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Dietary amino acid profiles and growth performance in juvenile kuruma prawn Marsupenaeus japonicus
Comparative Biochemistry and Physiology Part B 133 (2002) 289–297
Dietary amino acid profiles and growth performance in juvenile kuruma prawn Marsupenaeus japonicus Md. Shah Alam, Shin-ichi Teshima*, Dedy Yaniharto1, Manabu Ishikawa, Shunsuke Koshio Laboratory of Aquatic Animal Nutrition, Faculty of Fisheries, Kagoshima University, Shimoarata 4-50-20, Kagoshima 890-0056, Japan Received 19 March 2002; received in revised form 16 June 2002; accepted 25 June 2002
Abstract To assess the reference dietary amino acid profiles for juvenile kuruma prawn Marsupenaeus japonicus a feeding trial was conducted using six semi-purified diets containing casein-gelatin and pre-coated supplemental crystalline amino acids (CAA) and a control diet containing intact protein (casein-gelatin). Pre-coated CAA were supplemented to the diets to simulate dietary amino acid profiles to those of the prawn egg protein (PEP), prawn larvae whole body protein (PLP), prawn juvenile whole body protein (PJP), squid meal protein (SMP), short-necked clam protein (SNP) and brown fish meal protein (BFP). The result showed that kuruma prawn juveniles are capable of utilizing the pre-coated CAA and higher growth performances were observed in the groups fed the PJP, SMP and the control diets than those fed the PLP, SNP, BFP and PEP diets. The essential amino acid proportions (AyE ratios) of the whole body of kuruma prawn differ slightly when compared with the other penaeids or freshwater prawn. The results suggest that PJP and SMP would be suitable as a reference dietary amino acid profile for juvenile prawn. 䊚 2002 Elsevier Science Inc. All rights reserved. Keywords: Kuruma prawn; Marsupenaeus japonicus; Reference protein; Amino acid profile; Pre-coating; Crystalline amino acid; Utilization; AyE ratio
1. Introduction Since high protein diets are needed for good growth of most aquatic animals (NRC, 1993), estimation of minimum requirements of essential amino acids (EAA) is indispensable to formulate cost-effective diets. The quantitative EAA requi-
*Corresponding author. Tel.: q81-99-286-4181; fax: q8199-286-4184. E-mail address: [email protected] (S.-i. Teshima). 1 Present address: Agency for the Assessment and Application of Technology (BPPT), Jaluan, M. Husni, Thamrin No. 8; Jakarta Pusat 10340 – Indonesia.
rements of fish and crustaceans are often determined by feeding experiments with diets containing graded levels of the particular amino acid to be examined (Wilson, 1989). However, such a method requires much labor, expense and time. In addition, adaptation of the method to slow-eating aquatic animals such as prawns faces the obstacle that supplemental EAA leaches into the water before being consumed. Accordingly, several attempts have been made to assess the EAA requirements based on methods using ideal protein and reference amino acid patterns (Boghen et al., 1982; Wilson and Poe, 1985; Castell, 1990; Moon and Gatlin, 1991; Mambrini and Kaushik, 1995).
1096-4959/02/$ - see front matter 䊚 2002 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 6 - 4 9 5 9 Ž 0 2 . 0 0 1 6 5 - 3
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Table 1 Composition of the diets (g per 100 g dry diet) used for juvenile kuruma prawn Ingredient
CAA-dieta
Control
Casein Gelatin Amino acid mixb Cholesterol Squid liver oilc Soybean lecithind Vitamin mixe Mineral mixf a-Starch Sucrose Glucose Carboxymethyl cellulose k-Carrageenan a-Cellulose Attractantsg
17.0 8.0 20.0 1.0 4.0 4.0 7.0 4.0 8.0 7.0 5.0 4.0 2.5 7.1 1.4
30.0 15.0 0 1.0 4.0 4.0 7.0 4.0 8.0 7.0 5.0 4.0 2.5 7.1 1.4
a
Amino acid patterns of the diets were simulated to those of prawn egg protein (PEP), prawn larvae protein (PLP), prawn juvenile protein (PJP), squid meal protein (SMP) shortnecked clam protein (SNP) and brown fish meal protein (BFP). b See Table 4. c Feed oil squid (Riken Vitamin, Tokyo, Japan). d Kanto Chemical Co., Inc., Tokyo, Japan. e (mgy100 g) r-Amino benzoic acid, 47.24; biotin, 1.89; inositol, 1889.41; nicotinic acid, 188.94; ca-pantothenate, 283.41; pyridoxine–HCl, 56.70; riboflavin, 37.77; thiamin– HCl, 18.88; menadione, 18.93; vitamin A-palmitate, 47.53; atocopherol, 94.47; cyanocobalamin, 0.40; calciferol, 5.63; ascorbyl-2-phosphate-Mg, 1474.86; folic acid, 3.79 and choline chloride, 2830.13. f (mgy100 g dry diet): MgSO4Ø7H2O, 1422; NaH2PO4Ø2H2O, 370; KH2PO4, 935; Ca(H2PO4)2Ø2H2O, 1273. g (gy100 g): Glucosamine–HCl, 0.8; sodium citrate 0.3; sodium succinate, 0.3.
The EAA requirements of fish have been considered not to vary markedly among species (Kaushik, 1998). However, crustaceans such as prawns are different to fish in that they have an openvessel system and contain higher levels of nonprotein nitrogen compounds such as free amino acids in the body (Dall and Smith, 1987). Amino acids also play a role in osmotic regulation in crustaceans (Cheng and Chen, 1998). Considering these facts together, we assume that the EAA requirements of crustaceans possibly differ from those of fish. Although there are reports on the EAA requirements of prawn (Cowey and Forster, 1971; Shewbart et al., 1972; Kanazawa and Teshima, 1981; Smith and Dall, 1991; Chen et al., 1992; Fox et al., 1995; Millamena et al., 1996)
which were determined by dose-response or radioisotope methods, the knowledge of EAA requirements of crustaceans are only little and fragmentary. In a previous study, we have successfully evaluated the EAA requirements of the Japanese flounder, Paralichthys olivaceus, by using pre-coated crystalline amino acids (CAA) which enable retardation of the leaching of CAA into water (Alam et al., 2002). The kuruma prawn, Marsupenaeus japonicus, is the most popular penaeid with a high market value in Japan and many nutritional studies on this prawn have been conducted (Teshima and Kanazawa, 1971; Teshima et al., 1986, 1989, 2001; Shiau, 1998; Ishikawa et al., 2002). However, the quantitative EAA requirements of this species have not been established. Hence, we intended to evaluate the EAA requirements of the prawn by using the same method as used in the Japanese flounder in the viewpoint of comparative nutrition, with special interest in the difference in EAA requirements between fish and prawn. This paper deals with the relationship between the growth performance of the prawn, M. japonicus, and dietary amino acid profiles by feeding test diets containing provisional reference amino acid profiles. 2. Materials and methods 2.1. Experimental diets The basal and proximate compositions of the CAA-based diets and the control diets are shown in Tables 1 and 2, respectively. The amino acid profiles of prawn M. japonicus egg protein (PEP), prawn larvae (mysis) whole body protein (PLP), prawn (50 days after hatching) whole body juvenile protein (PJP), squid meal protein (Nippon Suisan Co., Ltd., Japan) (SMP), short-necked clam (locally purchased) protein (SNP) and brown fish meal (Nippon Suisan Co., Ltd., Japan) protein Table 2 The proximate composition of the test diets (% dry matter basis) fed to juvenile kuruma prawn Diet PEP PLP PJP
SMP SNP BFP Control
Crude protein 42.5 42.0 42.4 42.0 Total lipid 9.0 9.1 8.6 8.6 Ash 5.8 6.1 6.2 6.2 Moisture 16.1 16.4 15.6 15.4
42.6 42.0 43.4 9.1 8.6 8.9 6.2 6.1 6.1 15.4 15.6 14.8
M.S. Alam et al. / Comparative Biochemistry and Physiology Part B 133 (2002) 289–297 Table 3 Amino acid composition (g per 45 g protein) of different reference proteins Amino acid
PEP PLP PJP
SMP SNP BFP Control
Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Tryptophan Valine Aspartic acid Glutamic acid Serine Proline Glycine Alanine Tyrosine
3.14 1.56 2.66 3.41 3.66 1.07 2.08 2.46 0.28 3.06 3.42 7.63 1.85 2.05 1.75 2.42 1.91
3.72 1.11 1.99 3.30 3.48 2.14 1.91 1.85 0.80 1.86 4.54 6.35 1.55 2.78 2.06 2.16 1.92
3.71 1.01 1.85 2.87 3.17 1.27 1.93 1.79 0.65 2.17 4.12 6.45 2.00 4.56 2.56 2.16 1.78
4.59 0.90 1.88 3.19 3.40 1.30 1.66 1.51 1.00 1.88 4.14 6.76 1.10 3.42 3.38 2.23 1.58
3.44 0.96 1.68 2.67 3.59 0.63 1.46 1.61 0.38 1.85 4.51 6.29 1.85 2.16 2.97 2.55 1.18
2.85 1.61 1.86 3.40 4.34 1.12 2.05 1.98 1.21 2.21 4.25 5.44 1.43 2.34 2.40 2.59 1.79
2.49 0.71 1.76 3.02 3.48 0.91 2.17 1.37 0.75 2.21 2.86 7.85 1.37 5.24 3.62 2.11 2.02
(BFP) were considered as provisional references. Six semi-purified isocaloric diets were formulated to contain the amino acid patterns of PEP, PLP, PJP, SMP, SNP and BFP by supplementing casein– gelatin (approx. 2:1; 25 g) with pre-coated CAA (approx. 20 g). A control diet contained only intact protein sources (casein and gelatin, 2:1).
