Aquacult Int (2011) 19:143–153 DOI 10.1007/s10499-010-9348-1
Effect of partial fish meal replacement by soybean meal on the growth performance and biochemical indices of juvenile Japanese flounder Paralichthys olivaceus Jidan Ye • Xianghe Liu • Zijia Wang • Kun Wang
Received: 27 October 2009 / Accepted: 29 April 2010 / Published online: 15 May 2010 Ó Springer Science+Business Media B.V. 2010
Abstract A feeding trial was conducted to investigate the effect of partial fish meal (FM) replacement by dietary soybean meal (SBM) on the growth and protein and lipid metabolism of the juvenile Japanese flounder. Four isonitrogenous and isolipidic diets (Diets 1– 4) were formulated containing 47% protein and 9% lipid with different SBM inclusion (Diet 1, 11%; Diet 2, 16%; Diet 3, 24%; and Diet 4, 41%). The fish were fed to satiation twice daily for a feeding period of 56 days. The weight gain rate (WGR) and protein efficiency ratio of fish fed Diet 4 were significantly lower than those fed Diets 1, 2, and 3, and feed conversion ratio in the group fed Diet 4 was significantly higher than that in the groups fed Diets 1, 2, and 3. Hepatosomatic indices showed the similar trend as WGR, and the value (1.75%) for Diet 1 was significantly lower than that (1.96–2.2%) for other diets. There were no differences in whole body moisture, crude protein, crude lipid, and ash content among all treatments. With increasing dietary SBM level, serum triglyceride (TG), cholesterol (CHO), and low-density lipoprotein cholesterol (LDL-C) concentrations increased, whereas the serum total protein (TP) and high-density lipoprotein cholesterol (HDL-C) concentrations decreased. Compared with Diet 1, the serum TG, CHO, and LDLC concentrations of fish fed Diet 4 significantly increased by 78, 37, and 36%, respectively, while the TP and HDL-C concentrations decreased by 14 and 33%, respectively. No significant differences in condition factor, blood urea nitrogen concentration, and alanine and aspartate aminotransferase activities were observed among the dietary treatments. These results indicated that dietary SBM inclusion above 24% could adversely affect the growth and protein and lipid metabolism of Japanese flounder. Keywords Paralichthys olivaceus Soybean meal Feed utilization Intermediary metabolism
J. Ye (&) X. Liu Z. Wang K. Wang Xiamen Key Laboratory for Feed Quality Testing and Safety Evaluation, Fisheries College, Jimei University, 361021 Xiamen, China e-mail:
[email protected]
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Introduction Fish meal (FM) is the first choice as a raw material in aquafeed production for its high quality of protein with a well-balanced amino acid profile (Gatlin III et al. 2007). In the last two decades, although worldwide FM production remained at a relatively stable level, it still could not match the rapid worldwide development of aquaculture (Goytortu´a-Bores et al. 2006). The cost of FM increased constantly, which caused the price of commercial feed increase sharply. Thus, there is an urgent need to find alternative protein sources to make up for the shortage of FM and to secure a stable supply for commercial diets (Hardy 2006). Soybean meal (SBM) is regarded as an economical and nutritious feedstuff with high crude protein content and a reasonably balanced amino acid profile (Carter and Hauler 2000) compared to other plant proteins (Gatlin III et al. 2007). For this reason, it may be the most promising alternative protein source to FM. The evaluation of SBM as a replacer for FM has been a long-standing research priority (Hardy 1999). There has been considerable success in replacing FM with SBM in diets of aquatic animals (Dersjant-Li 2002). However, high dietary SBM inclusion led to growth retardation for most species of fish, especially for marine or carnivorous fish (Kaushik et al. 1995; Toma´s et al. 2005; Wang et al. 2006; Martı´nez-Llorens et al. 2009; Ura´n et al. 2009). This may be due to certain nutritional characteristics with essential amino acids imbalance (Watanabe et al. 1993) and/or higher ammonia excretion rates (Ballestrazzi