Effects of dietary amylose/amylopectin ratio on growth performance, feed utilization, digestive enzymes, and postprandial metabolic responses in juvenile obscure puffer Takifugu obscurus Xiang-he Liu, Chao-xia Ye, Ji-dan Ye, Bi-duan Shen, Chun-yan Wang & An-li Wang Fish Physiology and Biochemistry ISSN 0920-1742 Volume 40 Number 5 Fish Physiol Biochem (2014) 40:1423-1436 DOI 10.1007/s10695-014-9937-4
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Author's personal copy Fish Physiol Biochem (2014) 40:1423–1436 DOI 10.1007/s10695-014-9937-4
Effects of dietary amylose/amylopectin ratio on growth performance, feed utilization, digestive enzymes, and postprandial metabolic responses in juvenile obscure puffer Takifugu obscurus Xiang-he Liu • Chao-xia Ye • Ji-dan Ye • Bi-duan Shen • Chun-yan Wang • An-li Wang
Received: 2 November 2013 / Accepted: 31 March 2014 / Published online: 8 April 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract The effect of dietary amylose/amylopectin (AM/AP) ratio on growth, feed utilization, digestive enzyme activities, plasma parameters, and postprandial blood glucose responses was evaluated in juvenile obscure puffer, Takifugu obscurus. Five isonitrogenous (430 g kg-1 crude protein) and isolipidic (90 g kg-1 crude lipid) diets containing an equal starch level (250 g kg-1 starch) with different AM/AP ratio diets of 0/25, 3/22, 6/19, 9/16 and 12/13 were formulated. Each experimental diet was fed to triplicate groups (25 fish per tank), twice daily during a period of 60 days. After the growth trial, a postprandial blood response test was carried out. Fish fed diet 6/19 showed best growth, feed efficiency and protein efficiency ratio.
X. Liu (&) C. Ye B. Shen C. Wang A. Wang (&) Key Laboratory of Ecology and Environment Science of Guangdong Higher Education Institutes, Guangdong Provincial Key Laboratory for Healthy and Safe Aquaculture, College of Life Science, South China Normal University, Guangzhou 510631, People’s Republic of China e-mail:
[email protected] A. Wang e-mail:
[email protected] J. Ye Key Laboratory of Healthy Mariculture for East China Sea, Ministry of Agriculture, Xiamen 361021, People’s Republic of China
Hepatosomatic index, plasma total cholesterol concentration, liver glycogen and lipid content, and gluconokinase, pyruvate kinase and fructose-1,6bisphosphatase activities were lower in fish fed highest AM/AP diet (12/13) than in fish fed the low-amylose diets. Activities of liver and intestinal trypsin in fish fed diet 3/22 and diet 6/19 were higher than in fish fed diet 9/16 and diet 12/13. Activities of liver and intestinal amylase and intestinal lipase, and starch digestibility were negatively correlated with dietary AM/AP ratio. Fish fed diet 3/22 and diet 6/19 showed higher plasma total amino acid concentration than fish fed the other diets, while plasma urea nitrogen concentration and activities of alanine aminotransferase and aspartate aminotransferase showed the opposite trend. Equal values were found for viscerosomatic index and condition factor, whole body and muscle composition, plasma high-density and low-density lipoprotein cholesterol concentrations, and activities of lipase and hexokinase and glucose-6-phosphatase in liver. Postprandial plasma glucose and triglyceride peak value of fish fed diet 12/13 were lower than in fish fed the lowamylose diets, and the peak time of plasma glucose was later than in fish fed the other diets. Plasma glucose and triglyceride concentrations showed a significant difference at 2 and 4 h after a meal and varied between dietary treatments. According to regression analysis of weight gain against dietary AM/AP ratio, the optimum dietary AM/AP ratio for maximum growth of obscure puffer was 0.25. The present result indicates that dietary AM/AP ratio could affect growth performance
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and feed utilization, some plasma parameters, digestive enzyme as well as hepatic glucose metabolic enzyme activities in juvenile obscure puffer. Keywords Takifugu obscurus Amylose Amylopectin Digestive enzymes Postprandial responses
Introduction The obscure puffer, Takifugu obscurus (Abe 1949), is an anadromous species and one of the most promising candidate endemic puffer species in China (Yang and Chen 2005). The annual production of the fish farmed in freshwater reached 20,000–30,000 metric tons per year in recent years, and it has been developed rapidly owing to the large body size, rapid growth and high market value (Yang and Chen 2003). However, the nutritional requirements of this species are not well known; no commercial feed for this fish species has been developed in China yet. The conventional farming of the fish is mainly dependent on low-value trash fish (such as sardines and sand lance) as feed. Only very recently has the utilization of nutrients by juvenile obscure puffer begun to be studied (Zhong et al. 2011). Carbohydrates are the most economical source of energy available in great quantities at low prices and have protein-sparing effect in some low-protein diets and adhere to other ingredients (Hemre et al. 2002; Keshavanath et al. 2002). Although digestive and metabolic systems of fish are known to be better adapted to using protein and lipid than carbohydrate for energy, incorporation of appropriate levels of carbohydrate in diets has been the subject of many studies to reduce protein and lipid levels (Wilson 1994; Stone 2003; Mohanta et al. 2009). Carbohydrate utilization varies widely among fish species and is affected by the carbohydrate molecular complexity, structure type, source, inclusion level, gelatinization degree and interaction with other nutrients as well as the feeding habit and digestive system of fish (Shiau 1997; Hemre et al. 2002; Peres and Oliva-Teles 2002; Stone 2003). Starch is the principle digestible carbohydrate found in commercial fish and shrimp feeds. It is a complex carbohydrate composed essentially of two types of macromolecules, amylose (AM, normally 18–33 %)