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The other ingredients were according to the recent nutrient requirement information for juvenile kuruma prawn (Teshima et al., 2001). The amino acid compositions of the reference proteins, the dietary ingredients, and the supplementation of CAA are shown in Tables 3 and 4. The preparation of precoated CAA and diets were as per Alam et al. (2000). In brief, CAA mixes were pre-coated with carboxymethylcellulose (CMC) to prevent leaching losses. CMC-bound CAA mixture and the other dry ingredients were added to the casein– gelatin paste. To improve the water stability of the diets, gelatinized k-carrageenan was added to the mixture. The pH of the diets was adjusted to 7.0– 7.5 by adding 4 N sodium hydroxide. The pellets with 2.1 mm diameter were obtained using a pelletizer and dried at 40 8C for 2 h. The dried pellets of prawn were steamed at 100 8C for 1 min in a cylindrical steamer to improve water stability. Diets were stored in freezer at y30 8C until used. 2.2. Experimental prawn and feeding protocol The brood stock prawn, M. japonicus were obtained from Matsumoto Suisan, Miyazaki, Japan, transported to the Kagoshima University facility, and acclimatized to laboratory conditions. The eggs were hatched and larvae were reared by
Table 4 Amino acid composition (g per 100 g dry diet) of ingredients and supplementation of CAA in different diets to simulate amino acid pattern of references proteins (45% protein) Amino acid
Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Tryptophan Valine Aspartic acid Glutamic acid Serine Proline Glycine Alanine Tyrosine a
Supplementation of CAAa
Supplied by Casein 17%
Gelatin 8%
Diet PEP
PLP
PJP
SMP
SNP
BFP
0.59 0.38 0.82 1.40 1.53 0.45 1.01 0.61 0.42 1.01 1.06 3.42 0.56 1.63 0.22 0.41 1.06
0.78 0.02 0.17 0.29 0.41 0.06 0.21 0.16 0.01 0.23 0.53 0.97 0.20 1.26 1.73 0.74 0.09
1.77 1.16 1.67 1.72 1.72 0.56 0.86 1.69 0 1.82 1.83 3.24 1.09 0 0 1.27 0.76
2.34 0.61 0.86 1.18 1.23 0.76 0.71 1.02 0.22 0.93 2.53 2.06 1.24 1.67 0.61 1.01 0.63
3.22 0.50 0.89 1.50 1.46 0.79 0.44 0.74 0.57 0.64 2.55 2.37 0.34 0.53 1.43 1.08 0.43
2.35 0.71 1.00 1.61 1.54 1.63 0.69 1.08 0.37 0.62 2.95 1.96 0.79 0 0.11 1.01 0.77
2.07 0.56 0.69 0.98 1.65 0.12 0.24 0.84 0 0.61 2.92 1.90 1.09 0 1.02 1.40 0.03
1.48 1.21 0.87 1.71 2.40 0.61 0.83 1.21 0.78 0.97 2.66 1.05 0.67 0 0.45 1.44 0.64
Supplemented as L-form (Ajinomoto Co., Inc., Japan).
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Table 5 Growth performance of the juvenile kuruma prawn fed test diets for 40 days Diet
Weight gain (%)
FCEa
PERb
APRc
Survival (%)
PEP PLP PJP SMP SNP BFP Control
131.3"4.7a 168.0"4.6b 206.7"4.7c 210.0"3.5c 170.7"3.5b 184.0"4.6b 212.7"5.5c
0.26"0.02 0.34"0.06 0.35"0.02 0.33"0.03 0.26"0.02 0.30"0.03 0.34"0.04
0.62"0.02a 0.81"0.03bc 0.96"0.05d 0.97"0.02d 0.70"0.02ab 0.86"0.03cd 0.92"0.04cd
9.4"0.3a 10.9"0.2ab 12.6"0.9b 13.2"0.7b 8.5"0.4a 10.5"0.64ab 10.9"0.6ab
78"4 78"4 73"7 75"4 80"0 80"0 78"4
Values are means"S.E. of triplicate groups. Means with different letter in the same column differ significantly (P-0.05). a Feed conversion efficiency (FCE)sweight gain (g)ytotal feed intake in dry weight basis (g). b Protein efficiency ratio (PER)sweight gain (g)ytotal protein intake in dry weight basis (g). c Apparent protein retention (APR)sprotein gain=100yprotein intake.