et al. 1994; Tantikitti et al. 2005), the presence of several antinutritional factors that increase digesta viscosity and transit rate (Francis et al. 2001; Leenhouwers et al. 2006), secretion of pancreatic proteases (Olli et al. 1994), and/or cause typical histopathology changes in intestine (Boonyaratpalin et al. 1998; Krogdahl et al. 2003; Heikkinen et al. 2006) and the diet composition (Wang et al. 2006). The Japanese flounder is one of the most important marine cultured species. There is now a large and flourishing industry for this fish in China and other Far Eastern countries (Seikai 2002). As a carnivorous species, it requires a high dietary protein level and has strong dependence on FM, the inclusion level of which is above 50% in its commercial diets (Lim and Lee 2008). Previous studies on the utilization of SBM as a FM alternative for the fish were focused on the effects of dietary SBM inclusion on fish growth and feed utilization (Kikuchi et al. 1994; Kikuchi 1999; Saitoh et al. 2003; Choi et al. 2004; Pham et al. 2007). The results showed a relatively low substitute proportion of FM protein with SBM in commercial diets of the species. To our knowledge, less attention has been paid to the relationship between dietary SBM inclusion and fish physiological status (Krogdahl et al. 2003; Kaushik et al. 2004; Romarheim et al. 2006; Olsen et al. 2007), and the mechanism of poor SBM utilization by fish. In the present study, the effect of FM replacement with SBM in practical diets containing different animal-plant protein ratios on growth performance of Japanese flounder was examined and the blood biochemical parameters were determined in an attempt to understand the mechanisms of protein and lipid metabolism associated with its growth and nutrient utilization.
Materials and methods Experimental diets White FM (USA, 64.2% crude protein) and commercially dehulled and solvent-extracted SBM (Baisuihang Feed Co. Ltd., Xiamen, China, 50.4% crude protein) were used as the
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main animal and plant protein ingredients, respectively. Four isonitrogenous (47% crude protein) and isolipidic (9% crude lipid) diets (Diets 1–4) were designed with different animal–plant protein ratios (Diet 1, 4:1; Diet 2, 3:1; Diet 3, 2:1; and Diet 4, 1:1). FM protein was replaced by 5.6, 8.1, 12.1, and 20.7% of SBM protein in the four experimental diets, respectively. The ingredients and proximate composition of four experimental diets are shown in Table 1. All ingredients were finely ground in a hammer mill and passed through a 250-lm mesh sieve and weighed according to the composition of diet. The ingredients of each diet were mixed in a 3D dynamic mixer. The ingredients of each diet were blended to a homogeneous mixture. Water (approximately 50% of the diet weight) was added, and the dough was extruded to form strands and then pelleted to suitable size through a 2.5-mm die using a multifunctional spiral extrusion machinery (CD4XITS, South China University of Technology, China). The pellets were dried in a ventilated oven at 50°C for 12 h and then placed at room temperature for 1 d before sealing in plastic bags and stored at -20°C until feeding. Growth trial The experimental fish were obtained from a commercial fish farm in Zhaoan County, China and transported to our laboratory in Jimei University. The fish were reared in twelve 1,000 l fiberglass tanks (0.85 m height 9 1.22 m upper diameter, 1.04 m lower diameter) within recirculated seawater with continuous aeration. The fish were fed with a commercial Table 1 Ingredients and proximate composition of the experimental diets (as fed basis)
Ingredients (%)
Soybean meal inclusion level Diet 1 (11%)
Diet 2 (16%)
Diet 3 (24%)
Diet 4 (42%)
Fish meal
55.8
52.2
46.4
33.9
Soybean meal
11.1
16
24
41.2
a-potato starch
5
5
5
5
Shrimp head meal
2
2
2
2
Brewer yeast
3
3
3
3
Corn gluten meal
2
2
2
2
Soybean phospholipid
2
2
2
2
Squid visceral meal
1
1
1
1
Blood meal
1
1
1
1
Wheat flour
13.6
12
9.3
3.6
Betaine
0.1
0.1
0.1
0.1
Choline chloride
0.2
0.2
0.2
0.2
Fish oil
1
1.3
1.8
2.8