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and amylopectin (AP, normally 72–82 %) depending on the botanical origin (Bule´on et al. 1998). However, starch from high-AM varieties may contain up to 70 % AM, while waxy starch contains almost none (\1 %) AM (Svihus et al. 2005). AM has a straight-chain structure with D-glucose units joined by a-(1,4) links, while AP has a branched-chain structure with glucose units connected by both a-(1,4) and a-(l,6) links (Rawles and Lochmann 2003). Structural differences in starch are associated with different patterns of digestion and postprandial glucose utilization as well as lipid regulation in sunshine bass (Morone chrysops $ 9 M. saxatilis #) (Hutchins et al. 1998; Rawles and Lochmann 2003). AM-rich starches are poorly digestible due to the fact that amylose cannot be hydrolyzed or hydrolyzed slowly by a-amylase (Svihus et al. 2005). In contrast, AP-rich starches are hydrolyzed relatively rapidly and well digested owing to rich branches easily match up by a-amylase (Velurtas et al. 2011), which may induce faster and higher glycemic and insulinemic responses compared with those high in AM (Behall et al. 1989, 2002; Granfeldt et al. 1994; Zhou and Kaplan 1997; Rawles and Lochmann 2003). The utilization efficiency of starch with different amylose/amylopectin (AM/AP) ratio for fish is contradictory. Although Pfeffer et al. (1991) observed better growth and utilization in rainbow trout (Oncorhynchus mykiss) fed diets with waxy maize starch compared with normal starch and Bergot (1993) found higher digestibility of waxy maize starch than amylomaize or normal maize in rainbow trout, Enes et al. (2006) found no differences in growth performance and feed utilization in European sea bass (Dicentrarchus labrax) fed diets with waxy and normal starch. However, Sa´ et al. (2008) found that normal starch diets appeared to the higher energy digestibility and lipogenic enzyme activities than waxy starch in white sea bream (Diplodus sargus). Chen et al. (2013) indicated that high amylose–amylopectin ratio diets significantly decreased growth performance and lowered the peak values of blood glucose and triglycerides after postprandial starch load in tilapia (Oreochromis niloticus). On the contrary, Rawles and Lochmann (2003) observed better utilization in sunshine bass fed diets with a higher proportion of amylose than amylopectin. Omnivorous fish are known to use dietary carbohydrate more efficiently than carnivorous fish (Wilson 1994). Obscure puffer is an omnivorous species, and its
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Table 1 Ingredients and proximate composition of experimental diets (g kg-1 dry matter) Diets with different amylose/amylopectin ratioa 0/25
3/22
6/19
9/16
12/13
300
300
300
300
300 270
Ingredients Fish mealb c
Casein
270
270
270
270
Yeast feed
30
30
30
30
30
Amylosed
0
43
85
127
170
Amylopectine
250
207
165
123
80
Cellulose
17
17
17
17
17
Fish oil
30
30
30
30
30
Soybean oil
30
30
30
30
30
Soya lecithin
5
5
5
5
5
Choline chloride (50 %)
5
5
5
5
5
Vitamin premixf
10
10
10
10
10
Mineral premixg
10
10
10
10
10
Ca(H2PO4)2
10
10
10
10
10
2 1
2 1
2 1
2 1
2 1
Dry matter
903
905
907
908
902
Crude protein
Vitamin C Yttrium oxide Proximate analysis
433
429
436
432
430
Crude lipid
94
92
93
92
92
Ash
94
96
95
93
94
0
30
59
89
119
Amylopectin
245
216
187
158
129
AM/AP ratio
0
Amylose
0.14
0.32
0.56
0.92
a Designations were 0/25 = 0 % amylose/70 % amylopectin in diet, 3/22 = 3 % amylose/22 % amylopectin in diet, 6/19 = 6 % amylose/19 % amylopectin in diet, 9/16 = 9 % amylose/16 % amylopectin in diet, and 12/13 = 12 % amylose/13 % amylopectin in diet. The following tables and figures were referenced by identical identifier b
Steam-dried fish meal (first feed grade) was produced by Hayduk, Peru
c
Casein was produced by Gannanzhou Kerui Dairy Products Development Co., Ltd., Gansu, China
d
High-amylose corn starch (Hylon VII, 70 % amylose) was provided by National Starch & Chemicals (Guangdong) Ltd., Guangzhou, China
e
Waxy corn starch (98 % amylopectin) was produced by Yufeng starch products Co., Ltd., Shijiazhuang, China
f
Vitamin premix (g kg-1 of mixture): L-ascorbic acid monophosphate, 150.0; myoinositol, 40.0; niacin, 36.0; DL-a-tocopheryl acetate, 20.0; thiamin hydrochloride, 4.0; riboflavin, 9.0; pyridoxine hydrochloride, 4.0; D-pantothenic acid hemicalcium salt, 14.5; D-biotin, 0.3; folic acid, 0.8; menadione, 0.2; retinyl acetate, 1.0; cholecalciferol, 0.05; cyanocobalamin, 0.01
g
Mineral premix (g kg-1 of mixture): MgSO47H2O, 80.0; NaH2PO42H2O, 370.0; KCl, 130.0; FeSO47H2O, 40.0; ZnSO47H2O, 20.0; Ca-lactate, 356.5; CuSO4, 0.2; AlCl36H2O, 0.15; Na2Se2O3, 0.01; MnSO4H2O, 2.0; CoCl26H2O, 1.0
natural food includes algae and invertebrates. It is therefore expected that it can use carbohydrates more efficiently than tiger puffer Takifugu rubripes (carnivorous species). Indeed, the optimal dietary carbohydrate level for obscure puffer has been reported recently (Liu et al. 2013). To further elucidate carbohydrate
utilization (structural differences caused) in obscure puffer, we hypothesized that fish fed diets with different dietary AM/AP ratio would exhibit different growth and metabolic responses. Therefore, the present trial was designed to investigate the effects of dietary AM/ AP ratio on growth performance, feed utilization,
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plasma intermediary metabolites, digestive enzymes as well as hepatic glucose catabolic enzyme activities in juvenile obscure puffer.
