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Dietary choline requirement for juvenile cobia, Rachycentron canadum
Aquaculture 289 (2009) 124–128
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Aquaculture j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e
Dietary choline requirement for juvenile cobia, Rachycentron canadum Kangsen Mai ⁎, Lindong Xiao, Qinghui Ai, Xiaojie Wang, Wei Xu, Wenbing Zhang, Zhiguo Liufu, Mingchun Ren The Key Laboratory of Mariculture (Ministry Education of China), Ocean University of China, Qingdao 266003, PR China
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Article history: Received 30 November 2008 Received in revised form 13 January 2009 Accepted 13 January 2009 Keywords: Cobia Rachycentron canadum Choline Requirement Feeding Nutrition
a b s t r a c t A 10-wk feeding trial was conducted to determine dietary choline requirement for juvenile cobia. The basal diet was formulated to contain 47.1 g crude protein 100 g− 1 dry weight from vitamin-free casein, gelatin and fish protein concentrate. This premix provided methionine at 1.05%, slightly less than the optimal requirement of cobia (1.19%), so endogenous synthesis of choline from methionine would be limited. Choline chloride was supplemented to the basal diet to formulate six purified diets containing 133 (control group), 350, 548, 940, 2017 and 3981 mg choline kg− 1 diet, respectively. Each diet was randomly fed to triplicate groups of juvenile cobia with initial average weight 4.2 ± 0.4 g in a flow-through system. Dietary choline level significantly influenced survival, feeding rate, weight gain, feed efficiency ratio, hepatosomatic index, as well as the choline concentrations in the liver and muscle of cobia. Broke-line regression of weight gain, liver and muscle choline concentration yield choline requirements of 696, 877 and 950 mg choline kg− 1 diet in the form of choline chloride, respectively. In addition, dietary choline supplementation significantly increased muscle lipid content of cobia. Potential manipulation of muscle lipid and associated flavor and texture by choline supplementation warrants further investigation. © 2009 Published by Elsevier B.V.
1. Introduction Cobia is a carnivorous species and widely distributed in tropical and subtropical waters (Ditty and Shaw, 1992). Excellent flesh quality, rapid growth, and adaptability to culture conditions, confer highly desirable characteristics for global commercial aquaculture on cobia (Holt et al., 2007). Following successful aquaculture development in Taiwan Province, China (Liao et al., 2004), cobia is extensively farmed in cages in China, Vietnam, and Philippines. Recently, its production has been initiated in EU, Brazil, and other Latin American and Caribbean countries (Holt et al., 2007). Among the technical limitations in global cobia farming, development of sustainable, highquality feeds for cobia is one of the major objectives identified by International Initiative of Sustainable and Biosecure Aquafarming, established in 2005 to accelerate commercial viability of cobia culture through international collaborations (Holt et al., 2007). The nutritional value of several plant protein sources have been evaluated for potential use in cobia formulated feeds (Chou et al., 2004; Lunger et al., 2006). Dietary requirements for macronutrients including crude
⁎ Corresponding author. Tel./fax: +86 532 82032038. E-mail address: [email protected] (K. Mai). 0044-8486/$ – see front matter © 2009 Published by Elsevier B.V. doi:10.1016/j.aquaculture.2009.01.016
protein (Chou et al., 2001; Craig et al., 2006), lipid (Wang et al., 2005), methionine (Zhou et al., 2006), and lysine (Zhou et al., 2007) have been reported. However, the dietary requirements for micronutrients, such as vitamins and minerals, have not been reported. Considered as a vitamin for young vertebrates (NRC, 1993), choline is the most abundant vitamin constituent in most fish feeds. Choline acts as an important methyl donor, a component of lecithin and acetylcholine in animals (NRC, 1993). Although de novo choline synthesis and the sparing effects of methyl-donating compounds on choline requirement have been reported, fish fed choline deficient diets usually demonstrate an aversion to feeding, growth retardation and poor survival (Wilson and Poe,1988; Hung,1989; Zhang and Wilson,1999). In addition, choline is a lipotropic and antihemorrhagic factor preventing excessive lipid accumulation and the development of fatty liver (Halver, 2002). Recent studies showed that dietary supplementation of soybean lecithin increased growth and feed utilization of juvenile cobia (Niu et al., 2008). However, the choline concentration in feed ingredients varies, as well as the relative bioavailability of choline for fishes (Zhang and Wilson, 1999). Establishment of the dietary requirement for choline is therefore important to refine feed formulations for juvenile cobia in terms of cost, optimal growth and feed utilization. Therefore, this study was designed to determine the requirement of dietary choline in the form of choline chloride for juvenile cobia, facilitate commercial feed development of this fish, and explore the influence of dietary choline on muscle lipid composition.
K. Mai et al. / Aquaculture 289 (2009) 124–128
2. Materials and methods
Table 2 Effect of different dietary choline on weight gain, feed efficiency ratio, feed intake and survival of cobia
2.1. Experimental diets The basal diet, which utilized casein, gelatin and fish protein concentrate as protein sources, was formulated to contain 47% crude protein and 14% crude lipid (Table 1), which satisfied the protein and lipid requirements for this fish (Chou et al., 2001; Craig et al., 2006). The experimental diets were formulated with a choline-free vitamin premix. Graded levels (0, 250, 500, 1000, 2000 and 4000 mg choline kg− 1 diet) of choline chloride (Sigma-Aldrich Corp., St. Louis, MO, USA) were supplemented to the basal diet. The choline concentration was analyzed by the method of Venugopal (1985). The actual levels of dietary choline were 133, 350, 548, 940, 2017 and 3981 mg kg− 1 diet, respectively (Table 1). Ingredients were ground to a fine powder and sieved through a 246 μm screen. All ingredients were thoroughly mixed with menhaden fish oil, and water was added to produce stiff dough. The dough was then pelleted with an experimental feed mill and dried for 24 h in a ventilated oven at 38 °C. The diets were then broken up and sieved into a proper pellet size (2.5 × 5.0 mm) and stored at −15 °C until used.