Vitamin premixa
0.2
0.2
0.2
0.2
Mineral premixb
2
2
2
2
Nutrient level (%)
a b
Vitamin
Mineral premix were provided by Xiamen Haikong Biotechnological Co., Ltd
Dry matter
90.25
90.56
90.65
90.47
Crude protein
47.17
47.33
47.08
47.14
Crude lipid
9.11
9.05
9.06
9.13
Ash
9.35
9.21
8.99
8.51
Animal–plant protein ratio
4.04
3.01
2.00
1.01
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diet for 2 weeks to acclimate them to experimental conditions. At the start of the feeding trial, the fish were fasted for 24 h, batch weighed (13.22 ± 0.02 g /fish), and randomly sorted into 12 tanks of 20 fish each. Three tanks were used for each dietary treatment. Fish were hand-fed to satiation twice daily (08:00 and 15:00) for 8 weeks. Approximately 30% of water was lost each week during tank cleaning, and due to evaporation, and this was replaced. Uneaten feed was collected 30 min after each feeding. Water temperature ranged from 12.3 to 17.7°C during the feeding trial. At the end of the trial, all fish were starved for 24 h and bulk weighed. Sample collection and analysis At the end of the feeding trial, five fish were randomly sampled from each tank and sacrificed with an overdose of MS 222 (tricaine methanesulfonate) solution. The fish were then pooled in plastic bags and stored at -20°C for whole body composition analysis. Another five fish from each tank were randomly sampled, anesthetized with MS 222 (100 mg/l), and weighed individually. Blood samples were then collected via venipuncture and aspirated into a microcentrifuge tube. Blood samples were allowed to clot for 2 h and centrifuged at 3,000g for 10 min at 4°C. The serum was collected, pooled by tank, and stored in microcentrifuge tubes at -80°C for subsequent analysis of blood biochemical parameters. After hemospasia, the fish was killed by a sharp blow on the head, the visceral cavity was opened, and the liver was immediately dissected out, weighed, and pooled by tank. The whole fish samples were autoclaved at 121°C for 20 min, homogenized, and dried at 65°C for 24 h for chemical analysis. The samples of the ingredients, tested diets, and fish samples were ground into fine powder using a laboratory grinder. Moisture, crude protein, crude lipid, and ash in these samples were determined according to AOAC (1995). Blood urea nitrogen (BUN), alanine aminotransferase (ALT), aspartate aminotransferase (AST), and total protein (TP) in serum were determined with their respective kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). Triglyceride (TG), cholesterol (CHO), high-density lipoprotein cholesterol (HDL-C), and low-density lipoprotein cholesterol (LDL-C) in serum were also measured with their corresponding kits (BioSino Bio-technology and Science, Inc., Beijing, China). All these parameters were determined using an automatic biochemical analyzer (Hitachi 7020, Tokyo, Japan). Calculation and statistical analysis Weight gain rate (WGR), feed conversion ratio (FCR), protein efficiency ratio (PER), hepatosomatic index (HSI), and condition factor (CF) were calculated as follows: WGR ð%Þ ¼ 100 ðWt W0 Þ=W0 FCR ¼ FI=ðWt W0 Þ PER ð%Þ ¼ 100 ðWt W0 Þ Wp HSI ð%Þ ¼ 100 W1 =Wb CF ð%Þ ¼ 100 Wb l3 where W0 (g) is the initial mean body weight, Wt (g) is the final mean body weight, FI (g) is the total amount of the diet intake per fish in each tank, Wp is the total amount of dietary
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protein intake per fish in each tank, Wl (g) is the liver weight of sampled fish, Wb (g) is the final body weight of the sampled fish, and l (cm) is the final body length of the sampled fish. Experimental results were expressed as mean ± SD. All data were subjected to oneway ANOVA test to determine whether significant differences occurred among dietary treatments after confirmation of normality and homogeneity of variance, where differences were identified, multiple comparisons among means were performed with Duncan’s multiple range test. Data expressed as percentage or ratio were subjected to arcsine or log transformation prior to statistical analysis. Significance was declared at P \ 0.05.