Materials and methods Experimental diets Five isonitrogenous (430 g kg-1 crude protein) and isolipidic (90 g kg-1 crude lipid) semi-purified diets were formulated to contain an equal starch level (250 g kg-1 starch). Different AM/AP ratios were obtained by using high-amylose corn starch as the amylose source and waxy corn starch as the amylopectin source, hereafter identified according to percent amylose and amylopectin inclusion in diet: 0/25 (i.e., 0 g kg-1 amylose and 250 g kg-1 amylopectin in diet), 3/22, 6/19, 9/16 and 12/13, respectively (Table 1). Fish meal and casein were used as protein sources, and fish oil and soybean oil were used as the lipid sources. Prior to preparing the experimental diets, all ingredients were grounded in a hammer mill and passed through an 80-mesh screen. All ingredients of each diet were weighed according to the composition except oil and soya lecithin and were mixed in a 3D dynamic mixer (SHY-15, Changzhou Drying Equipment Co., Ltd., Changzhou, China) to a homogeneous mixture. Lipid, lecithin and distilled water were added to the premixed dry ingredients and thoroughly mixed until homogenous in a Hobart-type mixer. The 2.5-mm diameter pellets were wetextruded using a multi-functional spiral extrusion machinery (CD4 9 1TS, South China University of Technology, Guangzhou, China) and then air-drying to about 100 g kg-1 moisture, sealed in plastic bags, and stored frozen (-20 °C) until fed. Fish and rearing conditions Juvenile obscure puffer were obtained from Guangzhou Jinyang Aquaculture Co., Ltd., Guangdong Province and were stocked into two re-circular rectangular concrete ponds (3 m 9 2 m 9 2 m, L 9 W 9 H) with roughly equal number of individuals each for 2 weeks. During the holding period, fish were maintained on commercial diet twice daily. Healthy fish with an initial weight of 7.0 ± 0.5 g were randomly
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allocated into 15 circular fiberglass tanks (300-L, 3 tanks per diet, 25 fish per tank) within a re-circulating system. Fish were hand-fed the experimental diets to satiation twice daily at 8:00 and 16:00 under a natural photoperiod during a 60-day feeding period. To minimize overfeeding, the amount of diet offered was adjusted by checking the bottom of the tanks for excess feed remaining 30 min after each feeding. Two hours after feeding, uneaten feed and fecal residues were removed. Fecal samples were collected each morning prior to the next feeding. Feces collected from the settling columns were immediately filtered with filter paper at 4 °C and stored at -20 °C for chemical analyses (Zhou et al. 2004). During the feeding trial, water temperature was kept at 28 ± 2 °C, dissolved oxygen was not less than 6.0 mg L-1, pH ranged from 7.3 to 8.2, and ammoniaN and nitrite-N were maintained lower than 0.5 and 0.1 mg L-1, respectively. Analysis and measurement Samples collection At the termination of the feeding trial, the fish were starved for 24 h. All fish in each tank were weighed and counted. Five fish from each tank were randomly selected and anesthetized (MS-222, 50 mg L-1) for length and weight measurements. Then, blood, liver, muscle and intestinal samples were taken for analysis. Blood was withdrawn from the caudal vein of individuals using 2.5-mL sterile syringes. Plasma samples were collected after centrifugation at 3,0009g for 20 min at 4 °C and pooled into one tube for each tank and stored at -80 °C prior to analysis of biochemical indices. After blood collection, the liver, intestine and muscle were immediately excised, weighted and stored at -80 °C for subsequent analysis. Another three fish from each tank were randomly sampled and frozen at -20 °C for subsequent analysis of proximate whole-body composition. The remaining fish were continued to be maintained on the former diets for 7 days. Fish were fed a final meal, after that six fish per experimental diet was killed at predetermined intervals (0, 1, 2, 4, 8, 12 and 24 h postprandial) for blood sampling. Plasma samples were collected after centrifugation at 3,0009g for 20 min at 4 °C and were stored at -80 °C until analyzed for glucose and triglyceride concentrations.