2.2. Experimental procedure The experimental fish were obtained from a commercial farm in Sanya, Hainan, China. Cobia were reared in 18, 1000-L, flow-through plastic tanks and fed the basal diet for one week to acclimate to the experimental diet and conditions. The water flow-rate was maintained at approximately 2 L min− 1 to maintain optimal water quality throughout the study. Before commencing the feeding trial, fish were fasted for 24 h, then weighed after being anesthetized with eugenol (1:10 000) (Shanghai Reagent Corp., China). Fish of similar size (4.2 ± 0.4 g) were randomly distributed into 18 tanks at a density of 25 fish per tank. Each diet was randomly assigned to triplicate tanks. Fish were hand-fed to apparent satiation twice (08:00 and 17:00 h) daily for 10 weeks. During the trial period, water temperature ranged from 28.5 to 32 °C, the salinity of seawater ranged from 24 to 26‰ and dissolved oxygen was approximately 7 mg L− 1. Fish were reared under natural light.
Table 1 Formulation and proximate composition of the experimental diets (% dry matter) Ingredients
Common ingredientsa Microcrystalline cellulose Choline chloride (mg kg− 1)
Diet no. (choline supplementation level, mg kg− 1 diet) Diet 1 (0.0)
Diet 2 (250.0)
Diet 3 (500.0)
Diet 4 (1000.0)
Diet 5 (2000.0)
Diet 6 (4000.0)
96.0
96.0
96.0
96.0
96.0
96.0
4 0.0
125
3.975 250.0
3.950 500.0
Proximate analysis (%, on a dry weight basis) Crude protein 46.9 47.0 47.1 Crude lipid 13.7 13.9 14.0 −1 Choline (mg kg ) 133.33 350.00 547.92
3.90 1000.0
46.8 14.0 939.58
3.80
3.60
2000.0
4000.0
47.2 14.1 2016.67
47.1 13.9 3981.25
a Common ingredients (%): casein, 36; gelatin, 9; fish protein concentrate, 5; dextrin, 25; fish oil, 14; taurine, 0.5; mineral premix, 4.5 {(mg 100 g− 1 mix): NaF, 20 mg; KI, 8 mg; CoCl2·6H2O (1%), 500 mg; CuSO4·5H2O, 100 mg; FeSO4·H2O, 800 mg; ZnSO4·H2O, 500 mg; MnSO4·H2O, 600 mg; MgSO4·7H2O, 12,000 mg; Ca (H2PO4)2·H2O, 80,000 mg; NaCl, 1,000 mg; Zoelite, 4,472 mg}; Vitamin premix, 2 {(mg kg− 1 diet): thiamin, 25 mg; riboflavin, 60 mg; pyridoxine–HCl, 20 mg; Vitamin B12, 0.1 mg; Vitamin K3, 10 mg; inositol, 800 mg; pantothenic acid, 60 mg; folic acid, 20 mg; niacin acid, 200 mg; biotin, 1.20 mg; retinol acetate, 32 mg; cholecalciferol, 5 mg; alpha- tocopherol, 120 mg; Lascorbly-2-polyphosphate, 2000 mg; ethoxyquin, 150 mg; dextrin, 12625 mg}.
Dietary choline (mg kg− 1)
Weight gain (%)
Feed efficiency ratio
Feeding rate (% day− 1)
Survival (%)
133.33 350.00 547.92 939.58 2016.67 3981.25
269.0 ± 14.7d 350.4 ± 16.6c 445.0 ± 14.9b 506.4 ± 8.3a 506.6 ± 16.0a 518.7 ± 19.3a
0.30 ± 0.03c 0.47 ± 0.03b 0.68 ± 0.03a 0.70 ± 0.01a 0.70 ± 0.01a 0.76 ± 0.03a
2.28 ± 0.02b 2.51 ± 0.04ab 2.46 ± 0.05ab 2.67 ± 0.04a 2.58 ± 0.06a 2.59 ± 0.09a
68.7 ± 3.5b 92.7 ± 2.7a 92.7 ± 3.5a 92.0 ± 2.3a 89.3 ± 3.5a 89.3 ± 1.3a
ANOVA F value P value
57.502 b 0.001
34.559 b 0.001
6.188 0.005
21.717 b 0.001
Values are means ± SEM of three replicate aquaria. Values in a column that do not have the same superscript are significantly different at P ≤ 0.05, based on Tukey's test. ANOVA: analysis of variances.
2.3. Analysis and measurements At the termination of the feeding trial, five fish were randomly sampled from each tank and pooled for individual proximate composition analysis. Fish body and diet composition were performed by standard methods (AOAC, 1990). Dry matter was determined by drying at 105 °C for 24 h, crude protein by the Kjeldahl method, crude fat after extraction with ether by the Soxhlet method and ash by combustion at 550 °C. Another ten fish from each tank were sampled for measuring hepatosomatic index (HSI) and visceral somatic index (VSI), and then an aliquot of the pooled samples of liver and muscle was used for lipid concentration analysis using the method of Folch et al. (1957), and the remaining samples of liver and muscle were used for choline analysis by the method of Venugopal (1985). 2.4. Calculations and statistical analysis The following variables were calculated: Survival (%) = 100 × final amount of fish / initial amount of fish Weight gain (%) = 100 × (final body weight − initial body weight) / initial body weight Feed efficiency ratio = wet weight gain in g/dry feed fed in g (Hardy and Barrows, 2002) Feeding rate (% day− 1) = 100 × total fed feeds × 2 / ((final body weight + initial body weight) × total days for trial) (Ai et al., 2006) HSI (%) = 100 × liver wet weight / body wet weight VSI (%) = 100 × viscera wet weight / body wet weight. All data from the feeding trial were subjected to Levene's test of equality of error variances and one-way ANOVA followed by Tukey's test using SPSS® (SPSS, Inc, Chicago, IL). All treatment effects were considered significant at a P value of 0.05 or less. Response indices that
Fig. 1. Relationship between dietary choline level and weight gain of cobia fed the six diets for 10 weeks.