Results All experimental diets were well accepted by the Japanese flounder, who maintained active ingestion during the experimental period. The growth performance of the experimental fish is shown in Table 2. The survival rate of fish in each dietary treatment was 100%. With the increase of dietary SBM level, WGR and PER decreased significantly, while FCR increased significantly (P \ 0.05). Fish fed with Diet 3 and Diet 4 had significantly lower WGR, but higher FCR than fish fed with Diet 1 (P \ 0.05). PER was significantly higher in fish fed with Diet 1 than that in fish fed with other experimental diets (P \ 0.05). CF exhibited a slight reduction with increasing dietary SBM levels (P [ 0.05). HSI followed the similar trend as FCR, and the value of fish fed with Diet 1 was significantly lower than that of fish fed with other diets (P \ 0.05). There were no significant differences in body composition among all dietary treatments (P [ 0.05) (Table 3). As shown in Table 4, BUN concentration and ALT and AST activities among all dietary treatments did not have considerable differences (P [ 0.05). The TP concentration in the fish fed Diet 4 was significantly lower than that in fish fed Diet 1 and Diet 2 (P \ 0.05). TG, CHO, HDL-C, and LDL-C concentrations were significantly influenced by the dietary treatments (Table 4). TG concentration increased sharply as the dietary SBM inclusion increased up to 24% (P \ 0.05). Compared with Diet 1 and Diet 2, fish fed with
Table 2 The effect of dietary soybean meal inclusion on growth performance of juvenile Japanese flounder Parameters
Soybean meal inclusion level Diet 1 (11%)
Diet 2 (16%)
Diet 3 (24%)
Diet 4 (42%)
IBW (g)§
13.13 ± 0.02
13.15 ± 0.03
13.16 ± 0.01
13.13 ± 0.01
FBW (g)§
33.37 ± 0.95c
32.78 ± 0.43bc
31.76 ± 0.66b
29.55 ± 0.13a
c
bc
b
125.04 ± 0.71a
b
1.35 ± 0.02c
b
157.37 ± 1.04a
§
WGR (%) §
a
FCR
1.14 ± 0.03
PER (%) CF (%)
154.09 ± 4.08
§
#
HSI (%)#
c
149.38 ± 2.19
ab
1.16 ± 0.02
b
141.33 ± 2.77 1.21 ± 0.02
190.44 ± 2.11
181.94 ± 3.11
175.94 ± 2.89
1.02 ± 0.34
1.00 ± 0.31
0.99 ± 0.20
0.99 ± 0.25
1.75 ± 0.24a
2.03 ± 0.36b
1.96 ± 0.58b
2.20 ± 0.21c
Values with different superscripts in the same row show significant difference (P \ 0.05) IBW initial body weight; FBW final body weight; WGR weight gain rate; FCR feed conversion ratio; PER protein efficiency ratio; CF condition factor; HSI hepatosomatic index §
Data from each dietary treatment are mean ± SD of three replicates
#
Data from each dietary treatment are mean ± SD of 15 fish per treatment
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Table 3 Effect of dietary soybean meal inclusion on whole body composition of juvenile Japanese flounder Parameters (%)
Soybean meal inclusion level Diet 1 (11%)
Diet 2 (16%)
Diet 3 (24%)
Diet 4 (42%)
Moisture
76.09 ± 0.47
76.22 ± 0.24
76.49 ± 0.33
76.35 ± 0.10
Crude protein
15.72 ± 0.16
15.57 ± 0.32
15.45 ± 0.32
15.62 ± 0.24
Crude lipid
2.43 ± 0.28
2.39 ± 0.38
2.31 ± 0.39
2.22 ± 0.11
Ash
4.08 ± 0.73
3.99 ± 0.44
4.02 ± 0.37
4.06 ± 0.22
Crude protein, crude lipid and ash are expressed on a wet weight basis Data from each dietary treatment are mean ± SD of three replicates Values with different superscripts in the same row show significant difference (P \ 0.05)
Table 4 Biochemical indices of juvenile Japanese flounder in response to dietary soybean meal inclusion Parameters
Soybean meal inclusion level Diet 1 (11%)
Diet 2 (16%)
Diet 3 (24%)
Diet 4 (42%)
88.60 ± 8.31b
82.89 ± 6.55b
81.57 ± 7.23ab
75.79 ± 3.86a
BUN (mmol/l)
9.88 ± 1.12
11.21 ± 2.74
11.87 ± 3.02
12.32 ± 1.47
ALT (U/l)
6.09 ± 0.37
6.02 ± 0.12
5.68 ± 1.09
5.74 ± 1.31
AST (U/l)
8.04 ± 1.32
7.92 ± 1.42
7.33 ± 0.75
7.08 ± 1.23
TG (mmol/l)
4.44 ± 0.40a
4.63 ± 0.52a
6.80 ± 0.56b
7.91 ± 0.53b
CHO (mmol/l)
3.99 ± 1.14a
5.60 ± 0.72b
6.19 ± 0.85b
5.48 ± 0.59b
c
b
b
0.99 ± 0.07a
b
3.85 ± 0.58b
b
3.05 ± 0.47b
TP(g/l)