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Chemical analysis Dry matter, crude protein, crude lipid and ash gross energy contents in ingredients, diets, feces and fish samples were determined according to the methods of the Association of Official Analytical Chemists (AOAC 1998). Moisture was determined by the drying method using an oven at 105 °C. Crude protein was determined by the Kjeldahl method (N 9 6.25) using KjeltecTM 8400 Auto Sample Systems (Foss Tecator AB, Ho¨gana¨s, Sweden). Crude lipid was determined by the Soxhlet method using a Soxtec Avanti 2050 (Foss Tecator AB, Ho¨gana¨s, Sweden). Ash was determined by the combustion method using a muffle furnace at 550 °C. Diets and feces Yttrium oxide were determined using an inductively coupled plasma mass spectrometry [IRIS Advantage (HR), Thermo Jarrel Ash Corporation, Boston, MA, USA] after perchloric acid digestion. The total starch content in corn starch, diets and feces were determined by using total starch assay kits, and the amylose content in corn starch and diets were analyzed by using amylose assay kits (Megazyme International Ireland Ltd., Ireland). Biochemical analysis The frozen liver and intestine samples from each tank were homogenized at a ratio of 1:10 (w/v) (tissue weight/ volume of chilled 10 mmol Tris–HCl buffer at pH 7.4). Enzyme extract was obtained after centrifugation at 3,0009g for 20 min at 4 °C. The supernatant was recovered and kept at 4 °C; all enzymatic assays were conducted within 24 h after extraction. Trypsin, amylase and lipase activities were measured by Folin phenol reagent, iodine solution to reveal non-hydrolyzed starch, and q-nitrophenyl colorimetry method using casein, soluble starch and q-nitrophenyl palmitate as the substrate by using commercial kits [Nanjing Jiancheng Biotechnic Institute (NJBI), Nanjing, China], respectively. Blood glucose was determined by the glucose oxidase method by using a kit (NJBI, Nanjing, China). Liver and muscle glycogen were determined by the anthrone reagent method (Carroll et al. 1956). Triacylglycerol (TG), total cholesterol (T-CHO), highdensity lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), total amino acids (TAA) and urea nitrogen (UN) concentrations, and aspartate aminotransferase (AST, EC 2.6.1.1) and
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alanine aminotransferase (ALT, EC 2.6.1.2) activities were measured using diagnostic reagent kits (BioSino Bio-technology and Science, Inc., China) based on colorimetric reactions in an automatic analyzer (Hitachi 7020, Japan). The frozen liver samples were homogenized (dilution 1/10) in ice-cold buffer (30 mM HEPES, 0.25 mM sucrose, 0.5 mM EDTA, 5 mM K2HPO4, 1 mM DTT, pH 7.4). Homogenates were centrifuged at 9009g for 10 min at 4 °C, and the supernatant was separated for HK and GK activity measurements. Hexokinase (low Km HK; EC 2.7.1.1) and gluconokinase (GK, high Km HK or HK IV; EC 2.7.1.11) activities were measured using 0.5 mM and 100 mM of glucose, respectively, as described previously (Tranulis et al. 1996; Panserat et al. 2000b) at 37 °C by coupling ribulose-5-phosphate formation from glucose-6-phosphate to the reduction in b-NADP using purified glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase as coupling enzymes. This assay for measuring GK activity on frozen samples necessitated correction by measuring glucose dehydrogenase (EC 1.1.1.47) activity as described by Tranulis et al. (1996). The supernatant was centrifuged at 10,0009g for 20 min at 4 °C, and the resultant cytosolic fraction was used for enzyme activity measurements. Pyruvate kinase (PK; EC 2.7.1.40), glucose-6-phosphatase (G6Pase; EC 3.1.3.9) and fructose-1,6-bisphosphatase (FBPase; EC 3.1.3.11) activities were measured using lactate dehydrogenase (LDH; EC 1.1.1.27) (Foster and Moon 1990), glucose dehydrogenase in excess (Alegre et al. 1988), glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase (Tranulis et al. 1996) as the coupling enzyme at 37 °C by monitoring the decrease in absorbance at 340 nm, respectively. One unit of enzyme activity was defined as the amount of enzyme that catalyzed the hydrolysis of 1 lmol of substrate by per mg protein per minute at 37 °C. Protein content of the supernatant solutions was determined using bovine serum albumin as a standard at 37 °C based on the method of (Bradford 1976). Statistical analysis Data expressed as percentages or ratios were subjected to arcsine transformation prior to statistical analysis. Results are presented as mean ± S.D. The normality and variance’s homogeneity of all data were systematically checked before applying One-way ANOVA
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Table 2 Growth performance and morphological indicators for juvenile obscure puffer fed diets containing different amylose/ amylopectin ratio for 60 days Diets with different amylose/amylopectin ratio 0/25 FBW (g) WG (%) PER FE HSI (%)
3/22
21.1 ± 0.1b 199 ± 4
22.5 ± 0.2c
b
217 ± 5
1.44 ± 0.03
b
0.60 ± 0.03
ab
11.1 ± 0.2
b
6/19
9/16
22.8 ± 0.3c
c
21.2 ± 0.3b
c
223 ± 5 bc
1.49 ± 0.05
b
12/13
201 ± 6 c
1.53 ± 0.04
b
20.2 ± 0.2a
b
186 ± 2a b
1.30 ± 0.03a
a
0.54 ± 0.03a
1.41 ± 0.04
0.62 ± 0.02
0.65 ± 0.02
0.58 ± 0.03
b
b
b
9.7 ± 0.3a
11.2 ± 0.3
11.3 ± 0.2
11.0 ± 0.3
VSI (%)
16.7 ± 0.5
16.2 ± 0.7
16.4 ± 0.6
16.0 ± 0.8
15.8 ± 0.5
CF
2.51 ± 0.28
2.56 ± 0.33
2.61 ± 0.25
2.48 ± 0.25
2.42 ± 0.18
Values are mean ± SD (n = 3). Means in the same lines with different superscripts indicate significant difference (P \ 0.05) FBW final body weight, WG weight gain (%) = 100 9 [(FBW - initial body weight) 9 initial body weight-1], PER protein efficiency ratio = wet weight gain 9 crude protein intake-1, FE feed efficiency = wet weight gain 9 dry feed consumed-1, HSI hepatosomatic index (%) = 100 9 (liver weight 9 body weight-1), VSI viscerosomatic index (%) = 100 9 (viscera weight 9 body weight-1), CF condition factor = 100 9 [body weight 9 (whole-body length3)-1]
using the SPSS 17.0 for Windows software package (SPSS Inc., Chicago, Illinois, USA). Significant differences among groups were determined by the Tukey’s multiple range test. Significance is reported at P \ 0.05.