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Table 3 Effect of different dietary choline on hepatosomatic index (HSI), visceral somatic index (VSI) and whole-body composition of cobia Dietary choline (mg kg− 1)
HSI
133.33 350.00 547.92 939.58 2016.67 3981.25
3.2 ± 0.15a 3.3 ± 0.17a 2.9 ± 0.14ab 2.5 ± 0.12b 2.3 ± 0.15b 2.4 ± 0.12b
ANOVA F value P value
8.643 0.001
VSI
Whole-body composition (% of fresh weight) Moisture
Crude protein
Crude lipid
Ash
15.9 ± 0.59 16.7 ± 1.44 15.1 ± 1.24 16.1 ± 0.19 14.8 ± 0.22 15.8 ± 0.35
70.0 ± 0.94 68.3 ± 0.62 69.2 ± 0.23 68.4 ± 0.41 67.2 ± 0.64 68.3 ± 0.75
17.8 ± 1.47 19.3 ± 1.02 18.7 ± 0.49 19.2 ± 0.64 20.3 ± 0.50 19.4 ± 0.59
9.3 ± 0.58 9.4 ± 0.92 9.2 ± 0.57 8.9 ± 0.38 9.3 ± 0.58 9.6 ± 0.68
3.0 ± 0.20 2.8 ± 0.23 3.0 ± 0.13 3.3±0.30 3.0 ± 0.28 2.8 ± 0.20
0.708 0.629
2.152 0.128
0.898 0.513
0.146 0.978
0.615 0.691
Values are means ± SEM of three replicate aquaria. Values in a column that do not have the same superscript are significantly different at P ≤ 0.05, based on Tukey's test. ANOVA: analysis of variances.
were significantly influenced by dietary choline level also were subjected to linear regression analysis against dietary choline. Brokeline regression analysis was performed on weight gain, choline concentrations in liver and muscle to establish the dietary requirement for choline (Robbins et al., 1979). The equation used in the model is Y = L + U ðR−XLR Þ where Y is the parameter (weight gain, liver or muscle choline) chosen to estimate the requirement, L is the ordinate and R is the abscissa of the breakpoint. R is taken as the estimated requirement. XLR means X less than R, and U is the slope of the line for XLR. By definition R − XLR = 0 when X N R. 3. Results 3.1. Growth performance Fish fed the basal diet had significantly lower feeding rate compared to those fed the other experimental diets. After the 10-week feeding trial, survival of cobia fed the basal diet averaged 68.7% which was significantly lower than those (89.3–92.7%) fed the cholinesupplemented diets. Similarly, weight gain and feed efficiency of cobia fed the basal diet were significantly lower than those fed diets containing added choline (Table 2). A significant positive correlation was observed between dietary choline level and either weight gain or feed efficiency ratio (Table 2). Broke-line regression analysis on weight gain estimated the minimum dietary requirement for choline in the
Table 4 Effect of dietary choline on liver lipid concentration and muscle lipid concentration of cobia Dietary choline (mg kg− 1)
Lipid (%) Liver
Muscle
133.33 350.00 547.92 939.58 2016.67 3981.25
45.0 ± 1.93b 56.1 ± 1.16a 46.7 ± 1.38b 35.4 ± 1.22c 34.7 ± 0.98c 35.7 ± 1.12c
9.7 ± 0.57b 11.1 ± 0.29ab 11.7 ± 0.64ab 12.2 ± 0.31ab 12.5 ± 0.81a 12.4 ± 0.53a
ANOVA F value P value
41.253 b 0.001
3.551 0.033
Values are means ± SEM of three composite samples of fish from replicate aquaria. Values in a column that do not have the same superscript are significantly different at P ≤ 0.05, based on Tukey's test (P b 0.05). ANOVA: analysis of variances.
Fig. 2. Relationship between dietary choline level and liver choline of cobia fed the six diets for 10 weeks.
form of choline chloride to be 696 mg kg− 1 diet for juvenile cobia under the experimental conditions used (Fig. 1). 3.2. VSI, HSI, and whole-body composition VSI of cobia ranged from 14.8–16.7% without significant dietary influences (Table 3). However, the HSI was significantly affected by dietary choline level (Table 3). HSI of fish in groups with dietary choline equal to or lower than 350 mg kg− 1 diet was significantly higher than the groups with dietary choline equal to or higher than 940 mg kg− 1 diet. The carcass crude protein, crude lipid and ash of cobia were 17.8–20.3, 8.9–9.6 and 2.8–3.3% of fresh weight, respectively (Table 3). There was no significant difference in the whole-body composition of cobia fed diets containing different levels of choline. 3.3. Lipid content in liver and muscle The lipid levels in both fish muscle (9.7–12.5%) and liver (34.7– 56.1%) were significantly influenced by dietary choline level. A general decrease trend of liver lipid was observed as dietary choline increased (Table 4). However, muscle lipid content, which was much lower than the liver lipid level, showed an increasing trend as dietary choline increased (Table 4). 3.4. Choline concentration in liver and muscle The choline concentration in cobia liver was progressively increased with increasing concentration of dietary choline within the range of 133 to 939 mg kg− 1 diet, and then leveled off. Based on linear regression of liver choline concentration (P b 0.01, R2 = 0.93), a minimum dietary requirement for choline in the form of choline chloride was estimated to be 877 mg kg− 1 diet (Fig. 2). Similarly, choline concentration in cobia muscle reached a plateau when dietary choline was higher than 950 mg kg− 1 diet (Fig. 3).