HDL-C (mmol/l) LDL-C (mmol/l) LDL-C/ HDL-C
1.48 ± 0.13
a
2.83 ± 0.22
a
1.92 ± 0.07
1.31 ± 0.25
b
3.70 ± 1.01
ab
2.91 ± 0.14
1.21 ± 0.23 4.30 ± 1.13 3.54 ± 0.08
Data from each dietary treatment are mean ± SD of three replicates Values with different superscripts in the same row show significant difference (P \ 0.05) BUN blood urea nitrogen; ALT alanine aminotransferase; AST aspartate aminotransferase; TP total protein; TG triglyceride; CHO cholesterol; HDL-C high-density lipoprotein cholesterol; LDL-C low-density lipoprotein cholesterol
Diet 3 and Diet 4 had significantly higher TG concentrations (P \ 0.05). The CHO concentration of fish fed with Diet 1 was significantly lower than that of fish fed with other experimental diets (P \ 0.05). The HDL-C concentration decreased, but the LDL-C concentration increased gradually with increasing dietary SBM inclusion. The HDL-C concentration was notably higher, whereas the LDL-C concentration was notably lower in fish fed with Diet 1 than that in fish fed with other experimental diets (P \ 0.05). The LDL-C/HDL-C ratio followed the similar trend as LDL-C concentration.
Discussion In the present study, crude protein and lipid levels of the experimental diets were formulated based on previous reports (Kikuchi 1999; Kim et al. 2002, 2006; Cho et al. 2006). Fish growth and feed utilization in the current work were inferior to those previous studies using the same species with similar body weight (Kikuchi 1999; Cho et al. 2006; Pham
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et al. 2007). However, the results were in agreement with the study by Kim et al. (2006) with similar seawater temperatures. The inferior growth performance of the fish in the present study was probably due to the lower rearing seawater temperature (12.3–17.7°C in the present study versus 20–24°C in previous studies). The present study showed that different SBM levels significantly affected the growth and feed utilization of Japanese flounder. The negative effects of WGR, FCR, and PER in response to dietary SBM increase, suggesting that dietary SBM level below 16% was suitable for Japanese flounder. Pham et al. (2007) reported that 20% FM protein replacement by cottonseed meal (9.4%) and SBM (8.7%) had no adverse effect on the growth of Japanese flounder. A similar result was observed by Kikuchi (1999), who found that 43% of FM protein could be replaced by SBM (25%) in combination with blood meal (10%) or corn gluten meal (10%) and blue mussel meat (5%). Dietary SBM inclusion of up to 32 or 20% did not affect the fish growth in another two separate feeding experiments (Saitoh et al. 2003; Choi et al. 2004). The data in present and previous studies on Japanese flounder indicated that tolerance to FM substitution by SBM alone or in combination with other plant proteins was somewhat low. In the current study, we observed a significant increase in HSI with increased dietary SBM levels. However, dietary SBM inclusion did not affected CF and body composition of fish in this study. Similar results were observed for HSI in European seabass (Dicentrarchus labrax; Kaushik et al. 2004), Atlantic cod (Gadus morhua; Hansen et al. 2007), and Japanese flounder (Pham et al. 2007), for CF in cobia (Rachycentron canadum; Chou et al. 2004) and Japanese flounder (Pham et al. 2007) and for body composition in Korean rockfish (Sebastes schlegeli; Lim et al. 2004), cobia (Zhou et al. 2005) and gilthead sea bream (Sparus aurata; Martı´nez-Llorens et al. 2009). With regard to HSI, several studies have pointed to the fact that fish fed the diet containing high lipid (Lee et al. 2002; RuedaJasso et al. 2004) or carbohydrates (Hung et al. 1990; Dias et al. 1998; Rawles and Gatlin III 1998) had higher HSI. Since SBM contains relatively high carbohydrates, high-SBM inclusion levels might result in higher HSI in the present study. Our