Results Final body weight and weight gain were significantly higher in fish fed diet 3/22 and diet 6/19 than fish fed the other diets (P \ 0.05) (Table 2). The polynomial regression equation between weight gain and the amylopectin content in diet was y = -0.7954 x2 ? 31.266 x - 87.989 (R2 = 0.9208). Protein efficiency ratio was significantly higher in fish fed diet 6/19 than in fish fed the other diets except diet 3/22 (P \ 0.05). Feed efficiency was significantly higher in fish fed diet 3/22 and diet 6/19 than in fish fed diet 9/16 and diet 12/13 (P \ 0.05). Fish fed diet 12/13 had lower HSI compared with fish fed the other diets (P \ 0.05). VSI and CF did not vary across dietary treatments. There were no significant differences in whole body and muscle moisture, crude protein, crude lipid, ash and muscle glycogen contents of fish fed diets containing different AM/AP ratio (Table 3). Liver glycogen and lipid contents were significantly lower in fish fed diet 12/13 than in fish fed the other diets (P \ 0.05). The apparent digestibility of dry matter,
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crude protein, starch and energy in fish fed diet 12/13 were lower than in fish fed diet 0/25, diet 3/22 and diet 6/19 (P \ 0.05) (Table 4). Crude lipid digestibility did not differ among treatments. Trypsin, amylase and lipase activity in liver and intestine of fish were shown in (Table 5). Liver trypsin activity was significantly lower in fish fed diet 12/13 than in fish fed the other diets (P \ 0.05), and fish fed diet 9/16 had lower trypsin activity in liver compared with fish fed diet 0/25, diet 3/22 and diet 6/19 (P \ 0.05). Liver amylase activity was significantly higher in fish fed diet 0/25 than in fish fed the other diets (P \ 0.05). Intestinal trypsin activity was significantly higher in fish fed diet 3/22 and diet 6/19 than in fish fed diet 9/16 and diet 12/13 (P \ 0.05). Fish fed diet 9/16 and diet 12/13 had lower intestinal amylase and lipase activity compared with fish fed the other diets (P \ 0.05). Liver lipase activity did not differ among treatments. Plasma biochemical parameters of fish fed diets containing different AM/AP ratio were provided in Table 6. Plasma total cholesterol concentrations were significantly lower in fish fed diet 12/13 than in fish fed the other diets (P \ 0.05). Plasma total amino acids concentrations were significantly higher in fish fed diet 3/22 and diet 6/19 than in fish fed the other diets (P \ 0.05). Blood urea nitrogen concentrations were significantly higher in fish fed diet 12/13 than in fish fed the other diets (P \ 0.05). Plasma AST and ALT activities were significantly affected by dietary AM/AP
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Table 3 Proximate analysis of whole body and muscle, liver glycogen and lipid content of juvenile obscure puffer fed diets containing different amylose/amylopectin ratio for 60 days Diets with different amylose/amylopectin ratio 0/25
3/22
6/19
9/16
12/13
Whole body Moisturea
728 ± 3
725 ± 4
726 ± 7
732 ± 4
733 ± 5
Crude proteina
144 ± 2
148 ± 6
148 ± 5
143 ± 8
141 ± 3
Crude lipida
62 ± 2
62 ± 3
61 ± 2
59 ± 3
57 ± 3
Asha
25 ± 2
25 ± 3
24 ± 2
24 ± 1
23 ± 2
Moisturea
768 ± 5
763 ± 6
765 ± 4
762 ± 10
769 ± 7
Crude proteina
179 ± 4
180 ± 4
186 ± 4
183 ± 3
181 ± 2
7±1
8±1
8±1
8±1
7±1
14 ± 2
13 ± 2
13 ± 1
12 ± 2
13 ± 1
Glycogenb Liver
6.48 ± 0.67
6.85 ± 0.44
6.75 ± 0.39
7.11 ± 0.56
6.72 ± 0.54
Glycogenb
16.07 ± 0.37b
15.87 ± 0.55b
16.14 ± 0.54b
15.46 ± 0.58b
14.39 ± 0.39a
Muscle
Crude lipida Asha
b
Lipid
b
431 ± 18
b
432 ± 19
437 ± 17
b
415 ± 21
ab
386 ± 13a
Values are mean ± SD (n = 3). Means in the same lines with different superscripts indicate significant difference (P \ 0.05) a
Moisture, crude protein, crude lipid and ash content were expressed g kg-1 (wet weight basis)
b
Muscle glycogen, liver glycogen and lipid content were expressed mg g-1 tissue
Table 4 Apparent digestibility coefficient of nutrients of juvenile obscure puffer fed diets containing different amylose/amylopectin ratio for 60 days Diets with different amylose/amylopectin ratio 0/25
3/22 b
73.3 ± 2.5
6/19 b
72.5 ± 2.6
9/16 b
69.2 ± 2.1
12/13 ab
67.8 ± 1.8a
Dry matter
73.1 ± 2.3
Crude protein
86.3 ± 3.1ab
88.7 ± 1.5b
88.2 ± 2.9b
85.6 ± 2.5ab
82.5 ± 2.3a
Crude lipid Starch
91.1 ± 2.3 73.7 ± 2.8c
90.2 ± 2.8 71.8 ± 1.8c
89.3 ± 2.7 70.5 ± 1.9bc
88.6 ± 2.3 66.8 ± 2.3ab
88.2 ± 1.9 62.9 ± 2.7a
Energy
76.6 ± 2.2b
77.3 ± 1.7b
76.8 ± 1.3b
74.0 ± 1.9ab
71.3 ± 2.5a
Values are mean ± SD (n = 3). Means in the same lines with different superscripts indicate significant difference (P \ 0.05) ADC of nutrient (%) = 100 9 [1 - (% nutrient in feces) 9 (% nutrient in diet)-1 9 (Y2O3 in diet) 9 (Y2O3 in feces)-1
ratio (P \ 0.05), and the highest value was observed in fish fed diet 12/13. Plasma high-density lipoprotein cholesterol and low-density lipoprotein cholesterol concentrations were not affected by dietary treatments. Postprandial plasma glucose concentrations were significantly (P \ 0.05) affected by dietary treatments (Fig. 1a). Plasma glucose concentration of fish fed diet 0/25 reached the peak at 2 h, fish fed diet 3/22, diet 6/19 and diet 9/16 were at 4 h, and fish fed diet 12/13 was at 8 h after a meal, and thereafter, the values gradually decreased to the preprandial levels at 12 h. Plasma
glucose concentrations showed a significant difference at 1, 2 and 4 h after a meal between dietary treatments (P \ 0.05). Plasma triglyceride concentrations reached the peak at 8 h in fish fed all diets (Fig. 1b), and thereafter, the values gradually decreased to the preprandial levels at 24 h. Plasma triglyceride concentrations also showed a significant difference at 2, 4 and 8 h after a meal between dietary treatments (P \ 0.05). The peak values of plasma glucose and triglyceride concentrations in fish fed diet 9/16 and diet 12/13 were lower than fish fed the other diets (P \ 0.05).