Fig. 3. Relationship between dietary choline level and muscle choline of cobia fed the six diets for 10 weeks.
K. Mai et al. / Aquaculture 289 (2009) 124–128
4. Discussion Juvenile cobia exhibited an obvious requirement for dietary choline for optimal growth and diet utilization in the present study. Weight gain, feed efficiency ratio, feeding rate and survival demonstrated rather consistent patterns. With reduced values for fish fed the basal diet, they gradually increased values with increasing dietary choline up to the requirement level. To minimize the possible cholinesparing effect of methionine, the estimated choline requirement was determined utilizing diets containing 1.05% methionine of dry diet, which marginally met the methionine requirement (1.19% of dry diet, Zhou et al., 2006). Based on weight gain, the optimal choline requirement for cobia was 696 mg kg− 1 diet, which was higher than blue tilapia (500 mg kg− 1 diet, Roem et al., 1990), hybrid striped bass (500 mg kg− 1 diet, Griffin et al., 1994), red drum (588 mg kg− 1 diet, Craig and Gatlin, 1996), channel catfish (400 mg kg− 1 diet, Zhang and Wilson, 1999) and yellow perch (598–634 mg kg− 1 diet, Twibell and Brown, 2000). However, other fishes, such as lake trout (1000 mg kg− 1 diet, Ketola, 1976), sturgeon (1700–3200 mg kg− 1 diet, Hung, 1989), rainbow trout (4000 mg kg− 1 diet, Poston, 1991) and hybrid tilapia (1000 mg kg− 1 diet, Shiau and Lo, 2000), may require more dietary choline. The variation in dietary requirement of various fish species for choline across studies can be attributable to fish species, age/size (Rumsey, 1991; Griffin et al., 1994) and nutritional factors such as abundance of methyl donors including methionine and betaine. Environmental influences of one-carbon metabolism and choline synthesis of aquatic animals are poorly studied at this time. It is generally recognized that excessive accumulation of lipid in liver choline-deficient animals is attributable to impaired hepatic lipoprotein secretion and subsequent accumulation of triacyglycerols (Chan, 1991). Liver lipid content has been used as an indicator of choline status in animals, including some fishes. As the case of the present study, a negative correlation between dietary choline and liver lipid has been demonstrated in lake trout (Ketola, 1976), channel catfish (Wilson and Poe, 1988) and hybrid striped bass (Griffin et al., 1994). However, rainbow trout (Rumsey, 1991) and yellow perch (Twibell and Brown, 2000) were not responsive to dietary choline level. Furthermore, Shiau and Lo (2000) found that liver lipid content of hybrid tilapia increased with dietary choline level. Similarly, Craig and Gatlin (1996) suggested that red drum could accumulate large lipid in liver and dietary choline deficiency may depress this effect. Hence, further investigations are needed to study lipid accumulation mechanism in fish liver and its influence factors. Muscle lipid content was also dependent upon dietary choline level. Muscle lipid content has been recognized as a determinant of flavor and texture for terrestrial animals as well as salmonids (Robb, 2002). Because cobia is extensively used for sashimi and sushi, highlipid in fillet may present desirable flavor and texture. Therefore, supplementation of dietary choline may prevent fatty liver, but also improve flesh quality of this fish species. Choline concentration in liver and muscle of cobia were consistently increased as dietary choline level increased, until reaching a plateau after the requirement was met. This is in agreement with most of the previous studies with channel catfish (e.g. Zhang and Wilson, 1999). However, Shiau and Lo (2000) reported that whole-body choline concentration and weight gain of hybrid tilapia was decreased when dietary choline level becomes excessive. Because liver choline was highly responsive to choline sufficiency in the diets of cobia, dietary requirement for choline was also estimated based on liver choline. The dietary choline requirement of cobia based on liver choline was 877 mg kg− 1 diet and was higher than the value based on weight gain. This indicates that cobia needs more choline to maintain some special physiological functions than to maintain normal growth. In conclusion, juvenile cobia requires exogenous choline for normal growth and physiological functions. Based on weight gain, liver and muscle choline concentration, the dietary choline requirement
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of cobia is estimated as 696, 877 or 950 mg kg− 1 diet, respectively. The influence mechanism of dietary choline on liver and muscle lipid accumulation, flesh texture and taste of cobia warrant further investigation. Acknowledgements This study was financially supported by National Key Technology R&D Program for the 11th Five-year Plan of China (Grant no.: 2006BAD03B03). The authors thank Kai Liu and Mingchao Yu for their help in feeding and sampling. Thanks are also due to Peng Li for revising this manuscript, and Lu Zhang, Chunxiao Zhang and Xingwang Liu for their assistances in the study. References Ai, Q.H., Mai, K.S., Tan, B.P., Xu, W., Duan, Q.Y., Ma, H.M., Zhang, L., 2006. Replacement of fish meal by meat and bone meal in diets for large yellow croaker, Pseudosciaena crocea. Aquaculture 260, 255–263. Association of Official Analytical Chemists (AOAC), 1990. Official Methods of Analysis of Official Analytical Chemists International, 16th edn. 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Dietary choline requirement for juvenile cobia, Rachycentron canadum Kangsen Mai ⁎, Lindong Xiao, Qinghui Ai, Xiaojie Wang, Wei Xu, Wenbing Zhang, Zhiguo Liufu, Mingchun Ren The Key Laboratory of Mariculture (Ministry Education of China), Ocean University of China, Qingdao 266003, PR China
a r t i c l e
i n f o