feeding live food (Ceatocerus and Artemia) and commercial diets (Higashimaru Feed, Shrimp seed production number 0-1, Kagoshima, Japan) for 2.5 months. Before starting the feeding trial, the juveniles were sorted to obtain equal size prawns and transferred into other tanks. Seven triplicate groups of prawns, 0.50"0.01 g (mean"S.D.) in initial body weight, were fed the respective test diets in 21 rectangular tanks with a plastic cover (30 l capacity, filled with 28 l sea water) for 40 days. The tanks were individually equipped with a false bottom and sand substrate that acted to filter the water. Water was circulated at 0.8 lymin through the action of an air-lift device. Fifteen prawns were stocked randomly in each tank and diets were given daily by hand at 8–10% of body weight at 08:30 and 16:30 h. Known quantities of diets were given, and fecal matter and uneaten diets were collected by siphoning from the tank every morning. Lighting was provided using a 12 h light:12 h dark regime. Body weight was measured every 10 days of feeding periods when the tanks and sand were cleaned and filled with seawater again. Water temperature, salinity and pH were monitored daily. The mean values of water temperature, salinity and pH value during the experimental period were 23.5"1.5 8C, 33.5"0.71 ppt and 8.02"1.8, respectively. These values were thought to be suitable environmental conditions for the prawn M. japonicus (Shigueno, 1975). 2.3. Biochemical analysis The protein fraction of dietary protein sources was obtained by homogenizing wet ingredients with 10% trichloroacetic acid (TCA) and succes-
sively washed with 7% TCA, ethanol, chloroformy methanol (3:1), and diethyl ether followed by centrifugation to collect precipitates. Amino acid analyses of protein fractions, ingredients of the test diets and whole body of the juveniles were conducted according to Teshima et al. (1986) using high performance liquid chromatography (HPLC), (Shimadzu LC-6A, Japan). Ash and moisture contents were analyzed by standard methods (AOAC, 1990). Crude lipid was determined by the method of Bligh and Dyer (1959). Crude protein was determined by the Kjeldahl method (totalN=6.25) with a Tecator Kjeltec System (1007) Digestion system, 1002 Distilling unit, and Titration unit, Sweden) using boric acid to trap released ammonia. 2.4. Statistical analysis All data were subjected to statistical verification using one-way analysis of variance (package super-ANOVA, ver. 1.11, Abacus Concepts, Berkeley, California, USA). Significant differences between means were evaluated by the Tukey– Kramer test (Kramer, 1956). Probabilities of P0.05 were considered significant. 3. Results Table 5 presents the mean weight gain, percent survival, feed conversion efficiency (FCE), protein efficiency ratio (PER) and apparent protein retention (APR) of the juveniles fed test diets. Percent survivals were not significantly affected among the dietary treatments. The highest weight gain was obtained for prawn fed the control, PJP and SMP diets, whereas the lowest weight gain was
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Table 6 Body composition (% dry matter basis) (means"S.E.) of kuruma prawn fed test diets. Means with different letters in the same column differ significantly (P-0.05) Diet
Dry matter
Crude protein
Total lipid
Ash
PEP PLP PJP SMP SNP BFP Control
23.2"0.5c 21.8"0.2abc 22.2"0.6abc 22.6"0.5bc 20.7"0.2ab 21.0"0.5ab 20.2"0.4a
58.1"0.2a 59.5"0.1b 59.1"0.1b 58.5"0.1ab 58.1"0.2a 58.1"0.2a 59.4"0.3b
9.8"0.2b 9.4"0.1ab 9.3"0.1ab 9.8" 0.1b 9.3"0.2ab 9.4"0.1ab 8.8"0.1a
23.2"0.2c 21.9"0.4ab 22.4"0.4bc 21.0"0.3a 22.4"0.1bc 22.4"0.1bc 21.8"0.1ab
found in prawn fed the PEP diet. Thus the weight gains for the prawn fed the PEP, PLP, SNP and BFP diets were significantly lower than those of the PJP, SMP and control diets. There was no significant difference in FCE between the different groups. The SMP, PJP, BFP and control diets gave statistically higher PER than the PEP and SNP diets. Protein, lipid and ash contents (% dry matter basis) of the whole body after growth trial were influenced by the different patterns of the dietary amino acid in the diets (Table 6). Significantly higher protein contents were observed from the prawn fed the PLP, PJP and control diets than the other diets. The amino acid compositions of the whole body of the prawn after 40 days of the feeding trial are
shown in Table 7. Some differences in the level of a few amino acids, such as arginine, histidine and proline were significant (P-0.05) among the dietary groups. The prawn fed the PJP and SNP diets had higher arginine levels than these fed the BFP diet, but no significant differences with those fed the PEP, PLP, SMP or the control diets. Higher histidine was found in prawn fed the PJP and SNP diets than in those fed the other test diets. The other whole body amino acid concentrations did not show any significant differences among the dietary treatments. The AyE ratio w(each EAA contentytotal EAA content including cystine and tyrosine)=1000x of the EAA composition of the whole body after the growth trial are shown in Table 8. The AyE ratios
Table 7 Amino acid composition (g per 100 g dry sample) of the whole body of the juvenile kuruma prawn fed diets with different amino acid profiles Amino acids
Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Tryptophan Valine Aspartic acid Glutamic acid Serine Proline Glycine Alanine Tyrosine Taurine
Diet PEP
PLP
PJP
SMP
SNP
BFP
Control
3.49ab 1.07a 1.23 2.38 2.70 0.76 2.22 1.38 0.50 1.49 3.33 6.40 1.32 2.50ab 3.97 2.24 2.18 1.08
3.56ab 1.18a 1.40 2.63 3.11 0.93 2.14 1.50 0.60 1.40 3.60 6.96 1.39 2.75b 4.71 2.56 2.01 1.01
3.69b 1.48b 1.24 2.33 2.77 0.73 2.03 1.35 0.63 1.31 3.36 6.25 1.22 2.26ab 3.57 2.21 2.25 0.95
3.21ab 1.14a 1.32 2.40 2.71 0.75 1.99 1.41 0.42 1.39 3.35 6.44 1.27 2.62ab 3.60 2.11 1.98 0.86
3.77b 1.45b 1.38 2.56 2.95 0.84 2.24 1.42 0.53 1.39 3.55 6.77 1.33 2.30ab 4.62 2.08 2.15 1.06
2.72a 1.00a 1.20 2.13 2.42 0.72 1.82 1.24 0.40 1.33 3.00 5.82 1.15 1.87a 3.77 1.81 2.01 0.76
3.41ab 1.31ab 1.21 2.30 2.83 0.69 1.90 1.31 0.34 1.32 3.37 6.50 1.31 2.16a 3.84 2.36 1.91 1.11
Values are means of triplicate groups.
M.S. Alam et al. / Comparative Biochemistry and Physiology Part B 133 (2002) 289–297
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Table 8 AyE ratiosa of the essential amino acid composition of whole body tissue of the kuruma prawn fed different reference amino acid profile diets and compare with P. monodon and M. rosenbergii
Arg His Ile Leu Lys Met Phee Thr Trp Val
Diet PEP
PLP
PJP
SMP
SNP
BFP
Control
P. monodonb
M. rosenbergiic
180 55 63 123 139 39 227 71 26 77
174 58 68 129 152 46 203 73 29 68
186 75 63 118 140 37 216 68 32 66
171 61 71 128 145 40 212 75 22 74
182 70 67 124 143 41 212 69 26 67
160 59 71 125 143 42 225 73 24 78
184 71 65 124 153 37 206 71 18 71
153 47 85 146 145 74d 155 76 16 100
145 68 73 147 164 70 172 88 ND 72
N.D.snot detected. a AyE ratios(each EAA contenty total EAA content including cystine and tyrosine)=1000. b Dy-Penaflorida (1989). c Reed and D’Abramo (1989). d Methionine and cystine. e Phenylalanine and tyrosine.