present results showed decreased serum TP levels with the increase in dietary SBM, which was in line with the results by Tang et al. (2005). Moreover, several studies have shown that the animals fed high-quality protein feed (i.e. FM-based diet versus soy concentrate-based diet and fermented soy protein diet versus SBM diet) had higher blood concentrations of TP and/or lower BUN levels (Takagi et al. 2001; Cho et al. 2007). These results indicated a relationship between dietary protein quality and protein metabolism. Some studies have been involved in this respect. Asian seabass (Lates calcarifer) fed a plant protein-based diet had higher postprandial ammonia excretion than those fed an animal protein-based diet (Tantikitti et al. 2005), and Japanese flounder had a slight increase in nitrogen losses when fed the diet with high FM replacement by plant ingredients (Kaushik et al. 2004). Day and Plascencia Gonza´lez (2000) reported that low quality of dietary protein resulted in low dietary protein utilization of turbot (Psetta maxima), and there may be higher protein turnover and protein degradation rates in rainbow trout fed a high-SBM diet than in those fed a low-SBM diet (Martin et al. 2003). SBM inclusion may have been the result of excess protein (amino acid) catabolism in fish. As for lipid metabolism of fish involved in dietary SBM utilization, several studies showed serum CHO and/or TG levels decreased with the elevation of dietary SBM in rainbow trout (Kaushik et al. 1995; Romarheim et al. 2006), turbot (Regost et al. 1999), European seabass (Kaushik et al. 2004; Dias et al. 2005), and Atlantic cod (Hansen et al. 2007). The response was similar to what has been reported in terrestrial animals and humans (Fortyhte 1986; Bergeron and Jacques 1989; Beynen et al. 1990; Carroll and
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Kurowska 1995; Bhathena et al. 2003; Madani et al. 2004). On the contrary, increased dietary SBM level elevated CHO and/or TG level in flounder in the present study, and similar results in cobia (Zhou et al. 2005) and European seabass (Kaushik et al. 2004). Furthermore, LDL-C/HDL-C ratio increased with the elevation of dietary SBM level in the present study, which also was been found for Japanese flounder fed with graded levels of soy protein isolate or soy concentrate diet (Deng et al. 2009). As previously mentioned, the hepatic hyperplasia was related to dietary SBM. Recent results showed that the HSI increase was accompanied by elevated liver lipid content in fish fed higher plant protein diets (Sitja`-Bobadilla et al. 2005; de Francesco et al. 2007; Kjær et al. 2009). Panserat et al. (2009) observed an over-expression of genes involved in liver lipid biosynthesis (CHO metabolism and desaturation of polyunsaturated fatty acids) in rainbow trout fed the 100% plant diet (versus the FM-based diet). In addition, liver lipid was also positively correlated with serum TG and negatively correlated with HDL-C (Kotronen and Yki-Ja¨rvinen 2008). Taken together, the increase in HSI, TG, and CHO levels and LDL-C/HDL-C ratio imply that the fish may have had some disorder in lipid metabolism, leading to hyperlipidemia (Kritchevsky 1995). In conclusion, our data indicated that SBM inclusion at a relatively low level (less than 16%) did not affect the growth performance of Japanese flounder. Hypercholesterolemic effect rather than hypocholesterolemic effect occurred in Japanese flounder fed SBMcontaining diets. A higher dietary SBM inclusion might therefore compromise the health status of the fish. Acknowledgments The authors would like to thank Fudong Li, Zechun Lin and Rulong Ma for diet preparation and sampling. This work was funded by a grant from the Department of Science and Technology of Xiamen, China (Grant No. 3502Z20093024).
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