Article history: Received 30 November 2008 Received in revised form 13 January 2009 Accepted 13 January 2009 Keywords: Cobia Rachycentron canadum Choline Requirement Feeding Nutrition
a b s t r a c t A 10-wk feeding trial was conducted to determine dietary choline requirement for juvenile cobia. The basal diet was formulated to contain 47.1 g crude protein 100 g− 1 dry weight from vitamin-free casein, gelatin and fish protein concentrate. This premix provided methionine at 1.05%, slightly less than the optimal requirement of cobia (1.19%), so endogenous synthesis of choline from methionine would be limited. Choline chloride was supplemented to the basal diet to formulate six purified diets containing 133 (control group), 350, 548, 940, 2017 and 3981 mg choline kg− 1 diet, respectively. Each diet was randomly fed to triplicate groups of juvenile cobia with initial average weight 4.2 ± 0.4 g in a flow-through system. Dietary choline level significantly influenced survival, feeding rate, weight gain, feed efficiency ratio, hepatosomatic index, as well as the choline concentrations in the liver and muscle of cobia. Broke-line regression of weight gain, liver and muscle choline concentration yield choline requirements of 696, 877 and 950 mg choline kg− 1 diet in the form of choline chloride, respectively. In addition, dietary choline supplementation significantly increased muscle lipid content of cobia. Potential manipulation of muscle lipid and associated flavor and texture by choline supplementation warrants further investigation. © 2009 Published by Elsevier B.V.
1. Introduction Cobia is a carnivorous species and widely distributed in tropical and subtropical waters (Ditty and Shaw, 1992). Excellent flesh quality, rapid growth, and adaptability to culture conditions, confer highly desirable characteristics for global commercial aquaculture on cobia (Holt et al., 2007). Following successful aquaculture development in Taiwan Province, China (Liao et al., 2004), cobia is extensively farmed in cages in China, Vietnam, and Philippines. Recently, its production has been initiated in EU, Brazil, and other Latin American and Caribbean countries (Holt et al., 2007). Among the technical limitations in global cobia farming, development of sustainable, highquality feeds for cobia is one of the major objectives identified by International Initiative of Sustainable and Biosecure Aquafarming, established in 2005 to accelerate commercial viability of cobia culture through international collaborations (Holt et al., 2007). The nutritional value of several plant protein sources have been evaluated for potential use in cobia formulated feeds (Chou et al., 2004; Lunger et al., 2006). Dietary requirements for macronutrients including crude
⁎ Corresponding author. Tel./fax: +86 532 82032038. E-mail address: [email protected] (K. Mai). 0044-8486/$ – see front matter © 2009 Published by Elsevier B.V. doi:10.1016/j.aquaculture.2009.01.016
protein (Chou et al., 2001; Craig et al., 2006), lipid (Wang et al., 2005), methionine (Zhou et al., 2006), and lysine (Zhou et al., 2007) have been reported. However, the dietary requirements for micronutrients, such as vitamins and minerals, have not been reported. Considered as a vitamin for young vertebrates (NRC, 1993), choline is the most abundant vitamin constituent in most fish feeds. Choline acts as an important methyl donor, a component of lecithin and acetylcholine in animals (NRC, 1993). Although de novo choline synthesis and the sparing effects of methyl-donating compounds on choline requirement have been reported, fish fed choline deficient diets usually demonstrate an aversion to feeding, growth retardation and poor survival (Wilson and Poe,1988; Hung,1989; Zhang and Wilson,1999). In addition, choline is a lipotropic and antihemorrhagic factor preventing excessive lipid accumulation and the development of fatty liver (Halver, 2002). Recent studies showed that dietary supplementation of soybean lecithin increased growth and feed utilization of juvenile cobia (Niu et al., 2008). However, the choline concentration in feed ingredients varies, as well as the relative bioavailability of choline for fishes (Zhang and Wilson, 1999). Establishment of the dietary requirement for choline is therefore important to refine feed formulations for juvenile cobia in terms of cost, optimal growth and feed utilization. Therefore, this study was designed to determine the requirement of dietary choline in the form of choline chloride for juvenile cobia, facilitate commercial feed development of this fish, and explore the influence of dietary choline on muscle lipid composition.
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2. Materials and methods
Table 2 Effect of different dietary choline on weight gain, feed efficiency ratio, feed intake and survival of cobia
2.1. Experimental diets The basal diet, which utilized casein, gelatin and fish protein concentrate as protein sources, was formulated to contain 47% crude protein and 14% crude lipid (Table 1), which satisfied the protein and lipid requirements for this fish (Chou et al., 2001; Craig et al., 2006). The experimental diets were formulated with a choline-free vitamin premix. Graded levels (0, 250, 500, 1000, 2000 and 4000 mg choline kg− 1 diet) of choline chloride (Sigma-Aldrich Corp., St. Louis, MO, USA) were supplemented to the basal diet. The choline concentration was analyzed by the method of Venugopal (1985). The actual levels of dietary choline were 133, 350, 548, 940, 2017 and 3981 mg kg− 1 diet, respectively (Table 1). Ingredients were ground to a fine powder and sieved through a 246 μm screen. All ingredients were thoroughly mixed with menhaden fish oil, and water was added to produce stiff dough. The dough was then pelleted with an experimental feed mill and dried for 24 h in a ventilated oven at 38 °C. The diets were then broken up and sieved into a proper pellet size (2.5 × 5.0 mm) and stored at −15 °C until used.