among the dietary groups did not show much variation except for arginine (ranging from 160 to 186), histidine (from 55 to 75) and tryptophan (from 18 to 32). The AyE ratios of the whole body were compared to the previously reported values for penaeid shrimp P. monodon (Dy-Penaflorida, 1989) and freshwater prawn M. rosenbergii (Reed and D’Abramo, 1989) (Table 8). 4. Discussion Earlier, attempts to investigate the utilization of CAA by replacing dietary protein on kuruma prawn (Deshimaru and Kuroki, 1974) and tiger prawn (Pascual, 1989) were unsuccessful due to leaching of CAA from the diets. CAA supplementation in the diet of P. vannamei yielded positive results, but it was still inferior to the control diet (Lim, 1993). Millamena et al. (1996) have succeeded in preparing water stable CAA based diet using CMC and k-carrageenan as binders to determine the amino acid requirements of tiger prawn, P. monodon. In the present study, the weight gain on the SMP and PJP diets containing a mixture of casein-gelatin and pre-coated CAA were not significantly different with that on the control diet containing intact protein. This result showed that kuruma prawn juveniles were capable of utilizing pre-coated CAA. It therefore appears that coating of CAA before mixing all ingredients in the diet is an applicable technique to improve the utiliza-
tion of CAA by prawn, as also observed in our previous study on flatfish Japanese flounder (Alam et al., 2000). In fish and crustacean, feeding of dietary CAA results in rapid increase in plasma amino acid concentrations compared with that of intact dietary protein (Deshimaru, 1976; Dabrowski, 1983). From the present study, we assume that pre-coated CAA not only reduces the leaching losses but also makes CAA absorption slowly in the digestive tract of the prawn after ingestion. Thus supplementation of CAA with coatings can be an efficient means for the estimation of EAA requirements of prawn as also reported for fish like rainbow trout (Cho et al., 1992). In the present study, the body weight gain of kuruma prawn fed the diet with amino acid profile of prawn juvenile whole body protein (PJP) was significantly higher than those fed the PEP, PLP, SNP and BFP diets. This result supported the suggestion of Reed and D’Abramo (1989) that the whole body or tail muscle amino acid profile could be used as reference dietary profiles for freshwater prawn M. rosenbergii. In the case of fish, the EAA pattern of the whole body of a given species has been considered to be representative of the EAA requirement profile of that species (Wilson and Cowey, 1985; Mambrini and Kaushik, 1995). In contrast, the amino acid profiles of whole hen egg (Halver et al., 1959) and fish eggs (Ketola, 1982) have been suggested to reflect the EAA requirements of fish. Deshimaru and Shigueno (1972)
M.S. Alam et al. / Comparative Biochemistry and Physiology Part B 133 (2002) 289–297
also reported the best growth for kuruma prawn fed a squid meal-based diet. Deshimaru (1982) proposed that the proportional composition of amino acids found in the whole body of short-necked clam could be ideal for kuruma prawn. In the present study, however, the diets with the amino acid profiles of the prawn egg (PEP) and shortnecked clam (SNP) gave significantly lower weight gain than those with amino acid profiles of squid meal (SMP) and prawn juveniles proteins (PJP). There is much information to show that well-balanced amino acid profiles in the diet are needed for good growth of the prawn (Millamena et al., 1997) and carp (Murai et al., 1989). We deduce that the amino acid profiles of squid meal protein and prawn juvenile whole body protein might reflect the requirement pattern of EAA for the prawn. In the present study, the amino acid profiles of the juvenile prawn protein and squid meal protein are thought to be ideal amino acid patterns for good growth of M. japonicus juveniles not only on the basis of weight gain data but also considering on the values of PER and APR. The values of these parameters are similar to those of the high quality diet (Giri et al., 1997) and higher than those of the other diets with the amino acid profiles of PEP and SNP diet (Table 5). The differences in protein retention among the groups could be due to bioavailability of dietary amino acids by prawn. Therefore, the amino acid profile of the juvenile prawn protein (PJP) or the squid meal protein (SMP) appeared to better reflect reference dietary amino acid patterns for juvenile kuruma prawn. The concentration of amino acids in a certain protein in animal bodies is commonly regarded as fixed by the messenger RNA sequence. In fact, Kaushik (1998) did not find any significant difference in the total whole body amino acids of two different sizes of European sea bass, gilthead sea bream and turbot. In the present study, the whole body total amino acid composition (% dry sample) of the juvenile prawn, was not altered by dietary treatments, except for some amino acids as also observed in fish such as rainbow trout (Mohanty and Kaushik, 1991) and Japanese flounder (Alam et al., 2002). The small differences of certain amino acid levels in the whole body among the dietary treatments found in the present study may be due to the differences in the tissue levels of free amino acids as also observed in rainbow
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trout (Kaushik and Luquet, 1980). Dall and Smith (1987) also showed that concentration of whole muscle total amino acids in tiger prawn P. esculentus changed only slightly when starved, but concentrations of various free amino acids changed significantly. Several studies have assessed the requirements of EAA using the concept of AyE ratio (Moon and Gatlin, 1991). The concept of AyE ratio was first introduced by Arai (1981) to formulate test diets for coho salmon Oncorhynchus kisutch. In the present research, the calculated AyE ratios of the whole body of kuruma prawn for arginine and phenylalanine were a little higher as compared with the reported value for tiger shrimp P. monodon (Dy-Penaflorida, 1989). However, the AyE ratio of leucine for the kuruma prawn was a little lower than those values reported for P. monodon and M. rosenbergii (Reed and D’Abramo, 1989). The other AyE ratios in the whole body did not show a big difference as compared with other tiger shrimp except methionine (as cystine content was not determined). This suggests that the differences in the requirement values for EAA between M. japonicus and P. monodon could be minor, as pointed out by D’Abramo (1998) from a comparison of AyE ratios between M. rosenbergii and penaeid species. In conclusion, juvenile prawn whole body protein as well as squid meal protein appears to provide the most appropriate dietary amino acid profiles for the maximum growth of juvenile kuruma prawn. These data will provide information to prepare balanced amino acid based diets for kuruma prawn until the requirements of all EAA are established. Acknowledgments The scholarship received by Md. Shah Alam from the Ministry of Education, Culture, Sports, Science and Technology (Monbukagakusho) of Japan and the scholarship for D. Yaniharto from Science and Technology for Industrial Development Project, Indonesia are gratefully acknowledged. The authors wish to acknowledge Ajinomoto Co., Inc., Japan for supplying crystalline amino acids. References Alam, M.S., Teshima, S., Ishikawa, M., Koshio, S., 2000. Methionine requirement of juvenile Japanese flounder Paralichthys olivaceus. J. World Aquacult. Soc. 31, 618–626.
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Alam, M.S., Teshima, S., Yaniharto, D., Ishikawa, M., Koshio, S., 2002. Influence of different dietary amino acid pattern on growth and body composition of juvenile Japanese flounder Paralichthys olivaceus. Aquaculture 210, 359–369. AOAC, 1990. In: Helric, K. (Ed.), Official Methods of Analysis of AOAC. 15th ed. Association of Official Analytical Chemists Inc, Arlington, VA,. Arai, S., 1981. A purified test diet for coho salmon, Oncorhynchus kisutch, fry. Nippon Suisan Gakkaishi 47, 547–550. Boghen, A.D., Castell, J.D., Conklin, D.E., 1982. In search of a reference protein to replace ‘vitamin free casein’ in lobster nutrition studies. Can. J. Zool. 60, 2033–2038. Bligh, E.G., Dyer, W.J., 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917. Castell, J.D., 1990. Reference diet for crustacean principles of experimentation.Advances in Tropical Aquaculture. Actes des Colloques 9, IFREMER, Plouzane, France. pp. 339–354. Chen, H.Y., Len, Y.T., Roelants, I., 1992. Quantification of arginine requirements of juvenile marine shrimp Penaeus monodon using microencapsulated arginine. Mar. Biol. 114, 229–233. Cheng, S.Y., Chen, J.C., 1998. Effects of nitrite exposure on the hemolymph electrolyte, respiratory protein and free amino acid levels and water content of P. japonicus. Aquatic Toxicol. 44, 129–139. Cho, C.Y., Kaushik, S.J., Woodward, B., 1992. Dietary arginine requirement of young rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 102A, 211–216. Cowey, C.B., Forster, J.R.M., 1971. The essential amino acid requirements of the prawn, Palaemon serratus. The growth of prawns on diets containing proteins of different amino acid composition. Mar. Biol. 10, 77–81. D’Abramo, L.R., 1998. Nutritional requirements of the freshwater prawn Macrobrachium rosenbergii: comparisons with species of penaeid shrimp. Rev. Fish. Sci. 6, 153–163. Dabrowski, K., 1983. Comparative aspects of protein digestion and amino acid absorption in fish and other animals. Comp. Biochem. Physiol. A 74, 417–425. Dall, W., Smith, D.M., 1987. Changes in protein-bound and free amino acids in the muscle of the tiger prawn Penaeus esculentus during starvation. Mar. Biol. 95, 509–520. Deshimaru, O., 1976. Studies on a purified diet for prawn. 6. Absorption rate of amino acids in amino acid test diet. Bull. Jpn. Soc. Sci. Fish. 42, 331–335. Deshimaru, O., 1982. Protein and amino acid nutrition of the prawn Penaeus japonicus. In: Proceedings of the 2nd International Conference on Aquaculture Nutrition. Pruder, G.D., Landgon, C., Conklin, D. (Eds.). Louisiana State University, Baton Rouge, LA, pp. 106–123. Deshimaru, O., Shigueno, K., 1972. Introduction to the artificial diet for prawn Penaeus japonicus. Aquaculture 1, 115–133. Deshimaru, O., Kuroki, K., 1974. Studies on a purified diet for prawn. III. A feeding experiment with amino acid test diets. Bull. Jpn. Soc. Sci. Fish. 41, 101–103. Dy-Penaflorida, V., 1989. An evaluation of indigenous protein sources as potential component in the diet formulation for tiger prawn, Penaeus monodon, using essential amino acid index (EAAI). Aquaculture 83, 319–330.
