Aquaculture Reports 20 (2021) 100666

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Aquaculture Reports
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Optimal dietary lipid requirement for juvenile Asian red-tailed catfish

(Hemibagrus wyckioides)
Dietary lipid level for Hemibagrus wyckioides
Junming Deng a, b, Xindang Zhang b, Yan Sun b, Lu Zhang c, *, Haifeng Mi c, *
a
College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China
b
College of Animal Science and Technology, Yunnan Agricultural University, Kunming, 650201, China
c
Tongwei Co., Ltd., Chengdu, 610093, China

A R T I C L E I N F O A B S T R A C T

Keywords: This study investigated the effects of dietary lipid content on growth rate, feed utilization, digestive enzyme
Antioxidant capacity activity, and antioxidant capacity of juvenile Asian red-tailed catfish (Hemibagrus wyckioides), and thereby to
Asian red-tailed catfish evaluate the optimal dietary lipid requirement. Five isoproteic diets were prepared to contain varied levels of
Growth
dietary lipid (3 %, 5.5 %, 8 %, 10.5 %, and 13 %). Each diet was fed to triplicate groups of juveniles (average
Lipid requirement
body weight 3.20 g) in a recirculating farming system maintained at 28 ± 1 ◦ C. Daily gain coefficient (DGC) and
protein efficiency ratio improved steadily with the dietary lipid content up to 10.5 %, and then reached a plateau.
Similarly, protein retention increased gradually with the dietary lipid content up to 13 %. Conversely, lipid
retention decreased linearly with increasing dietary lipid content, but no significant difference was found among
juveniles fed diets with 8 %, 10.5 %, and 13 % lipid. The optimum feed conversion ratio (FCR) was observed in
juveniles fed diets with 10.5 % or 13 % lipid. Plasma insulin-like growth factor 1 level increased steadily with the
dietary lipid content up to 8 %. However, plasma amino methyl propanediol, aspartate aminotransferase and
alanine aminotransferase activities depressed generally with increasing dietary lipid content. Besides, the highest
hepatic peroxidase, catalase, glutathione peroxidase, and alkaline phosphatase activities were found in juveniles
fed diet with 10.5 % lipid. Single-slope broken-line regression analysis of DGC or FCR response to varied levels of
dietary lipid showed that the optimal dietary lipid requirement of juvenile H. wyckioides was 11.1 % or 9.4 % of
diet containing 42 % protein, respectively.

1. Introduction et al., 2011; Hung et al., 2015).

Asian red-tailed catfish (Hemibagrus wyckioides), a species of catfish
of the family Bagridae, distributes throughout much of the Mekong
River Basin including China, Laos, Vietnam, Cambodia, and Thailand
(Prasertwattana et al., 2005). This species is the largest bagrid catfish
with fast growth, large size, extensive adaptability, highly resistant to
disease and hypoxia (Ng, Rainboth, 1999). Additionally, no cannibalism
phenomenon was found in the breeding of this species unlike other
catfish (Jiwyam, Nithikulworawong, 2014). Thus, H. wyckioides is an
excellent species for intensive aquaculture (Ng, Rainboth, 1999). At
present, it is widely cultured in both pond and cage throughout the
Mekong River Basin (Prasertwattana et al., 2005). However, there are
few data on the nutritional requirements of this species so far (Deng
Lipid is regarded as one of the most important nutrients for fish,
which plays a very important role in providing essential fatty acids and
energy source, and a carrier of fat-soluble vitamins (Chang et al., 2017).
Additionally, extra lipid generally exerts the protein sparing action
through free fatty acids oxidation, and thereby can minimize the use of
high-priced protein sources and reduce the nitrogen emissions to the
environment (Guo et al., 2011). However, an excess dietary lipid not
only results in growth retardation but also causes abnormal fat deposi­
tion, which is detrimental to health and flesh quality of fish (Ahmad,
2008; Sivaramakrishnan et al., 2016). To date, there is no published
research on the optimal dietary lipid requirement for H. wyckioides.
Thus, the objective of the current research was to investigate the effects
of dietary lipid content on growth rate, feed utilization, digestive

* Corresponding authors at: Tongwei Co., Ltd., No. 588 Tianfu Road, Gaoxin District, Chengdu, 610093, China.
E-mail addresses: luzhangtw@163.com (L. Zhang), mihaifengtw@163.com (H. Mi).

https://doi.org/10.1016/j.aqrep.2021.100666
Received 1 December 2020; Received in revised form 23 January 2021; Accepted 7 March 2021
Available online 17 March 2021
2352-5134/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
J. Deng et al. Aquaculture Reports 20 (2021) 100666

enzyme activity, and antioxidant capacity of juvenile H. wyckioides, and maintained under natural photoperiod (13 L:11 D). Any uneaten feed
thereby to evaluate the optimal dietary lipid requirement. was collected 1 h after every feeding, and the dry matter content was
determined for both supplied and uneaten diets, and the data used for
2. Material and methods feed consumption calculation. Feed consumption was recorded by sub­
tracting the amount of uneaten diet from total amount of diet fed on a
2.1. Experimental diets dry matter basis.