2.2. Experimental procedure The experimental fish were obtained from a commercial farm in Sanya, Hainan, China. Cobia were reared in 18, 1000-L, flow-through plastic tanks and fed the basal diet for one week to acclimate to the experimental diet and conditions. The water flow-rate was maintained at approximately 2 L min− 1 to maintain optimal water quality throughout the study. Before commencing the feeding trial, fish were fasted for 24 h, then weighed after being anesthetized with eugenol (1:10 000) (Shanghai Reagent Corp., China). Fish of similar size (4.2 ± 0.4 g) were randomly distributed into 18 tanks at a density of 25 fish per tank. Each diet was randomly assigned to triplicate tanks. Fish were hand-fed to apparent satiation twice (08:00 and 17:00 h) daily for 10 weeks. During the trial period, water temperature ranged from 28.5 to 32 °C, the salinity of seawater ranged from 24 to 26‰ and dissolved oxygen was approximately 7 mg L− 1. Fish were reared under natural light.
Table 1 Formulation and proximate composition of the experimental diets (% dry matter) Ingredients
Common ingredientsa Microcrystalline cellulose Choline chloride (mg kg− 1)
Diet no. (choline supplementation level, mg kg− 1 diet) Diet 1 (0.0)
Diet 2 (250.0)
Diet 3 (500.0)
Diet 4 (1000.0)
Diet 5 (2000.0)
Diet 6 (4000.0)
96.0
96.0
96.0
96.0
96.0
96.0
4 0.0
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3.975 250.0
3.950 500.0
Proximate analysis (%, on a dry weight basis) Crude protein 46.9 47.0 47.1 Crude lipid 13.7 13.9 14.0 −1 Choline (mg kg ) 133.33 350.00 547.92
3.90 1000.0
46.8 14.0 939.58
3.80
3.60
2000.0
4000.0
47.2 14.1 2016.67
47.1 13.9 3981.25
a Common ingredients (%): casein, 36; gelatin, 9; fish protein concentrate, 5; dextrin, 25; fish oil, 14; taurine, 0.5; mineral premix, 4.5 {(mg 100 g− 1 mix): NaF, 20 mg; KI, 8 mg; CoCl2·6H2O (1%), 500 mg; CuSO4·5H2O, 100 mg; FeSO4·H2O, 800 mg; ZnSO4·H2O, 500 mg; MnSO4·H2O, 600 mg; MgSO4·7H2O, 12,000 mg; Ca (H2PO4)2·H2O, 80,000 mg; NaCl, 1,000 mg; Zoelite, 4,472 mg}; Vitamin premix, 2 {(mg kg− 1 diet): thiamin, 25 mg; riboflavin, 60 mg; pyridoxine–HCl, 20 mg; Vitamin B12, 0.1 mg; Vitamin K3, 10 mg; inositol, 800 mg; pantothenic acid, 60 mg; folic acid, 20 mg; niacin acid, 200 mg; biotin, 1.20 mg; retinol acetate, 32 mg; cholecalciferol, 5 mg; alpha- tocopherol, 120 mg; Lascorbly-2-polyphosphate, 2000 mg; ethoxyquin, 150 mg; dextrin, 12625 mg}.
Dietary choline (mg kg− 1)
Weight gain (%)
Feed efficiency ratio
Feeding rate (% day− 1)
Survival (%)
133.33 350.00 547.92 939.58 2016.67 3981.25
269.0 ± 14.7d 350.4 ± 16.6c 445.0 ± 14.9b 506.4 ± 8.3a 506.6 ± 16.0a 518.7 ± 19.3a
0.30 ± 0.03c 0.47 ± 0.03b 0.68 ± 0.03a 0.70 ± 0.01a 0.70 ± 0.01a 0.76 ± 0.03a
2.28 ± 0.02b 2.51 ± 0.04ab 2.46 ± 0.05ab 2.67 ± 0.04a 2.58 ± 0.06a 2.59 ± 0.09a
68.7 ± 3.5b 92.7 ± 2.7a 92.7 ± 3.5a 92.0 ± 2.3a 89.3 ± 3.5a 89.3 ± 1.3a
ANOVA F value P value
57.502 b 0.001
34.559 b 0.001
6.188 0.005
21.717 b 0.001
Values are means ± SEM of three replicate aquaria. Values in a column that do not have the same superscript are significantly different at P ≤ 0.05, based on Tukey's test. ANOVA: analysis of variances.
2.3. Analysis and measurements At the termination of the feeding trial, five fish were randomly sampled from each tank and pooled for individual proximate composition analysis. Fish body and diet composition were performed by standard methods (AOAC, 1990). Dry matter was determined by drying at 105 °C for 24 h, crude protein by the Kjeldahl method, crude fat after extraction with ether by the Soxhlet method and ash by combustion at 550 °C. Another ten fish from each tank were sampled for measuring hepatosomatic index (HSI) and visceral somatic index (VSI), and then an aliquot of the pooled samples of liver and muscle was used for lipid concentration analysis using the method of Folch et al. (1957), and the remaining samples of liver and muscle were used for choline analysis by the method of Venugopal (1985). 2.4. Calculations and statistical analysis The following variables were calculated: Survival (%) = 100 × final amount of fish / initial amount of fish Weight gain (%) = 100 × (final body weight − initial body weight) / initial body weight Feed efficiency ratio = wet weight gain in g/dry feed fed in g (Hardy and Barrows, 2002) Feeding rate (% day− 1) = 100 × total fed feeds × 2 / ((final body weight + initial body weight) × total days for trial) (Ai et al., 2006) HSI (%) = 100 × liver wet weight / body wet weight VSI (%) = 100 × viscera wet weight / body wet weight. All data from the feeding trial were subjected to Levene's test of equality of error variances and one-way ANOVA followed by Tukey's test using SPSS® (SPSS, Inc, Chicago, IL). All treatment effects were considered significant at a P value of 0.05 or less. Response indices that
Fig. 1. Relationship between dietary choline level and weight gain of cobia fed the six diets for 10 weeks.
