and subsequent recovery in postlarval Pacific white shrimp, Penaeus vannamei. Marine Biology, 125(1), 33–45.
10.1007/BF00350758
CAS Web of Science® Google Scholar
Suárez, J. A., Gaxiola, G., Mendoza, R., Cadavid, S., Garcia, G., Alanis, G., & Cuzon, G. (2009). Substitution of fish meal with plant protein sources and energy budget for white shrimp (Litopenaeus vannamei) (Boone, 1931). Aquaculture, 289(1–2), 118–123. https://doi.org/10.1016/j.aquaculture.2009.01.001
10.1016/j.aquaculture.2009.01.001
CAS Web of Science® Google Scholar
Suresh, A. V., & Nates, S. (2011). Attractability and palatability of protein ingredients of aquatic and terrestrial animal origin, and their practical value for blue shrimp, Litopenaeus stylirostris fed diets formulated with high levels of poultry byproduct meal. Aquaculture, 319(1–2), 132–140. https://doi.org/10.1016/j.aquaculture.2011.06.039
10.1016/j.aquaculture.2011.06.039
CAS Web of Science® Google Scholar
Tacon, A. G. J., & Barg, U. C. (1998). Major challenges to feed development for marine and diadromous finfish and crustacean species. In S. S. De Silva (Ed.), Tropical mariculture (pp. 171–208). Academic Press.
10.1016/B978-012210845-7/50006-4
Google Scholar
Teshima, S. I., Koshio, S., Ishikawa, M., Alam, M. S., & Hernandez, L. H. H. (2004). Effects of protein and lipid sources on the growth and survival of red sea bream (Pagrus major) and Japanese flounder (Paralichthys olivaceus) receiving micro-bound diets during larval and early juvenile stage. Aquaculture Nutrition, 10(4), 279–287. https://doi.org/10.1111/j.1365-2095.2004.00303.x
10.1111/j.1365?2095.2004.00303.x
CAS Web of Science® Google Scholar
Wu, H. C., Chen, H. M., & Shiau, C. Y. (2003). Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus). Food Research International, 36(9–10), 949–957. https://doi.org/10.1016/S0963-9969(03)00104-2
10.1016/S0963?9969(03)00104?2
CAS Web of Science® Google Scholar
Xie, J. J., Chen, X., Liu, Y. J., Tian, L. X., Xie, S. W., & Niu, J. (2017). Effects of dietary astaxanthin on growth performance, hepatic antioxidative activity, hsp70, and HIF-1α gene expression of juvenile golden pompano (Trachinotus ovatus). Israeli Journal of Aquaculture-Bamidgeh., 69(1), 21026.
Google Scholar
Ye, J. D., Wang, K., Li, F. D., Sun, Y. Z., & Liu, X. H. (2011). Incorporation of a mixture of meat and bone meal, poultry by-product meal, blood meal and corn gluten meal as a replacement for fish meal in practical diets of Pacific white shrimp (Litopenaeus vannamei) at two dietary protein levels. Aquaculture Nutrition, 17(2), e337–e347. https://doi.org/10.1111/j.1365-2095.2010.00768.x
10.1111/j.1365?2095.2010.00768.x
Web of Science® Google Scholar
Yildiz, H. Y., & Benli, A. C. K. (2004). Nitrite toxicity to crayfish, Astacus leptodactylus, the effects of sublethal nitrite exposure on hemolymph nitrite, total hemocyte counts, and hemolymph glucose. Ecotoxicology and Environmental Safety, 59(3), 370–375. https://doi.org/10.1016/j.ecoenv.2003.07.007
10.1016/j.ecoenv.2003.07.007
CAS PubMed Web of Science® Google Scholar
Zhang, S. P., Li, J. F., Wu, X. C., Zhong, W. J., Xian, J. A., Liao, S. A., Miao, Y. T., & Wang, A. L. (2013). Effects of different dietary lipid level on the growth, survival and immune-relating genes expression in Pacific white shrimp, Litopenaeus vannamei. Fish & Shellfish Immunology, 34(5), 1131–1138. https://doi.org/10.1016/j.fsi.2013.01.016
10.1016/j.fsi.2013.01.016
CAS PubMed Web of Science® Google Scholar

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Marine protein hydrolysates as a substitute of squid-liver powder in diets for Pacific white shrimp (Litopenaeus vannamei)

Abstract

1 INTRODUCTION

2 MATERIALS AND METHODS

2.1 Experimental design and diet preparation

2.2 Shrimp and feeding trial

2.3 Sample collection

2.4 Sample analyses

2.5 Estimation of apparent digestibility coefficients

2.6 Statistical analysis

3 RESULTS

4 DISCUSSION

AUTHOR CONTRIBUTIONS

ACKNOWLEDGEMENTS

CONFLICT OF INTEREST

Open Research

DATA AVAILABILITY STATEMENT

REFERENCES

Citing Literature

References

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Marine protein hydrolysates as a substitute of squid-liver powder in diets for Pacific white shrimp (Litopenaeus vannamei)

Abstract

1 INTRODUCTION

2 MATERIALS AND METHODS

2.1 Experimental design and diet preparation

2.2 Shrimp and feeding trial

2.3 Sample collection

2.4 Sample analyses

2.5 Estimation of apparent digestibility coefficients

2.6 Statistical analysis

3 RESULTS

4 DISCUSSION

AUTHOR CONTRIBUTIONS

ACKNOWLEDGEMENTS

CONFLICT OF INTEREST

Open Research

DATA AVAILABILITY STATEMENT

REFERENCES

Citing Literature

References

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