Five isoproteic (crude protein 42 %) diets were prepared to contain 2.3. Sample collection
graded levels (3 %, 5.5 %, 8%, 10.5 %, and 13 %) of lipid (Table 1). The
dietary lipid sources were equally supplied by fish oil and soybean oil. At the end of the feeding trial, all fish were fasted for 24 h before
The diet preparation was conducted as previously described by Deng sampling. Total number and body weight of fish in each aquarium were
et al. (2011), and then was pelletized by a pellet feed maker (KS-180; measured to assess the growth rate, feed utilization and survival rate. All
Jiangsu Jingu Rice Mill Co., Ltd., Zhejiang, China) through a 1-mm die. experimental fish were anesthetized with eugenol (1:12000) (Shanghai
The wet pellets were dried in a convection air oven at 40 ◦ C for around Reagent Corporation, Shanghai, China) before sampling. Forty fish at
12 h and then were stored at − 20 ◦ C until used. the initiation of feeding trial and seven fish per aquarium at termination
were randomly collected and stored frozen (− 20 ◦ C) for proximate
composition analysis. Serum samples were collected from the caudal
2.2. Experimental procedure vein of five fish per tank with a sterile 1 mL syringe and withdrawn into
Eppendorf tubes without anticoagulant. Plasma samples were collected
Juvenile H. wyckioides obtained from the local farm were fed a from the caudal vein of five fish per tank with a heparinized syringe and
commercial feed (Beijing Bio-Tech Co., Ltd., Beijing, China) for 2 weeks transferred into a heparinized tube. Serum/plasma samples in Eppen­
to acclimatize the experimental environment. After the acclimation dorf tubes were allowed to clot for 4 h at 4 ◦ C. Following centrifugation
period, visually healthy fish (no signs and symptoms of disease) with (3000 × g for 10 min at 4 ◦ C), the serum/plasma was removed and
similar sizes (average weight 3.20 g) were randomly sorted into 15 frozen at − 80 ◦ C for the analyses of lipoprotein profile, protein meta­
aquaria (1.0 m × 0.6 m × 0.5 m) with 30 juveniles per aquarium. Fish bolism and antioxidant-related parameters. The homogenised liver and
were hand-fed to apparent satiation twice a day at 07:00 hr and 17:00 hr dorsal muscle from five fish were mixed separately for each aquarium
for 11 weeks. Water was recirculated through biological and mechanical and subjected to the determination of lipid profiles. Stomach, midgut
filters utilizing high-density polyester screens to remove particulate (the part from anterior valvula intestine to anterior rectum) and liver
material and provide the substrate for nitrifying bacteria. During the were dissected from five fish per aquarium and stored frozen (− 80 ◦ C)
feeding trial, the water temperature was maintained at 28 ± 1 ◦ C using a for subsequent determination of digestive enzyme activity. Five addi­
heating rod, all aquaria were provided with continuous aeration and tional livers per aquarium were dissected from the abdominal cavity of
fish, and frozen in liquid nitrogen and then stored at − 80 ◦ C for analyses
Table 1 of protein metabolism and antioxidant-related parameters.
Formulation and proximate composition (% dry weight) of experimental diets.
Dietary lipid level (%) 2.4. Chemical analysis
Ingredients
3 5.5 8 10.5 13
2.4.1. Proximate composition
Fish meala 30.00 30.00 30.00 30.00 30.00 Proximate composition of the ingredients, diets and whole-body
Soybean meala 22.00 22.00 22.00 22.00 22.00
Rapeseed meala 15.00 15.00 15.00 15.00 15.00
samples were determined by the standard AOAC methods (AOAC,
Wheat middlinga 15.00 15.00 15.00 15.00 15.00 2000): dry matter by dried to a constant weight at 105 ◦ C; crude protein
Fish oila 0.00 1.25 2.50 3.75 5.00 (N × 6.25) by the regular Kjeldahl method; crude lipid by the Soxhlet
Soybean oil 0.00 1.25 2.50 3.75 5.00 method with ether extraction; ash by incineration at 550 ◦ C for 16 h;
Microcrystalline celluloseb 10.00 7.50 5.00 2.50 0.00
gross energy in a bomb calorimeter.
Mineral premixc 0.50 0.50 0.50 0.50 0.50
Vitamin premixd 0.50 0.50 0.50 0.50 0.50
Otherse 7.00 7.00 7.00 7.00 7.00 2.4.2. Digestive enzyme activity
Proximate composition The tissues (stomach, midgut, and liver) preparation and digestive
Dry matter (DM, %) 89.00 88.23 88.94 88.78 89.42 enzymes (pepsin, EC 3.4.23.1; trypsin, EC 3.4.21.4; lipase, EC 3.1.1.3;
Crude protein (% DM) 42.56 42.21 42.01 42.46 42.31
Crude lipid (% DM) 3.04 5.50 7.99 10.60 13.22
amylase, EC 3.2.1.1; lactase, EC 3.2.1.108) analyses were performed
Ash (% DM) 9.88 10.07 9.89 9.58 9.93 according to the method described by Deng et al. (2010). One unit of
Energy (MJ/kg DM) 19.53 20.08 20.63 21.17 21.73 trypsin/pepsin activity was expressed as 1 mmol of tyrosine equivalent
a
Supplied by Kunming Tianyuan Feed Co., Ltd. (Yunnan, China); fish meal,
released per minute at 37 ◦ C. One unit of lipase activity was defined as
67.0 % crude protein, 11.5 % crude lipid; soybean meal, 48.6 % crude protein, the mmol of substrate hydrolysed per minute. One unit of amylase ac­
0.8 % crude lipid; rapeseed meal, 46.0 % crude protein, 2.6 % crude lipid; wheat tivity was defined as the amount of enzyme that hydrolyses 10.0 mg
middling, 13.6 % crude protein, 1.3 % crude lipid. starch per 30 min. One unit of lactase activity was defined as the amount
b
Supplied by Qufu Tianli Medical Supplements Co., Ltd. (Shandong, China). of enzyme that caused 0.1 unit increase in the optical density of reaction
c
Mineral premix (g/kg of mixture): MgSO47H2O, 180; KI, 1; FeSO4H2O, 260; mixture per minute. Specific enzyme activity was expressed as enzyme
• •