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Table 3 Effect of different dietary choline on hepatosomatic index (HSI), visceral somatic index (VSI) and whole-body composition of cobia Dietary choline (mg kg− 1)
HSI
133.33 350.00 547.92 939.58 2016.67 3981.25
3.2 ± 0.15a 3.3 ± 0.17a 2.9 ± 0.14ab 2.5 ± 0.12b 2.3 ± 0.15b 2.4 ± 0.12b
ANOVA F value P value
8.643 0.001
VSI
Whole-body composition (% of fresh weight) Moisture
Crude protein
Crude lipid
Ash
15.9 ± 0.59 16.7 ± 1.44 15.1 ± 1.24 16.1 ± 0.19 14.8 ± 0.22 15.8 ± 0.35
70.0 ± 0.94 68.3 ± 0.62 69.2 ± 0.23 68.4 ± 0.41 67.2 ± 0.64 68.3 ± 0.75
17.8 ± 1.47 19.3 ± 1.02 18.7 ± 0.49 19.2 ± 0.64 20.3 ± 0.50 19.4 ± 0.59
9.3 ± 0.58 9.4 ± 0.92 9.2 ± 0.57 8.9 ± 0.38 9.3 ± 0.58 9.6 ± 0.68
3.0 ± 0.20 2.8 ± 0.23 3.0 ± 0.13 3.3±0.30 3.0 ± 0.28 2.8 ± 0.20
0.708 0.629
2.152 0.128
0.898 0.513
0.146 0.978
0.615 0.691
Values are means ± SEM of three replicate aquaria. Values in a column that do not have the same superscript are significantly different at P ≤ 0.05, based on Tukey's test. ANOVA: analysis of variances.
were significantly influenced by dietary choline level also were subjected to linear regression analysis against dietary choline. Brokeline regression analysis was performed on weight gain, choline concentrations in liver and muscle to establish the dietary requirement for choline (Robbins et al., 1979). The equation used in the model is Y = L + U ðR−XLR Þ where Y is the parameter (weight gain, liver or muscle choline) chosen to estimate the requirement, L is the ordinate and R is the abscissa of the breakpoint. R is taken as the estimated requirement. XLR means X less than R, and U is the slope of the line for XLR. By definition R − XLR = 0 when X N R. 3. Results 3.1. Growth performance Fish fed the basal diet had significantly lower feeding rate compared to those fed the other experimental diets. After the 10-week feeding trial, survival of cobia fed the basal diet averaged 68.7% which was significantly lower than those (89.3–92.7%) fed the cholinesupplemented diets. Similarly, weight gain and feed efficiency of cobia fed the basal diet were significantly lower than those fed diets containing added choline (Table 2). A significant positive correlation was observed between dietary choline level and either weight gain or feed efficiency ratio (Table 2). Broke-line regression analysis on weight gain estimated the minimum dietary requirement for choline in the
Table 4 Effect of dietary choline on liver lipid concentration and muscle lipid concentration of cobia Dietary choline (mg kg− 1)
Lipid (%) Liver
Muscle
133.33 350.00 547.92 939.58 2016.67 3981.25
45.0 ± 1.93b 56.1 ± 1.16a 46.7 ± 1.38b 35.4 ± 1.22c 34.7 ± 0.98c 35.7 ± 1.12c
9.7 ± 0.57b 11.1 ± 0.29ab 11.7 ± 0.64ab 12.2 ± 0.31ab 12.5 ± 0.81a 12.4 ± 0.53a
ANOVA F value P value
41.253 b 0.001
3.551 0.033
Values are means ± SEM of three composite samples of fish from replicate aquaria. Values in a column that do not have the same superscript are significantly different at P ≤ 0.05, based on Tukey's test (P b 0.05). ANOVA: analysis of variances.
Fig. 2. Relationship between dietary choline level and liver choline of cobia fed the six diets for 10 weeks.
form of choline chloride to be 696 mg kg− 1 diet for juvenile cobia under the experimental conditions used (Fig. 1). 3.2. VSI, HSI, and whole-body composition VSI of cobia ranged from 14.8–16.7% without significant dietary influences (Table 3). However, the HSI was significantly affected by dietary choline level (Table 3). HSI of fish in groups with dietary choline equal to or lower than 350 mg kg− 1 diet was significantly higher than the groups with dietary choline equal to or higher than 940 mg kg− 1 diet. The carcass crude protein, crude lipid and ash of cobia were 17.8–20.3, 8.9–9.6 and 2.8–3.3% of fresh weight, respectively (Table 3). There was no significant difference in the whole-body composition of cobia fed diets containing different levels of choline. 3.3. Lipid content in liver and muscle The lipid levels in both fish muscle (9.7–12.5%) and liver (34.7– 56.1%) were significantly influenced by dietary choline level. A general decrease trend of liver lipid was observed as dietary choline increased (Table 4). However, muscle lipid content, which was much lower than the liver lipid level, showed an increasing trend as dietary choline increased (Table 4). 3.4. Choline concentration in liver and muscle The choline concentration in cobia liver was progressively increased with increasing concentration of dietary choline within the range of 133 to 939 mg kg− 1 diet, and then leveled off. Based on linear regression of liver choline concentration (P b 0.01, R2 = 0.93), a minimum dietary requirement for choline in the form of choline chloride was estimated to be 877 mg kg− 1 diet (Fig. 2). Similarly, choline concentration in cobia muscle reached a plateau when dietary choline was higher than 950 mg kg− 1 diet (Fig. 3).