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M.S. Alam et al. / Comparative Biochemistry and Physiology Part B 133 (2002) 289–297 Reed, L., D’Abramo, L.R., 1989. A standard reference diet for crustacean nutrition research. 3. Effects on weight gain and amino acid composition of whole body and tail muscle of juvenile prawns Macrobrachium rosenbergii. J. World Aquacult. Soc. 20, 107–113. Shewbart, K.L., Meis, W.L., Ludwig, P.D., 1972. Identification and quantitative analysis of the amino acids present in protein of the brown shrimp, Penaeus aztecus. Mar. Biol. 16, 64–67. Shigueno, K., 1975. Shrimp Culture in Japan. Association for International Technical Promotion, Tokyo p. 153. Shiau, S.Y., 1998. Nutrient requirements of penaeid shrimp. Aquaculture 164, 77–93. Smith, D.M., Dall, W., 1991. Metabolism of proline by the tiger prawn Penaeus esculentus. Mar. Biol. 110, 85–91. Teshima, S., Kanazawa, A., 1971. Biosynthesis of sterols in the lobster Panulirus japonicus, the prawn Penaeus japonicus, and the crab Portunus trituberculatus. Comp. Biochem. Physiol. B 38, 597–602. Teshima, S., Kanazawa, A., Yamashita, M., 1986. Dietary value of several proteins and supplemental amino acids for
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Dietary amino acid profiles and growth performance in juvenile kuruma prawn Marsupenaeus japonicus Md. Shah Alam, Shin-ichi Teshima*, Dedy Yaniharto1, Manabu Ishikawa, Shunsuke Koshio Laboratory of Aquatic Animal Nutrition, Faculty of Fisheries, Kagoshima University, Shimoarata 4-50-20, Kagoshima 890-0056, Japan Received 19 March 2002; received in revised form 16 June 2002; accepted 25 June 2002
Abstract To assess the reference dietary amino acid profiles for juvenile kuruma prawn Marsupenaeus japonicus a feeding trial was conducted using six semi-purified diets containing casein-gelatin and pre-coated supplemental crystalline amino acids (CAA) and a control diet containing intact protein (casein-gelatin). Pre-coated CAA were supplemented to the diets to simulate dietary amino acid profiles to those of the prawn egg protein (PEP), prawn larvae whole body protein (PLP), prawn juvenile whole body protein (PJP), squid meal protein (SMP), short-necked clam protein (SNP) and brown fish meal protein (BFP). The result showed that kuruma prawn juveniles are capable of utilizing the pre-coated CAA and higher growth performances were observed in the groups fed the PJP, SMP and the control diets than those fed the PLP, SNP, BFP and PEP diets. The essential amino acid proportions (AyE ratios) of the whole body of kuruma prawn differ slightly when compared with the other penaeids or freshwater prawn. The results suggest that PJP and SMP would be suitable as a reference dietary amino acid profile for juvenile prawn. 䊚 2002 Elsevier Science Inc. All rights reserved. Keywords: Kuruma prawn; Marsupenaeus japonicus; Reference protein; Amino acid profile; Pre-coating; Crystalline amino acid; Utilization; AyE ratio
1. Introduction Since high protein diets are needed for good growth of most aquatic animals (NRC, 1993), estimation of minimum requirements of essential amino acids (EAA) is indispensable to formulate cost-effective diets. The quantitative EAA requi-
*Corresponding author. Tel.: q81-99-286-4181; fax: q8199-286-4184. E-mail address: [email protected] (S.-i. Teshima). 1 Present address: Agency for the Assessment and Application of Technology (BPPT), Jaluan, M. Husni, Thamrin No. 8; Jakarta Pusat 10340 – Indonesia.
rements of fish and crustaceans are often determined by feeding experiments with diets containing graded levels of the particular amino acid to be examined (Wilson, 1989). However, such a method requires much labor, expense and time. In addition, adaptation of the method to slow-eating aquatic animals such as prawns faces the obstacle that supplemental EAA leaches into the water before being consumed. Accordingly, several attempts have been made to assess the EAA requirements based on methods using ideal protein and reference amino acid patterns (Boghen et al., 1982; Wilson and Poe, 1985; Castell, 1990; Moon and Gatlin, 1991; Mambrini and Kaushik, 1995).
1096-4959/02/$ - see front matter 䊚 2002 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 6 - 4 9 5 9 Ž 0 2 . 0 0 1 6 5 - 3
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Table 1 Composition of the diets (g per 100 g dry diet) used for juvenile kuruma prawn Ingredient
CAA-dieta
Control
Casein Gelatin Amino acid mixb Cholesterol Squid liver oilc Soybean lecithind Vitamin mixe Mineral mixf a-Starch Sucrose Glucose Carboxymethyl cellulose k-Carrageenan a-Cellulose Attractantsg
17.0 8.0 20.0 1.0 4.0 4.0 7.0 4.0 8.0 7.0 5.0 4.0 2.5 7.1 1.4
30.0 15.0 0 1.0 4.0 4.0 7.0 4.0 8.0 7.0 5.0 4.0 2.5 7.1 1.4
a
Amino acid patterns of the diets were simulated to those of prawn egg protein (PEP), prawn larvae protein (PLP), prawn juvenile protein (PJP), squid meal protein (SMP) shortnecked clam protein (SNP) and brown fish meal protein (BFP). b See Table 4. c Feed oil squid (Riken Vitamin, Tokyo, Japan). d Kanto Chemical Co., Inc., Tokyo, Japan. e (mgy100 g) r-Amino benzoic acid, 47.24; biotin, 1.89; inositol, 1889.41; nicotinic acid, 188.94; ca-pantothenate, 283.41; pyridoxine–HCl, 56.70; riboflavin, 37.77; thiamin– HCl, 18.88; menadione, 18.93; vitamin A-palmitate, 47.53; atocopherol, 94.47; cyanocobalamin, 0.40; calciferol, 5.63; ascorbyl-2-phosphate-Mg, 1474.86; folic acid, 3.79 and choline chloride, 2830.13. f (mgy100 g dry diet): MgSO4Ø7H2O, 1422; NaH2PO4Ø2H2O, 370; KH2PO4, 935; Ca(H2PO4)2Ø2H2O, 1273. g (gy100 g): Glucosamine–HCl, 0.8; sodium citrate 0.3; sodium succinate, 0.3.