ZnSO4H2O, 180; CuSO45H2O, 25; Na2Se2O3, 0.01; MnSO4H2O, 180; CoCl26H2O, activity per gram protein. The soluble protein content was determined
• • • •

0.75. according to Bradford (1976) method.

d
Vitamin premix (g/kg of mixture): retinyl acetate (2800000 IU/g), 2 g;
cholecalciferol, 0.03 g; DL-α-tocopheryl acetate, 30 g; menadione, 3 g; thiamine
2.4.3. Lipid profiles in serum, liver, and muscle
hydrochloride, 8 g; riboflavin, 11 g; pyridoxine hydrochloride, 8 g; vitamin B12,
The serum triglyceride (TAG), total cholesterol (TC), and high-
0.02 g; ascorbic acid, 50 g; folic acid, 1 g; biotin 0.1 g; niacin, 30 g; calcium D-
pantothenate, 32 g; inositol, 25 g. density lipoprotein cholesterol (HDL-C) levels were determined
e
Others including α-starch, 4.65 %; soybean lecithin, 0.5 %; vitamin C (L- without extraction by using commercial kits (Nanjing Jiancheng
ascorbate-2- polyphosphate, 35 %), 0.02 %; calcium dihydrogen phosphate, 0.8 Bioengineering Institute, Nanjing, China). The serum low-density lipo­
%; sodium chloride, 0.22 %; ethoxyquin (30 %), 0.01 %; choline chloride (50 %), protein cholesterol (LDL-C) level and LDL-C/HDL-C ratio were estimated
0.3 %; chromic oxide, 0.5 %. according to the method of Friedewald et al. (1972). The TAG and TC

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J. Deng et al. Aquaculture Reports 20 (2021) 100666

contents in liver and muscle were measured using the same enzymatic where y is the whole-body moisture, protein, lipid or ash content (g), x is
kits used for serum, except these samples were extracted by the method the fish weight (g).
of Folch et al. (1957). The total lipid content in muscle was determined
gravimetrically (Folch et al., 1957). 3. Results