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Table 5 Liver and intestine digestive enzyme activity of juvenile obscure puffer fed diets containing different amylose/amylopectin ratio for 60 days Diets with different amylose/amylopectin ratio 0/25
3/22
6/19
9/16
12/13
Liver digestive enzyme Trypsin Amylase Lipase
1,189 ± 137bc 0.7 ± 0.1
1,390 ± 121c
c
0.5 ± 0.1
35.4 ± 3.5
b
37.2 ± 5.7
1,257 ± 108c 0.5 ± 0.1
b
32.5 ± 4.8
937 ± 158b b
0.4 ± 0.1
691 ± 155a 0.2 ± 0.1a
35.1 ± 7.5
34.5 ± 5.5
438 ± 69a
403 ± 55a
Intestinal digestive enzyme Trypsin Amylase Lipase
453 ± 48ab 2.6 ± 0.2
c
37.5 ± 3.4
d
537 ± 52b 2.6 ± 0.2
c
28.4 ± 1.6
c
520 ± 56b 2.5 ± 0.2
c
21.0 ± 1.8
b
b
1.9 ± 0.1a
a
14.3 ± 2.9a
2.2 ± 0.1 15.4 ± 2.0
Values are mean ± SD (n = 3). Means in the same lines with different superscripts indicate significant difference (P \ 0.05) Enzymes activities were expressed U mg-1 protein Table 6 Plasma biochemical parameters of juvenile obscure puffer fed diets containing different amylose/amylopectin ratio for 60 days Diets with different amylose/amylopectin ratio
T-CHO
0/25
3/22
6/19
9/16
12/13
7.91 ± 0.24b
8.21 ± 0.33b
8.42 ± 0.29b
8.07 ± 0.22b
7.26 ± 0.27a
HDL-C
2.29 ± 0.15
2.34 ± 0.12
2.39 ± 0.11
2.19 ± 0.09
2.16 ± 0.13
LDL-C
0.60 ± 0.05
0.55 ± 0.07
0.47 ± 0.13
0.51 ± 0.09
0.61 ± 0.11
TAA
33.7 ± 3.1b
40.8 ± 4.0c
39.9 ± 2.6c
27. ± 3.6a
24.5 ± 2.5a
UN AST ALT
ab
7.38 ± 0.65
a
6.81 ± 0.35
a
a
339 ± 15
16.3 ± 1.3
a
323 ± 17
15.8 ± 1.5
a
a
6.67 ± 0.21 ab
350 ± 19
a
16.1 ± 1.2
b
7.97 ± 0.42 b
376 ± 17
ab
17.5 ± 1.3
9.48 ± 0.23c 437 ± 13c 18.8 ± 1.2b
Values are mean ± SD (n = 3). Means in the same lines with different superscripts indicate significant difference (P \ 0.05) T-CHO total cholesterol, HDL-CHO high-density lipoprotein cholesterol, LDL-CHO low-density lipoprotein cholesterol, TAA total amino acids, UN urea nitrogen, ALT alanine aminotransferase, AST aspartate aminotransferase Plasma T-CHO, HDL-C, LDL-C, TAA and UN were expressed mmol l-1 Plasma AST and ALT were expressed U l-1
Hepatic enzyme activities of fish fed diets containing different AM/AP ratios were provided in Table 7. GK, PK and FBPase activities were significantly lower in fish fed diet 12/13 than in fish fed the other diets (P \ 0.05). HK and G6Pase activities of fish were not affected by dietary treatments.
Discussion Our results on WG, FE and PER agreed with results reported in tilapia saying that containing amylose–
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amylopectin at ratio of 0.24 enhanced growth (Chen et al. 2013); however, also opposite results have been reported (Rawles and Lochmann 2003). Our finding that an AM/AP ratio of 0.25 (5/20) is consistent with previously reported (Dai et al. 2008; Deng et al. 2010), wherein the dietary AM/AP ratio at 0.23 was suitable for its production. The optimal ratio found by us, and others are close to the average value of AM/AP normally found in starches (Shibanuma et al. 1994; Bule´on et al. 1998; Hoover 2001). The digestion of starch depends on its amylose to amylopectin ratio and their molecular weight (Granfeldt et al. 1994).