The EAA requirements of fish have been considered not to vary markedly among species (Kaushik, 1998). However, crustaceans such as prawns are different to fish in that they have an openvessel system and contain higher levels of nonprotein nitrogen compounds such as free amino acids in the body (Dall and Smith, 1987). Amino acids also play a role in osmotic regulation in crustaceans (Cheng and Chen, 1998). Considering these facts together, we assume that the EAA requirements of crustaceans possibly differ from those of fish. Although there are reports on the EAA requirements of prawn (Cowey and Forster, 1971; Shewbart et al., 1972; Kanazawa and Teshima, 1981; Smith and Dall, 1991; Chen et al., 1992; Fox et al., 1995; Millamena et al., 1996)
which were determined by dose-response or radioisotope methods, the knowledge of EAA requirements of crustaceans are only little and fragmentary. In a previous study, we have successfully evaluated the EAA requirements of the Japanese flounder, Paralichthys olivaceus, by using pre-coated crystalline amino acids (CAA) which enable retardation of the leaching of CAA into water (Alam et al., 2002). The kuruma prawn, Marsupenaeus japonicus, is the most popular penaeid with a high market value in Japan and many nutritional studies on this prawn have been conducted (Teshima and Kanazawa, 1971; Teshima et al., 1986, 1989, 2001; Shiau, 1998; Ishikawa et al., 2002). However, the quantitative EAA requirements of this species have not been established. Hence, we intended to evaluate the EAA requirements of the prawn by using the same method as used in the Japanese flounder in the viewpoint of comparative nutrition, with special interest in the difference in EAA requirements between fish and prawn. This paper deals with the relationship between the growth performance of the prawn, M. japonicus, and dietary amino acid profiles by feeding test diets containing provisional reference amino acid profiles. 2. Materials and methods 2.1. Experimental diets The basal and proximate compositions of the CAA-based diets and the control diets are shown in Tables 1 and 2, respectively. The amino acid profiles of prawn M. japonicus egg protein (PEP), prawn larvae (mysis) whole body protein (PLP), prawn (50 days after hatching) whole body juvenile protein (PJP), squid meal protein (Nippon Suisan Co., Ltd., Japan) (SMP), short-necked clam (locally purchased) protein (SNP) and brown fish meal (Nippon Suisan Co., Ltd., Japan) protein Table 2 The proximate composition of the test diets (% dry matter basis) fed to juvenile kuruma prawn Diet PEP PLP PJP
SMP SNP BFP Control
Crude protein 42.5 42.0 42.4 42.0 Total lipid 9.0 9.1 8.6 8.6 Ash 5.8 6.1 6.2 6.2 Moisture 16.1 16.4 15.6 15.4
42.6 42.0 43.4 9.1 8.6 8.9 6.2 6.1 6.1 15.4 15.6 14.8
M.S. Alam et al. / Comparative Biochemistry and Physiology Part B 133 (2002) 289–297 Table 3 Amino acid composition (g per 45 g protein) of different reference proteins Amino acid
PEP PLP PJP
SMP SNP BFP Control
Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Tryptophan Valine Aspartic acid Glutamic acid Serine Proline Glycine Alanine Tyrosine
3.14 1.56 2.66 3.41 3.66 1.07 2.08 2.46 0.28 3.06 3.42 7.63 1.85 2.05 1.75 2.42 1.91
3.72 1.11 1.99 3.30 3.48 2.14 1.91 1.85 0.80 1.86 4.54 6.35 1.55 2.78 2.06 2.16 1.92
3.71 1.01 1.85 2.87 3.17 1.27 1.93 1.79 0.65 2.17 4.12 6.45 2.00 4.56 2.56 2.16 1.78
4.59 0.90 1.88 3.19 3.40 1.30 1.66 1.51 1.00 1.88 4.14 6.76 1.10 3.42 3.38 2.23 1.58
3.44 0.96 1.68 2.67 3.59 0.63 1.46 1.61 0.38 1.85 4.51 6.29 1.85 2.16 2.97 2.55 1.18
2.85 1.61 1.86 3.40 4.34 1.12 2.05 1.98 1.21 2.21 4.25 5.44 1.43 2.34 2.40 2.59 1.79
2.49 0.71 1.76 3.02 3.48 0.91 2.17 1.37 0.75 2.21 2.86 7.85 1.37 5.24 3.62 2.11 2.02
(BFP) were considered as provisional references. Six semi-purified isocaloric diets were formulated to contain the amino acid patterns of PEP, PLP, PJP, SMP, SNP and BFP by supplementing casein– gelatin (approx. 2:1; 25 g) with pre-coated CAA (approx. 20 g). A control diet contained only intact protein sources (casein and gelatin, 2:1).
291
The other ingredients were according to the recent nutrient requirement information for juvenile kuruma prawn (Teshima et al., 2001). The amino acid compositions of the reference proteins, the dietary ingredients, and the supplementation of CAA are shown in Tables 3 and 4. The preparation of precoated CAA and diets were as per Alam et al. (2000). In brief, CAA mixes were pre-coated with carboxymethylcellulose (CMC) to prevent leaching losses. CMC-bound CAA mixture and the other dry ingredients were added to the casein– gelatin paste. To improve the water stability of the diets, gelatinized k-carrageenan was added to the mixture. The pH of the diets was adjusted to 7.0– 7.5 by adding 4 N sodium hydroxide. The pellets with 2.1 mm diameter were obtained using a pelletizer and dried at 40 8C for 2 h. The dried pellets of prawn were steamed at 100 8C for 1 min in a cylindrical steamer to improve water stability. Diets were stored in freezer at y30 8C until used. 2.2. Experimental prawn and feeding protocol The brood stock prawn, M. japonicus were obtained from Matsumoto Suisan, Miyazaki, Japan, transported to the Kagoshima University facility, and acclimatized to laboratory conditions. The eggs were hatched and larvae were reared by
Table 4 Amino acid composition (g per 100 g dry diet) of ingredients and supplementation of CAA in different diets to simulate amino acid pattern of references proteins (45% protein) Amino acid
Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Tryptophan Valine Aspartic acid Glutamic acid Serine Proline Glycine Alanine Tyrosine a
Supplementation of CAAa
Supplied by Casein 17%
Gelatin 8%
Diet PEP
PLP
PJP
SMP
SNP
BFP
0.59 0.38 0.82 1.40 1.53 0.45 1.01 0.61 0.42 1.01 1.06 3.42 0.56 1.63 0.22 0.41 1.06
0.78 0.02 0.17 0.29 0.41 0.06 0.21 0.16 0.01 0.23 0.53 0.97 0.20 1.26 1.73 0.74 0.09
1.77 1.16 1.67 1.72 1.72 0.56 0.86 1.69 0 1.82 1.83 3.24 1.09 0 0 1.27 0.76
2.34 0.61 0.86 1.18 1.23 0.76 0.71 1.02 0.22 0.93 2.53 2.06 1.24 1.67 0.61 1.01 0.63
3.22 0.50 0.89 1.50 1.46 0.79 0.44 0.74 0.57 0.64 2.55 2.37 0.34 0.53 1.43 1.08 0.43
2.35 0.71 1.00 1.61 1.54 1.63 0.69 1.08 0.37 0.62 2.95 1.96 0.79 0 0.11 1.01 0.77
2.07 0.56 0.69 0.98 1.65 0.12 0.24 0.84 0 0.61 2.92 1.90 1.09 0 1.02 1.40 0.03
1.48 1.21 0.87 1.71 2.40 0.61 0.83 1.21 0.78 0.97 2.66 1.05 0.67 0 0.45 1.44 0.64
Supplemented as L-form (Ajinomoto Co., Inc., Japan).