2.4.4. Protein metabolism-related parameters 3.1. Growth performance

The plasma total protein, albumin, and blood urea nitrogen (BUN)
contents, and plasma and hepatic aspartate aminotransferase (AST, EC
2.6.1.1) and alanine aminotransferase (ALT, EC 2.6.1.2) activities were
measured by using commercially available kits (Nanjing Jiancheng
Bioengineering Institute, Nanjing, China). The plasma insulin, insulin-
like growth factors-1 (IGF-1) and growth hormone (GH) contents, and
the plasma and hepatic adenosine monophosphate deaminase (AMPD,
EC 3.5.4.6) and glutamate dehydrogenase (GDH, EC 1.4.1.2) activities
were measured by the enzyme-linked immunosorbent assay (R&D Sys­
tems, Inc., Minneapolis, USA).
2.4.5. Antioxidant-related parameters
The plasma superoxide dismutase (SOD, EC 1.15.1.1), peroxidase
(POD, EC 1.11.1.7), catalase (CAT, EC 1.11.1.6), glutathione peroxidase
(GPx, EC 1.11.1.9), glutathione reductase (GR, EC 1.6.4.2), alkaline
phosphatase (AKP, EC 3.1.3.1) and total antioxidant capacity (TAC)
activities, and nitric oxide (NO) and malondialdehyde (MDA) contents
were measured using commercial kits (Nanjing Jiancheng Bioengi­
neering Institute, Nanjing, China). The hepatic antioxidant-related pa­
rameters were determined using the same kits in plasma and expressed
as enzyme activity/content per gram protein.
2.5. Statistical analysis
All data were analyzed using a one-way analysis of variance
(ANOVA), followed by Tukey’s multiple test. The difference was
considered significant at P < 0.05. The optimal dietary lipid requirement
was estimated using the daily gain coefficient (DGC) and feed conver­
sion ratio (FCR) data by the single-slope broken-line analysis (Robbins
et al., 2006). The SAS 9.0 for Windows (SAS Institute Inc., Cary, North
Carolina, USA) was employed to perform the statistical analysis. In order
to eliminate fish weight specific influences on whole-body proximate
composition, allometric analysis was performed using the following
equation (Shearer, 1994):
log y = a + b log x
After 11 weeks of the feeding period, all fish appeared to be healthy
and active. There was no significant difference in the feed intake among
the dietary treatments (P > 0.05) (Table 2). Weight gain (WG), DGC and
protein efficiency ratio (PER) gradually improved with the dietary lipid
content up to 10.5 % and then reached a plateau. Conversely, FCR
steadily decreased with the dietary lipid content up to 10.5 % and
reached a plateau. The protein retention generally enhanced with the
dietary lipid content up to 13 %. However, the lipid retention linearly
decreased with increasing dietary lipid content, but no significant dif­
ference was observed among fish fed diets with 8 %, 10.5 %, and 13 %
lipid. The single-slope broken-line regression analysis showed that the
optimal dietary lipid content for supporting best DGC and FCR were 11.1
% (y = 2.140 – 0.0220 × [11.113 − x]; R2 = 0.972, P < 0.001; Fig. 1)
and 9.4 % (y = 0.893 – 0.0215 × [9.407 − x]; R2 = 0.941, P < 0.001;
Fig. 2) for juvenile H. wyckioides, respectively.
3.2. Digestive enzyme activity
The pepsin and midgut trypsin activities generally depressed with
increasing dietary lipid content; the pepsin activity in fish fed diets with
3 % and 8 % lipid was significantly higher than that in fish fed diet with
13 % lipid (P < 0.05), the midgut trypsin activity in fish fed diet with 3 %
lipid was significantly higher than that in fish fed diets with 10.5 % and
13 % lipid (Table 3). Conversely, the highest midgut lipase activity was
observed in fish fed diet with 13 % lipid, the midgut lactase activity in
fish fed diets with 8 %, 10.5 %, and 13 % lipid was significantly higher
than that in fish fed diets with 3 % and 5.5 % lipid. However, there was
no significant difference in the midgut amylase activity among the di­
etary treatments.
The hepatic trypsin activity in fish fed diet with 3 % lipid was
significantly higher than that in fish fed the other diets. Conversely, the
hepatic lipase activity in fish fed diets with 3 % and 5.5 % lipid was
significantly lower than that in fish fed diets with 10.5 % and 13 % lipid.
However, there were no significant differences in the hepatic amylase
and lactase activities among the dietary treatments.

Table 2
Growth performance of Hemibagrus wyckioides fed diets with different lipid level.
Dietary lipid level (%)

3 5.5 8 10.5 13

Initial weight (g) 3.14 ± 0.05 3.22 ± 0.02 3.21 ± 0.01 3.20 ± 0.01 3.22 ± 0.01
Final weight (g) 25.69 ± 0.61a 27.38 ± 0.48a,b 27.79 ± 0.36a,b 29.80 ± 0.37b 29.86 ± 0.69b
Feed intakeb (g/kg MBWa per day) 7.88 ± 0.12 7.80 ± 0.31 7.32 ± 0.17 7.33 ± 0.21 7.33 ± 0.27
Weight gainc 7.17 ± 0.06a 7.50 ± 0.13a,b 7.67 ± 0.12a,b 8.31 ± 0.12b 8.29 ± 0.22b
Daily gain coefficientd (%/day) 1.96 ± 0.02a 2.02 ± 0.02a,b 2.05 ± 0.02a,b 2.14 ± 0.02b 2.14 ± 0.03b
Feed conversion ratee 1.03 ± 0.03b 1.00 ± 0.03a,b 0.93 ± 0.02a,b 0.90 ± 0.01a 0.90 ± 0.03a
Protein efficiency ratiof 2.29 ± 0.06a 2.35 ± 0.03a,b 2.58 ± 0.04a,b 2.64 ± 0.01b 2.66 ± 0.06b
Protein retentiong (%) 36.37 ± 0.35a 41.06 ± 0.66a,b 41.69 ± 1.37a,b 41.53 ± 1.35a,b 43.88 ± 1.11b
Lipid retentionh (%) 257.14 ± 5.71c 187.89 ± 5.59b 126.48 ± 5.94a 108.30 ± 6.84a 97.64 ± 7.60a
Survival ratei (%) 100 100 100 100 100