Author's personal copy
10
12/13
5 4
P=0.592
6
P=0.361
7
P=0.378
-1
3/22 6/19 9/16 P=0.195
8
Plasma glucose (mmol l )
0/25
P=0.001
9
1431
P=0.016
A
P=0.001
Fish Physiol Biochem (2014) 40:1423–1436
3 2 1 0
0
2
4
6
8
10
12
14
16
18
20
22
24
Time (h) after feeding
0/25 3/22 6/19 9/16
-1
P=0.037
7
Plasma triglyceride (mmol l )
P=0.021
8 P=0.001
B
P=0.385
P=0.183
P=0.351
5
12/13
P=0.232
6
4
3
2
0
2
4
6
8
10
12
14
16
18
20
22
24
Time (h) after feeding
Fig. 1 Postprandial plasma glucose (a) and triglyceride (b) concentrations in juvenile obscure puffer fed diets containing different amylose/amylopectin (AM/AP) ratio over 60-day
feeding period. Data are mean ± SD (n = 6) representing six fish per experimental diet used at each sampling time. P indicates the difference between treatments at each sampling time
Amylose is more resistant to hydrolytic enzymes compared with amylopectin (Kabir et al. 1998), which may be partly attributed to the presence or development of resistance starch (Behall and Hallfrisch 2002), whereas amylopectin allows a greater access to digestive enzymes. In the present study, a negatively linear correlation was found between dietary AM/AP ratio and starch digestibility (R2 = 0.9935), which reflected the direct impact of dietary AM/AP ratio on
starch digestion at a larger level. Indeed, waxy maize starch digestibility was significantly higher than normal maize or amylomaize starch in rainbow trout (Bergot 1993) and European sea bass (Enes et al. 2006). Significantly lower ADCs of protein and energy were found in fish fed high-amylose diet (12/ 13) compared with low-amylose diets, which may partly account for the inferior growth and feed utilization of fish. Also, no differences were observed
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Fish Physiol Biochem (2014) 40:1423–1436
Table 7 Hepatic enzyme activities of juvenile obscure puffer fed diets containing different amylose/amylopectin ratio for 60 days Diets with different amylose/amylopectin ratio 0/25
3/22
6/19
9/16
12/13
HK
5.62 ± 0.35
6.03 ± 0.53
6.25 ± 0.42
5.83 ± 0.37
5.77 ± 0.31
GK
37.6 ± 2.5b
37.3 ± 3.3b
39.5 ± 2.9b
35.8 ± 2.3ab
30.7 ± 3.1a
PK
32.9 ± 1.8c
31.1 ± 1.5c
29.7 ± 1.7bc
28.3 ± 1.4ab
25.8 ± 1.6a
G6Pase
13.5 ± 3.2
13.6 ± 2.4
12.8 ± 3.4
11.6 ± 2.8
11.2 ± 2.3
FBPase
18.2 ± 2.4b
19.4 ± 1.6b
19.5 ± 2.6b
16.4 ± 2.3ab
13.3 ± 2.1a
Values are mean ± SD (n = 3). Means in the same lines with different superscripts indicate significant difference (P \ 0.05) Enzymes activities were expressed mU mg-1 protein HK hexokinase, GK gluconokinase, PK pyruvate kinase, G6Pase glucose-6-phosphatase, FBPase fructose-1,6-bisphosphatase
in ADCs of protein and energy between fish fed all amylopectin (0/25) diet and low-amylose diets. However, significantly lower ADCs of protein and energy in white sea bream fed the high waxy starch diets compared with normal starch diets, which indicated that waxy starch negatively interfered with protein digestibility (Sa´ et al. 2008). Enlargement of liver size is associated with increased storage of lipid and glycogen (Brauge et al. 1994; Hutchins et al. 1998; Gumus and Ikiz 2009). Our results indicating debase lipid synthesis and deposition in fish fed high-amylose diet agree with results in sunshine bass (Rawles and Lochmann 2003) and tilapia (Chen et al. 2013). The liver glycogen and lipid content were decreased in fish fed the highamylose diet, like the findings in high-amylose-fed sunshine bass (Rawles and Lochmann 2003). Previous studies showed that high levels starch diet could elevate liver glycogen deposits in rainbow trout, eel (Angilla Anguilla; Sua´rez et al. 2002) and European sea bass (Enes et al. 2006), indicating the relative low ability of these carnivorous fish to use glucose for energy. However, Chen et al. (2013) observed that higher liver glycogen deposition in tilapia fed the high-AM/AP ratio diet compared with at the low ratio. The variations may be caused by the difference in fish species. The proximate composition of whole body and muscle was hardly affected by dietary AM/AP ratio, as previously reported for sea bass (Peres and OlivaTeles 2002), rainbow trout (Brauge et al. 1994) and tilapia (Solomon et al. 2007; Chen et al. 2013). Although not significant, there was a progressive reduction in whole-body lipid retention to dietary AM/ AP ratio. Some authors had observed an increase in
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whole-body lipid content with increased dietary carbohydrate (Kaushik et al. 1989; Shimeno et al. 1996), while others found an opposite effect (Refstie and Austreng 1981; Hilton and Atkinson 1982). Digestive enzyme activities were suggested as predictors of potential feed utilization and growth differences (Sunde et al. 2001) and in fish appear to be strongly correlated with the feeding behavior, the quantity and composition of diet, and a number of other factors (Pe´res et al. 1998; Pe´rez-Jime´nez et al. 2009). Higher trypsin activities in liver and intestinal of fish fed diet 3/22 and diet 6/19 could improve crude protein digestibility (Table 4) and show better growth performance and protein efficiency ratio with these diets (Table 2). Some studies reported that the AM/AP ratio affected the digestion of starch and other macronutrients and its metabolic responses (Deng et al. 2010; He et al. 2010). Chen et al. (2013) observed digestive enzyme activities, and starch digestibility dramatically decreased as dietary AM/AP ratio increased. Activities of amylase in liver and intestine were negatively correlated with dietary AM/AP ratio, R2 = 0.9305 and R2 = 0.9433, respectively, and starch digestibility showed the same trend as amylase activity, which reflected that carbohydrates digestion was evidently influenced by dietary AM/AP ratio at a larger level, and these results were consistent with previous studies (Kabir et al. 1998; Svihus et al. 2005; Denardin et al. 2012). The intestinal lipase activity was a significant reduction in fish fed the highamylose diets, and crude lipid digestibility was negatively correlated with dietary AM/AP ratios (R2 = 0.9066), and it may be related that amylose– lipid complexes are resistant to enzymatic hydrolysis and slow the digestion or absorption of the high-
Author's personal copy Fish Physiol Biochem (2014) 40:1423–1436