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Table 5 Growth performance of the juvenile kuruma prawn fed test diets for 40 days Diet
Weight gain (%)
FCEa
PERb
APRc
Survival (%)
PEP PLP PJP SMP SNP BFP Control
131.3"4.7a 168.0"4.6b 206.7"4.7c 210.0"3.5c 170.7"3.5b 184.0"4.6b 212.7"5.5c
0.26"0.02 0.34"0.06 0.35"0.02 0.33"0.03 0.26"0.02 0.30"0.03 0.34"0.04
0.62"0.02a 0.81"0.03bc 0.96"0.05d 0.97"0.02d 0.70"0.02ab 0.86"0.03cd 0.92"0.04cd
9.4"0.3a 10.9"0.2ab 12.6"0.9b 13.2"0.7b 8.5"0.4a 10.5"0.64ab 10.9"0.6ab
78"4 78"4 73"7 75"4 80"0 80"0 78"4
Values are means"S.E. of triplicate groups. Means with different letter in the same column differ significantly (P-0.05). a Feed conversion efficiency (FCE)sweight gain (g)ytotal feed intake in dry weight basis (g). b Protein efficiency ratio (PER)sweight gain (g)ytotal protein intake in dry weight basis (g). c Apparent protein retention (APR)sprotein gain=100yprotein intake.
feeding live food (Ceatocerus and Artemia) and commercial diets (Higashimaru Feed, Shrimp seed production number 0-1, Kagoshima, Japan) for 2.5 months. Before starting the feeding trial, the juveniles were sorted to obtain equal size prawns and transferred into other tanks. Seven triplicate groups of prawns, 0.50"0.01 g (mean"S.D.) in initial body weight, were fed the respective test diets in 21 rectangular tanks with a plastic cover (30 l capacity, filled with 28 l sea water) for 40 days. The tanks were individually equipped with a false bottom and sand substrate that acted to filter the water. Water was circulated at 0.8 lymin through the action of an air-lift device. Fifteen prawns were stocked randomly in each tank and diets were given daily by hand at 8–10% of body weight at 08:30 and 16:30 h. Known quantities of diets were given, and fecal matter and uneaten diets were collected by siphoning from the tank every morning. Lighting was provided using a 12 h light:12 h dark regime. Body weight was measured every 10 days of feeding periods when the tanks and sand were cleaned and filled with seawater again. Water temperature, salinity and pH were monitored daily. The mean values of water temperature, salinity and pH value during the experimental period were 23.5"1.5 8C, 33.5"0.71 ppt and 8.02"1.8, respectively. These values were thought to be suitable environmental conditions for the prawn M. japonicus (Shigueno, 1975). 2.3. Biochemical analysis The protein fraction of dietary protein sources was obtained by homogenizing wet ingredients with 10% trichloroacetic acid (TCA) and succes-
sively washed with 7% TCA, ethanol, chloroformy methanol (3:1), and diethyl ether followed by centrifugation to collect precipitates. Amino acid analyses of protein fractions, ingredients of the test diets and whole body of the juveniles were conducted according to Teshima et al. (1986) using high performance liquid chromatography (HPLC), (Shimadzu LC-6A, Japan). Ash and moisture contents were analyzed by standard methods (AOAC, 1990). Crude lipid was determined by the method of Bligh and Dyer (1959). Crude protein was determined by the Kjeldahl method (totalN=6.25) with a Tecator Kjeltec System (1007) Digestion system, 1002 Distilling unit, and Titration unit, Sweden) using boric acid to trap released ammonia. 2.4. Statistical analysis All data were subjected to statistical verification using one-way analysis of variance (package super-ANOVA, ver. 1.11, Abacus Concepts, Berkeley, California, USA). Significant differences between means were evaluated by the Tukey– Kramer test (Kramer, 1956). Probabilities of P0.05 were considered significant. 3. Results Table 5 presents the mean weight gain, percent survival, feed conversion efficiency (FCE), protein efficiency ratio (PER) and apparent protein retention (APR) of the juveniles fed test diets. Percent survivals were not significantly affected among the dietary treatments. The highest weight gain was obtained for prawn fed the control, PJP and SMP diets, whereas the lowest weight gain was
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Table 6 Body composition (% dry matter basis) (means"S.E.) of kuruma prawn fed test diets. Means with different letters in the same column differ significantly (P-0.05) Diet
Dry matter
Crude protein
Total lipid
Ash
PEP PLP PJP SMP SNP BFP Control
23.2"0.5c 21.8"0.2abc 22.2"0.6abc 22.6"0.5bc 20.7"0.2ab 21.0"0.5ab 20.2"0.4a
58.1"0.2a 59.5"0.1b 59.1"0.1b 58.5"0.1ab 58.1"0.2a 58.1"0.2a 59.4"0.3b
9.8"0.2b 9.4"0.1ab 9.3"0.1ab 9.8" 0.1b 9.3"0.2ab 9.4"0.1ab 8.8"0.1a
23.2"0.2c 21.9"0.4ab 22.4"0.4bc 21.0"0.3a 22.4"0.1bc 22.4"0.1bc 21.8"0.1ab
found in prawn fed the PEP diet. Thus the weight gains for the prawn fed the PEP, PLP, SNP and BFP diets were significantly lower than those of the PJP, SMP and control diets. There was no significant difference in FCE between the different groups. The SMP, PJP, BFP and control diets gave statistically higher PER than the PEP and SNP diets. Protein, lipid and ash contents (% dry matter basis) of the whole body after growth trial were influenced by the different patterns of the dietary amino acid in the diets (Table 6). Significantly higher protein contents were observed from the prawn fed the PLP, PJP and control diets than the other diets. The amino acid compositions of the whole body of the prawn after 40 days of the feeding trial are
shown in Table 7. Some differences in the level of a few amino acids, such as arginine, histidine and proline were significant (P-0.05) among the dietary groups. The prawn fed the PJP and SNP diets had higher arginine levels than these fed the BFP diet, but no significant differences with those fed the PEP, PLP, SMP or the control diets. Higher histidine was found in prawn fed the PJP and SNP diets than in those fed the other test diets. The other whole body amino acid concentrations did not show any significant differences among the dietary treatments. The AyE ratio w(each EAA contentytotal EAA content including cystine and tyrosine)=1000x of the EAA composition of the whole body after the growth trial are shown in Table 8. The AyE ratios
Table 7 Amino acid composition (g per 100 g dry sample) of the whole body of the juvenile kuruma prawn fed diets with different amino acid profiles Amino acids
Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Tryptophan Valine Aspartic acid Glutamic acid Serine Proline Glycine Alanine Tyrosine Taurine
Diet PEP
PLP
PJP
SMP
SNP
BFP
Control
3.49ab 1.07a 1.23 2.38 2.70 0.76 2.22 1.38 0.50 1.49 3.33 6.40 1.32 2.50ab 3.97 2.24 2.18 1.08
3.56ab 1.18a 1.40 2.63 3.11 0.93 2.14 1.50 0.60 1.40 3.60 6.96 1.39 2.75b 4.71 2.56 2.01 1.01
3.69b 1.48b 1.24 2.33 2.77 0.73 2.03 1.35 0.63 1.31 3.36 6.25 1.22 2.26ab 3.57 2.21 2.25 0.95
3.21ab 1.14a 1.32 2.40 2.71 0.75 1.99 1.41 0.42 1.39 3.35 6.44 1.27 2.62ab 3.60 2.11 1.98 0.86
3.77b 1.45b 1.38 2.56 2.95 0.84 2.24 1.42 0.53 1.39 3.55 6.77 1.33 2.30ab 4.62 2.08 2.15 1.06
2.72a 1.00a 1.20 2.13 2.42 0.72 1.82 1.24 0.40 1.33 3.00 5.82 1.15 1.87a 3.77 1.81 2.01 0.76
3.41ab 1.31ab 1.21 2.30 2.83 0.69 1.90 1.31 0.34 1.32 3.37 6.50 1.31 2.16a 3.84 2.36 1.91 1.11
Values are means of triplicate groups.