Values are presented as means ± SE, n = 3. Means in the same row with different superscripts are significantly different from each other (P < 0.05).
a
MBW: mean metabolic body weight = ((initial body weight/1000)0.75 + (final body weight/1000)0.75)/2.
b
Feed intake: feed consumption/(MBW × feeding days).
c
Weight gain: (final body weight – initial body weight)/initial body weight.
d
Daily gain coefficient: 100 × (final body weight1/3 – initial body weight1/3)/feeding days.
e
Feed conversion ratio: weight gain (g)/dry feed fed (g).
f
Protein efficiency ratio: weight gain (g)/protein fed (g).
g
Protein retention: 100 × (protein gain (g)/protein intake (g)).
h
Lipid retention: 100 × (lipid gain (g)/lipid intake (g)).
i
Survival rate: 100 × (final number of fish/initial number of fish).

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J. Deng et al. Aquaculture Reports 20 (2021) 100666

Fig. 1. Lipid requirement for juvenile Hemibagrus wyckioides calculated by single-slope broken-line regression analysis of daily gain coefficient (%/day) against
dietary lipid level (%).

Fig. 2. Lipid requirement for juvenile Hemibagrus wyckioides calculated by broken-line regression analysis of feed conversion rate against dietary lipid level (%).

3.3. Lipid profile in serum, liver, and muscle
The serum TAG level in fish fed diet with 10.5 % lipid was signifi­
cantly higher than that in fish fed diets with 3 %, 5.5 %, and 8 % lipid
(Table 4). However, there were no significant differences in the serum
TC, HDL-C and LDL-C levels and LDL-C/HDL-C ratio among the dietary
treatments.
The hepatic TAG and TC contents linearly increased with increasing
dietary lipid content, and those were higher in fish fed diets with 10.5 %
and 13 % lipid as compared to fish fed diets with 3 % and 5.5 % lipid.
The TAG content in muscle steadily increased with the dietary lipid
content up to 10.5 %, and then slightly decreased. However, there were
no significant differences in the muscle total fat and TC contents among
the dietary treatments.
3.4. Protein metabolism-related parameters
The plasma insulin level in fish fed diet with 3 % lipid was signifi­
cantly higher than that in fish fed the other diets (Table 5). Conversely,
the plasma IGF-1 level in fish fed diet with 3 % lipid was significantly

Table 3
Digestive enzyme activity in the gastrointestinal tract and liver of Hemibagrus wyckioides fed diets with different lipid level.
Dietary lipid level (%)

3 5.5 8 10.5 13

Stomach
Pepsin (U/mg protein) 3.48 ± 0.15c 1.69 ± 0.22ab 2.46 ± 0.15bc 1.53 ± 0.23ab 1.11 ± 0.31a
Midgut
Trypsin (U/μg protein) 0.17 ± 0.02b 0.15 ± 0.02ab 0.14 ± 0.01ab 0.10 ± 0.01a 0.11 ± 0.01a
Lipase (U/g protein) 24.68 ± 2.57a 23.67 ± 1.96a 18.76 ± 1.27a 23.09 ± 2.81a 39.33 ± 0.82b
Amylase (U/mg protein) 0.35 ± 0.02 0.33 ± 0.04 0.43 ± 0.03 0.33 ± 0.02 0.31 ± 0.03
Lactase (U/mg protein) 11.99 ± 0.28a 11.79 ± 1.36a 22.73 ± 1.04b 22.27 ± 0.66b 21.34 ± 1.49b
Liver
Trypsin (U/mg protein) 125.60 ± 1.49b 53.97 ± 8.23a 40.88 ± 2.46a 33.93 ± 2.89a 51.71 ± 6.91a
Lipase (U/g protein) 17.58 ± 1.86a 18.93 ± 4.78a 24.52 ± 1.89ab 36.06 ± 2.48b 30.80 ± 1.42b
Amylase (U/mg protein) 0.24 ± 0.05 0.23 ± 0.09 0.18 ± 0.05 0.16 ± 0.07 0.16 ± 0.06
Lactase (U/mg protein) 22.69 ± 2.99 30.54 ± 2.02 24.45 ± 5.94 26.06 ± 2.40 19.85 ± 1.80

Values are presented as means ± SE, n = 3. Means in the same row with different superscripts are significantly different from each other (P < 0.05).