amylose rice (Hu et al. 2004; Wu et al. 2006), though little is known about the mechanisms controlling these effects. The amount of native starch hydrolysis by amylase is reported to be inversely related to the amylose content (Rendleman 2000; Tester et al. 2006; Zhu et al. 2011). High-amylose starches have been shown to differ from high-amylopectin starches in postprandial plasma glucose and insulinemic responses and be associated with a lowered rate of amylolysis (Zhou and Kaplan 1997; Behall and Hallfrisch 2002; Aziz et al. 2009). Postprandial plasma glucose concentration had decreased significantly as dietary AM/AP ratio increasing, meanwhile the time of plasma glucose peak was postponed (Fig. 1a), and similar results observed in sunshine bass (Rawles and Lochmann 2003) and tilapia (Chen et al. 2013). Higher plasma glucose flowing to liver in fish fed the lowamylose diets resulted in increased hepatic metabolism and caused liver hypertrophy as glycogen and/or lipid accumulation (Table 3), and it was also consistent with the HSI values. The lower glycemic response was observed in fish fed the high-amylose diet (Rawles and Lochmann 2003; Chen et al. 2013), and a similar phenomenon was observed in mammals (Behall and Scholfield 2005; Aziz et al. 2009). The invariable plasma glucose concentrations after 8–24 h feed deprivation indicated that obscure puffer may have good regulation capacity of absorbed glucose. Denardin et al. (2007) suggested that high blood glucose concentration as being the main determining factor for high serum total cholesterol and triglyceride concentration, and higher glucose flow in liver would be metabolized into fatty acids, increasing serum triglyceride and cholesterol concentration. The peak of blood triglyceride paralleled with the glucose change in response to dietary amylose–amylopectin ratio in tilapia (Chen et al. 2013). Postprandial plasma triglyceride concentration is significantly reduced as dietary AM/AP ratio is increasing (Fig. 1b), and it may be related to the downgrade of plasma glucose concentration (Fig. 1a) and intestine lipase activity inhibition (Table 5). Behall and Howe (1995) suggested that plasma triglyceride and total cholesterol levels significantly decreased after consumption of rich amylose diet compared with a rich amylopectin diet in human. In general, AST and ALT mainly exist in hepatocytes and cardiomyocytes and play important roles in
1433
protein metabolism. When the liver and myocardial cells are damaged or their permeability increased, AST and ALT will be released into the blood, resulting in elevated blood transaminase activity (Ming et al. 2012). Therefore, the activities of AST and ALT in the blood can be used monitor the health status of fish. Activities of plasma AST and ALT were significantly increased in fish fed the high-amylose diet, indicating that the higher AM/AP ratio diet would be undermined protein utilization and glucose metabolic responses. However, amino acid metabolism-related enzymes (AST, ALT and glutamate dehydrogenase) activities were not affected by starch sources in white sea bream (Sa´ et al. 2008). Furthermore, plasma total amino acid concentration significantly decreased with increasing dietary AM/AP ratio, while plasma urea nitrogen concentration showed a reverse trend. Chen et al. (2013) observed that peak total amino acid time was delayed in fish fed the high-amylose diet compared with the low-amylose diet in tilapia, and the highest dietary AM/AP ratio produced the weakest metabolic responses, regardless of blood glucose, triglyceride or total amino acids. These results mentioned above suggested that protein and amino acid metabolism could be enhanced as fish fed the low-amylose diet, and it is in accordance with protein efficiency ratio. This is the first study on key hepatic glycolytic and gluconeogenic enzymes involved in glucose metabolic pathway in puffer fish. A significant lower on the glycolytic enzymes (GK and PK) and gluconeogenic enzyme (FBPase) activities in liver of fish fed the high-amylose diet compared with those fed the lowamylose diets were observed, and it is in line with previous results in common carp (Panserat et al. 2000a) and European sea bass (Enes et al. 2006). However, FBPase activity regulation was dietary protein levels and not dietary carbohydrates (Enes et al. 2006). Kirchner et al. (2003) reported that rainbow trout fed the high protein diet had higher activity of FBPase than low-protein diet. G6Pase activity in liver was not affected by dietary AM/AP ratio; previous studies with this species also confirmed that G6Pase activities were not regulated by dietary carbohydrates (Liu et al. 2013), and these results agreed with Panserat et al. (2000b) and Enes et al. (2006, 2008). In conclusion, our data demonstrated that the appropriate dietary AM/AP ratio could improve growth performance, feed utilization, liver and intestine
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Author's personal copy 1434
digestive enzyme activities as well as hepatic glucose catabolic enzyme activities in juvenile obscure puffer. Moreover, the optimum dietary AM/AP ratio of obscure puffer for maximum weight gain was 0.25 and is close to the average value of AM/AP found in cereal starch. Postprandial plasma glucose and triglyceride responses were affected by dietary AM/AP ratio. Acknowledgments This research was supported by Project for the Construction of Guangdong Provincial Key Laboratory (2009A060800019), the Guangdong Education UniversityIndustry-Research Cooperation Project (2011B090500009), and the Key Project of Department of Education of Guangdong Province (CXZD1114). The authors would like to thank Qiu-Xia Zhang, Li-Mian Zheng, Ji-Chang Zhou and Jian Pen for their assistance in this study.
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Author's personal copy 1436 Zhong G, Hua X, Yuan K, Zhou H (2011) Effect of CGM on growth performance and digestibility in puffer (Takifugu fasciatus). Aquacult Int 19:395–403 Zhou X, Kaplan ML (1997) Soluble amylose cornstarch is more digestible than soluble amylopectin potato starch in rats. J Nutr 127:1349–1356 Zhou QC, Tan BP, Mai KS, Liu YJ (2004) Apparent digestibility of selected feed ingredients for juvenile cobia, Rachycentron canadum. Aquaculture 241:441–451
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