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Table 8 AyE ratiosa of the essential amino acid composition of whole body tissue of the kuruma prawn fed different reference amino acid profile diets and compare with P. monodon and M. rosenbergii
Arg His Ile Leu Lys Met Phee Thr Trp Val
Diet PEP
PLP
PJP
SMP
SNP
BFP
Control
P. monodonb
M. rosenbergiic
180 55 63 123 139 39 227 71 26 77
174 58 68 129 152 46 203 73 29 68
186 75 63 118 140 37 216 68 32 66
171 61 71 128 145 40 212 75 22 74
182 70 67 124 143 41 212 69 26 67
160 59 71 125 143 42 225 73 24 78
184 71 65 124 153 37 206 71 18 71
153 47 85 146 145 74d 155 76 16 100
145 68 73 147 164 70 172 88 ND 72
N.D.snot detected. a AyE ratios(each EAA contenty total EAA content including cystine and tyrosine)=1000. b Dy-Penaflorida (1989). c Reed and D’Abramo (1989). d Methionine and cystine. e Phenylalanine and tyrosine.
among the dietary groups did not show much variation except for arginine (ranging from 160 to 186), histidine (from 55 to 75) and tryptophan (from 18 to 32). The AyE ratios of the whole body were compared to the previously reported values for penaeid shrimp P. monodon (Dy-Penaflorida, 1989) and freshwater prawn M. rosenbergii (Reed and D’Abramo, 1989) (Table 8). 4. Discussion Earlier, attempts to investigate the utilization of CAA by replacing dietary protein on kuruma prawn (Deshimaru and Kuroki, 1974) and tiger prawn (Pascual, 1989) were unsuccessful due to leaching of CAA from the diets. CAA supplementation in the diet of P. vannamei yielded positive results, but it was still inferior to the control diet (Lim, 1993). Millamena et al. (1996) have succeeded in preparing water stable CAA based diet using CMC and k-carrageenan as binders to determine the amino acid requirements of tiger prawn, P. monodon. In the present study, the weight gain on the SMP and PJP diets containing a mixture of casein-gelatin and pre-coated CAA were not significantly different with that on the control diet containing intact protein. This result showed that kuruma prawn juveniles were capable of utilizing pre-coated CAA. It therefore appears that coating of CAA before mixing all ingredients in the diet is an applicable technique to improve the utiliza-
tion of CAA by prawn, as also observed in our previous study on flatfish Japanese flounder (Alam et al., 2000). In fish and crustacean, feeding of dietary CAA results in rapid increase in plasma amino acid concentrations compared with that of intact dietary protein (Deshimaru, 1976; Dabrowski, 1983). From the present study, we assume that pre-coated CAA not only reduces the leaching losses but also makes CAA absorption slowly in the digestive tract of the prawn after ingestion. Thus supplementation of CAA with coatings can be an efficient means for the estimation of EAA requirements of prawn as also reported for fish like rainbow trout (Cho et al., 1992). In the present study, the body weight gain of kuruma prawn fed the diet with amino acid profile of prawn juvenile whole body protein (PJP) was significantly higher than those fed the PEP, PLP, SNP and BFP diets. This result supported the suggestion of Reed and D’Abramo (1989) that the whole body or tail muscle amino acid profile could be used as reference dietary profiles for freshwater prawn M. rosenbergii. In the case of fish, the EAA pattern of the whole body of a given species has been considered to be representative of the EAA requirement profile of that species (Wilson and Cowey, 1985; Mambrini and Kaushik, 1995). In contrast, the amino acid profiles of whole hen egg (Halver et al., 1959) and fish eggs (Ketola, 1982) have been suggested to reflect the EAA requirements of fish. Deshimaru and Shigueno (1972)
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also reported the best growth for kuruma prawn fed a squid meal-based diet. Deshimaru (1982) proposed that the proportional composition of amino acids found in the whole body of short-necked clam could be ideal for kuruma prawn. In the present study, however, the diets with the amino acid profiles of the prawn egg (PEP) and shortnecked clam (SNP) gave significantly lower weight gain than those with amino acid profiles of squid meal (SMP) and prawn juveniles proteins (PJP). There is much information to show that well-balanced amino acid profiles in the diet are needed for good growth of the prawn (Millamena et al., 1997) and carp (Murai et al., 1989). We deduce that the amino acid profiles of squid meal protein and prawn juvenile whole body protein might reflect the requirement pattern of EAA for the prawn. In the present study, the amino acid profiles of the juvenile prawn protein and squid meal protein are thought to be ideal amino acid patterns for good growth of M. japonicus juveniles not only on the basis of weight gain data but also considering on the values of PER and APR. The values of these parameters are similar to those of the high quality diet (Giri et al., 1997) and higher than those of the other diets with the amino acid profiles of PEP and SNP diet (Table 5). The differences in protein retention among the groups could be due to bioavailability of dietary amino acids by prawn. Therefore, the amino acid profile of the juvenile prawn protein (PJP) or the squid meal protein (SMP) appeared to better reflect reference dietary amino acid patterns for juvenile kuruma prawn. The concentration of amino acids in a certain protein in animal bodies is commonly regarded as fixed by the messenger RNA sequence. In fact, Kaushik (1998) did not find any significant difference in the total whole body amino acids of two different sizes of European sea bass, gilthead sea bream and turbot. In the present study, the whole body total amino acid composition (% dry sample) of the juvenile prawn, was not altered by dietary treatments, except for some amino acids as also observed in fish such as rainbow trout (Mohanty and Kaushik, 1991) and Japanese flounder (Alam et al., 2002). The small differences of certain amino acid levels in the whole body among the dietary treatments found in the present study may be due to the differences in the tissue levels of free amino acids as also observed in rainbow
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trout (Kaushik and Luquet, 1980). Dall and Smith (1987) also showed that concentration of whole muscle total amino acids in tiger prawn P. esculentus changed only slightly when starved, but concentrations of various free amino acids changed significantly. Several studies have assessed the requirements of EAA using the concept of AyE ratio (Moon and Gatlin, 1991). The concept of AyE ratio was first introduced by Arai (1981) to formulate test diets for coho salmon Oncorhynchus kisutch. In the present research, the calculated AyE ratios of the whole body of kuruma prawn for arginine and phenylalanine were a little higher as compared with the reported value for tiger shrimp P. monodon (Dy-Penaflorida, 1989). However, the AyE ratio of leucine for the kuruma prawn was a little lower than those values reported for P. monodon and M. rosenbergii (Reed and D’Abramo, 1989). The other AyE ratios in the whole body did not show a big difference as compared with other tiger shrimp except methionine (as cystine content was not determined). This suggests that the differences in the requirement values for EAA between M. japonicus and P. monodon could be minor, as pointed out by D’Abramo (1998) from a comparison of AyE ratios between M. rosenbergii and penaeid species. In conclusion, juvenile prawn whole body protein as well as squid meal protein appears to provide the most appropriate dietary amino acid profiles for the maximum growth of juvenile kuruma prawn. These data will provide information to prepare balanced amino acid based diets for kuruma prawn until the requirements of all EAA are established. Acknowledgments The scholarship received by Md. Shah Alam from the Ministry of Education, Culture, Sports, Science and Technology (Monbukagakusho) of Japan and the scholarship for D. Yaniharto from Science and Technology for Industrial Development Project, Indonesia are gratefully acknowledged. The authors wish to acknowledge Ajinomoto Co., Inc., Japan for supplying crystalline amino acids. References Alam, M.S., Teshima, S., Ishikawa, M., Koshio, S., 2000. Methionine requirement of juvenile Japanese flounder Paralichthys olivaceus. J. World Aquacult. Soc. 31, 618–626.
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