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J. Deng et al. Aquaculture Reports 20 (2021) 100666

Table 4
Lipid profiles in the serum, liver and muscle of Hemibagrus wyckioides fed diets with different lipid level.
Dietary lipid level (%)

3 5.5 8 10.5 13

Serum (mmol/L)
Triglyceride 7.95 ± 0.29a 8.56 ± 0.61a 8.04 ± 0.62a 11.25 ± 0.51b 9.79 ± 0.38ab
Total cholesterol 6.64 ± 0.59 6.85 ± 0.51 7.20 ± 0.80 7.25 ± 0.50 7.29 ± 0.24
HDL-C 1.38 ± 0.20 1.57 ± 0.13 1.36 ± 0.20 1.30 ± 0.06 1.65 ± 0.15
LDL-C 3.67 ± 0.46 3.56 ± 0.50 4.23 ± 0.69 3.70 ± 0.42 3.68 ± 0.11
LDL-C/HDL-C 2.71 ± 0.33 2.25 ± 0.14 3.12 ± 0.25 2.86 ± 0.32 2.26 ± 0.17
Liver (mg/g wet liver)
Triglyceride 0.70 ± 0.18a 1.03 ± 0.15a 1.35 ± 0.17ab 1.88 ± 0.19b 1.96 ± 0.05b
Cholesterol 0.76 ± 0.03a 0.70 ± 0.04a 0.83 ± 0.04ab 1.06 ± 0.10bc 1.12 ± 0.08c
Muscle (mg/g wet liver)
Total fat 14.24 ± 1.96 14.31 ± 0.42 16.96 ± 1.87 15.28 ± 1.80 15.45 ± 1.59
Triglyceride 0.16 ± 0.02a 0.23 ± 0.01ab 0.29 ± 0.02b 0.35 ± 0.04b 0.24 ± 0.02ab
Cholesterol 0.17 ± 0.02 0.20 ± 0.02 0.16 ± 0.01 0.18 ± 0.01 0.22 ± 0.03

Values are presented as means ± SE, n = 3. Means in the same row with different superscripts are significantly different from each other (P < 0.05).
HDL-C = high-density lipoprotein cholesterol; LDL-C = low-density lipoprotein cholesterol.

Table 5
Protein metabolism-related paramters in plasma and liver of Hemibagrus wyckioides fed diets with different lipid level.
Dietary lipid level (%)

3 5.5 8 10.5 13

Plasma
Total protein (g/L) 27.51 ± 0.55 26.64 ± 0.66 26.25 ± 1.75 28.45 ± 0.97 26.85 ± 1.92
Albumin (g/L) 12.36 ± 1.22 12.21 ± 1.13 13.29 ± 0.76 12.05 ± 0.23 11.89 ± 0.62
Blood urea nitrogen (mmol/L) 14.29 ± 0.54 12.55 ± 1.26 12.52 ± 1.33 13.51 ± 1.96 12.55 ± 0.90
Insulin (mU/L) 7.48 ± 1.18b 0.91 ± 0.23a 1.40 ± 0.26a 1.43 ± 0.32a 2.44 ± 0.75a
Insulin-like growth factor 1 (μg/L) 5.34 ± 0.16a 7.24 ± 0.45ab 10.64 ± 1.58b 10.11 ± 1.03b 10.98 ± 1.08b
Growth hormone (μg/L) 13.02 ± 2.58 7.88 ± 1.42 8.13 ± 1.29 15.20 ± 1.92 8.27 ± 1.06
Amino methyl propanediol (ng/L) 10.86 ± 0.63b 8.20 ± 0.46ab 7.95 ± 1.10ab 7.64 ± 0.40ab 7.04 ± 0.24a
Glutamate dehydrogenase (U/mL) 2.06 ± 0.05 2.55 ± 0.34 2.49 ± 0.20 2.86 ± 0.34 2.60 ± 0.19
Aspartate aminotransferase (U/L) 33.99 ± 2.46bc 36.70 ± 1.40c 24.47 ± 2.41ab 26.48 ± 2.38abc 16.54 ± 3.39a
Alanine aminotransferase (U/L) 10.60 ± 0.54c 8.19 ± 1.21bc 7.39 ± 0.87abc 6.79 ± 0.39ab 4.06 ± 0.51a
Liver
Amino methyl propanediol (ng/g protein) 3.08 ± 0.18ab 3.47 ± 0.09b 3.19 ± 0.20ab 2.48 ± 0.07a 2.96 ± 0.22ab
Glutamate dehydrogenase (U/g protein) 3.62 ± 0.03 3.32 ± 0.19 3.75 ± 0.29 3.74 ± 0.29 3.74 ± 0.15
Aspartate aminotransferase (U/g protein) 22.13 ± 0.52b 14.09 ± 0.52a 14.02 ± 0.31a 14.54 ± 2.22a 25.91 ± 0.81b
Alanine aminotransferase (U/g protein) 24.49 ± 1.98 27.10 ± 1.34 21.99 ± 2.63 22.45 ± 3.19 20.94 ± 1.73