Fig. 3. Relationship between dietary choline level and muscle choline of cobia fed the six diets for 10 weeks.
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4. Discussion Juvenile cobia exhibited an obvious requirement for dietary choline for optimal growth and diet utilization in the present study. Weight gain, feed efficiency ratio, feeding rate and survival demonstrated rather consistent patterns. With reduced values for fish fed the basal diet, they gradually increased values with increasing dietary choline up to the requirement level. To minimize the possible cholinesparing effect of methionine, the estimated choline requirement was determined utilizing diets containing 1.05% methionine of dry diet, which marginally met the methionine requirement (1.19% of dry diet, Zhou et al., 2006). Based on weight gain, the optimal choline requirement for cobia was 696 mg kg− 1 diet, which was higher than blue tilapia (500 mg kg− 1 diet, Roem et al., 1990), hybrid striped bass (500 mg kg− 1 diet, Griffin et al., 1994), red drum (588 mg kg− 1 diet, Craig and Gatlin, 1996), channel catfish (400 mg kg− 1 diet, Zhang and Wilson, 1999) and yellow perch (598–634 mg kg− 1 diet, Twibell and Brown, 2000). However, other fishes, such as lake trout (1000 mg kg− 1 diet, Ketola, 1976), sturgeon (1700–3200 mg kg− 1 diet, Hung, 1989), rainbow trout (4000 mg kg− 1 diet, Poston, 1991) and hybrid tilapia (1000 mg kg− 1 diet, Shiau and Lo, 2000), may require more dietary choline. The variation in dietary requirement of various fish species for choline across studies can be attributable to fish species, age/size (Rumsey, 1991; Griffin et al., 1994) and nutritional factors such as abundance of methyl donors including methionine and betaine. Environmental influences of one-carbon metabolism and choline synthesis of aquatic animals are poorly studied at this time. It is generally recognized that excessive accumulation of lipid in liver choline-deficient animals is attributable to impaired hepatic lipoprotein secretion and subsequent accumulation of triacyglycerols (Chan, 1991). Liver lipid content has been used as an indicator of choline status in animals, including some fishes. As the case of the present study, a negative correlation between dietary choline and liver lipid has been demonstrated in lake trout (Ketola, 1976), channel catfish (Wilson and Poe, 1988) and hybrid striped bass (Griffin et al., 1994). However, rainbow trout (Rumsey, 1991) and yellow perch (Twibell and Brown, 2000) were not responsive to dietary choline level. Furthermore, Shiau and Lo (2000) found that liver lipid content of hybrid tilapia increased with dietary choline level. Similarly, Craig and Gatlin (1996) suggested that red drum could accumulate large lipid in liver and dietary choline deficiency may depress this effect. Hence, further investigations are needed to study lipid accumulation mechanism in fish liver and its influence factors. Muscle lipid content was also dependent upon dietary choline level. Muscle lipid content has been recognized as a determinant of flavor and texture for terrestrial animals as well as salmonids (Robb, 2002). Because cobia is extensively used for sashimi and sushi, highlipid in fillet may present desirable flavor and texture. Therefore, supplementation of dietary choline may prevent fatty liver, but also improve flesh quality of this fish species. Choline concentration in liver and muscle of cobia were consistently increased as dietary choline level increased, until reaching a plateau after the requirement was met. This is in agreement with most of the previous studies with channel catfish (e.g. Zhang and Wilson, 1999). However, Shiau and Lo (2000) reported that whole-body choline concentration and weight gain of hybrid tilapia was decreased when dietary choline level becomes excessive. Because liver choline was highly responsive to choline sufficiency in the diets of cobia, dietary requirement for choline was also estimated based on liver choline. The dietary choline requirement of cobia based on liver choline was 877 mg kg− 1 diet and was higher than the value based on weight gain. This indicates that cobia needs more choline to maintain some special physiological functions than to maintain normal growth. In conclusion, juvenile cobia requires exogenous choline for normal growth and physiological functions. Based on weight gain, liver and muscle choline concentration, the dietary choline requirement
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of cobia is estimated as 696, 877 or 950 mg kg− 1 diet, respectively. The influence mechanism of dietary choline on liver and muscle lipid accumulation, flesh texture and taste of cobia warrant further investigation. Acknowledgements This study was financially supported by National Key Technology R&D Program for the 11th Five-year Plan of China (Grant no.: 2006BAD03B03). The authors thank Kai Liu and Mingchao Yu for their help in feeding and sampling. Thanks are also due to Peng Li for revising this manuscript, and Lu Zhang, Chunxiao Zhang and Xingwang Liu for their assistances in the study. References Ai, Q.H., Mai, K.S., Tan, B.P., Xu, W., Duan, Q.Y., Ma, H.M., Zhang, L., 2006. Replacement of fish meal by meat and bone meal in diets for large yellow croaker, Pseudosciaena crocea. Aquaculture 260, 255–263. Association of Official Analytical Chemists (AOAC), 1990. Official Methods of Analysis of Official Analytical Chemists International, 16th edn. 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