Values are presented as means ± SE, n = 3. Means in the same row with different superscripts are significantly different from each other (P < 0.05).

lower than that in fish fed diets with 8 %, 10.5 %, and 13 % lipid.
However, there were no significant differences in the plasma total pro­
tein, albumin, BUN and GH levels, and GDH activity among the dietary
treatments. The plasma AMPD, AST and ALT activities generally
decreased with increasing dietary lipid content; the plasma AMPD ac­
tivity in fish fed diet with 3 % lipid was significantly higher than that in
fish fed diet with 13 % lipid, the plasma AST and ALT activities in fish
fed diets with 3 % and 5.5 % lipid were significantly higher than those in
fish fed diet with 13 % lipid.
The lowest hepatic AMPD activity was observed in fish fed diet with
10.5 % lipid (Table 5). The hepatic AST activity in fish fed diets with 5.5
%, 8 %, and 10.5 % lipid was significantly lower than that in fish fed
diets with 3 % and 13 % lipid. However, there were no significant dif­
ferences in the hepatic GDH and ALT activities among the dietary
treatments.
higher than that in fish fed diet with 13 % lipid. However, the plasma
AKP activity generally depressed with increasing dietary lipid level.
There were no significant differences in the hepatic SOD and TAC
activities among the dietary treatments (Table 6). The hepatic POD, CAT
and GPx activities gradually increased with the dietary lipid content up
to 10.5 %, and then thereafter decreased. Similarly, the hepatic GR ac­
tivity improved with the dietary lipid content up to 5.5 %, but thereafter
declined. The hepatic AKP activity in fish fed diet with 10.5 % lipid was
significantly higher than that in fish fed the other diets. The hepatic NO
content in fish fed diets with 8 % and 10.5 % lipid was significantly
higher than that in fish fed the other diets. Conversely, the hepatic MDA
content in fish fed diet with 13 % lipid was significantly higher than that
in fish fed the other diets.
3.6. Whole-body composition

3.5. Antioxidant-related parameters
There were no significant differences in the plasma SOD, CAT and
GPx activities, NO and MDA contents among the dietary treatments
(Table 6). The plasma POD activity in fish fed diet with 13 % lipid was
significantly lower than that in fish fed the other diets. The plasma GR
activity in fish fed diet with 8 % lipid was significantly higher than that
in fish fed diets with 5.5 % and 13 % lipid. Simiarly, the plasma TAC
activity in fish fed diets with 8 % and 10.5 % lipid was significantly
The whole-body lipid content linearly raised with increasing dietary
lipid content, whereas the opposite trend was observed in the whole-
body moisture content. However, there were no significant differences
in the whole-body protein and ash contents (Table 7). Allometric anal­
ysis of the whole-body components of fish versus fish weight showed
that fish weight was increasing faster than the whole-body moisture (the
content was decreasing) (b = 0.669 < 1, Fig. 3a), the whole-body pro­
tein (b = 1.134 > 1, Fig. 3b) and lipid (b = 3.017 > 1, Fig. 3c) contents
were making up an increasing portion of fish weight, the whole-body ash

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J. Deng et al. Aquaculture Reports 20 (2021) 100666

Table 6
Antioxidant capacity parameters in plasma and liver of Hemibagrus wyckioides fed diets with different lipid level.
Dietary lipid level (%)

3 5.5 8 10.5 13

Plasma
Superoxide dismutase (U/mL) 15.79 ± 0.47 15.52 ± 1.32 16.57 ± 2.47 16.57 ± 2.67 14.59 ± 0.64
Peroxidase (U/mL) 21.11 ± 1.72b 25.85 ± 4.61b 25.21 ± 2.14b 20.96 ± 0.99b 8.90 ± 0.83a
Catalase (U/mL) 26.42 ± 1.48 27.25 ± 2.48 20.10 ± 1.50 22.70 ± 2.80 25.82 ± 0.33
Glutathione peroxidase (U/μL) 0.62 ± 0.28 0.98 ± 0.32 0.34 ± 0.19 1.27 ± 0.11 0.37 ± 0.15
Glutathione reductase (U/L) 21.97 ± 1.93ab 21.26 ± 1.46a 32.15 ± 3.72b 26.80 ± 2.14ab 20.36 ± 1.07a
Total antioxidant capacity (U/mL) 6.66 ± 0.23ab 6.62 ± 0.04ab 8.30 ± 0.22b 7.32 ± 0.72b 5.18 ± 0.57a
Alkaline phosphatase (U/dL) 3.98 ± 0.34c 3.33 ± 0.21bc 2.48 ± 0.18b 2.89 ± 0.36bc 0.75 ± 0.07a
Nitric oxide (μmol/L) 0.21 ± 0.01 0.22 ± 0.02 0.24 ± 0.01 0.24 ± 0.02 0.23 ± 0.01
Malondialdehyde (nmol/mL) 12.95 ± 1.11 14.41 ± 1.37 11.26 ± 0.49 15.99 ± 2.00 14.64 ± 2.29
Liver
Superoxide dismutase (U/mg protein) 3.16 ± 0.21 3.73 ± 0.39 3.75 ± 0.27 3.83 ± 0.31 2.93 ± 0.54
Peroxidase (U/mg protein) 4.90 ± 0.50a 5.93 ± 0.54ab 6.33 ± 0.21ab 7.03 ± 0.43b 4.54 ± 0.18a
Catalase (U/mg protein) 14.18 ± 1.22ab 16.00 ± 0.50ab 18.64 ± 0.86ab 18.94 ± 1.86b 11.98 ± 0.69a
Glutathione peroxidase (U/μg protein) 0.22 ± 0.03ab 0.17 ± 0.01ab 0.35 ± 0.07ab 0.37 ± 0.07b 0.15 ± 0.01a
Glutathione reductase (U/g protein) 20.77 ± 1.32bc 27.15 ± 2.56c 15.77 ± 2.83ab 11.62 ± 0.53a 10.01 ± 1.50a
Total antioxidant capacity (U/mg protein) 0.91 ± 0.09 0.91 ± 0.03 1.27 ± 0.13 0.95 ± 0.04 1.01 ± 0.11
Alkaline phosphatase (U/g protein) 3.28 ± 0.38a 2.91 ± 0.19a 3.05 ± 0.27a 5.40 ± 0.26b 2.97 ± 0.13a
Nitric oxide (μmol/g protein) 2.04 ± 0.02a 1.72 ± 0.23a 3.83 ± 0.45b 4.82 ± 0.25b 1.62 ± 0.43a
Malondialdehyde (μmol/g protein) 0.32 ± 0.04a 0.11 ± 0.01a 0.26 ± 0.01a 0.25 ± 0.08a 0.65 ± 0.12b

Values are presented as means ± SE, n = 3. Means in the same row with different superscripts are significantly different from each other (P < 0.05).

content was homeostatically controlled (b ≈ 1, Fig. 3d).
4. Discussion
An appropriate dietary lipid level is crucial to maintain normal
growth and health of fish (Yi et al., 2014; Li et al., 2015). In this study,
the growth rate and feed utilization improved with the dietary lipid
content up to an optimal level (10.5 %) and then reached a plateau. The
similar growth responses to dietary lipid content were reported in large
yellow croaker (Larimichthys croceus) (Yi et al., 2014), orange-spotted
grouper (Epinephelus coioides) (Li et al., 2015), chu’s croaker (Nibea
coibor) (Huang et al., 2016), and yellow drum (Nibea albiflora) (Wang
et al., 2016). The single-slope broken-line regression analysis showed
that the optimal lipid requirement of juvenile H. wyckioides for sup­
porting best DGC or FCR was 9.4 % or 11.1 % of diet, respectively. This
value (9.4–11.1 %) was similar to that of some other catfish species
including Asian catfish (Pangasius hypophthalmus) (9.0 %; Liu et al.,
2011), channel catfish (Ictalurus punctatus) (10.0 %; Gatlin, Stickney,
1982), striped catfish (Pangasianodon hypophthalmus) (10.1 %; Sivar­
amakrishnan et al., 2016), yellow catfish (Pelteobagrus fulvidraco) (11.3
%; Han et al., 2005), and African catfish (Clarias gariepinus) (12.0 %;
Ahmad, 2008). However, it was lower than that observed in Chinese
longsnout catfish (Leiocassis longirostris) (14.3 %; Pei et al., 2004), South
American catfish (Pseudoplatystoma sp.) (16.0 %; Arslan et al., 2012), Far
Eastern catfish (Silurus asotus) (17.0 %; Kim et al., 2012), and bagrid
catfish (Pseudobagrus fulvidraco) (19.0 %; Kim, Lee, 2005), but higher
than that for Ussuri catfish (Pseudobagrus ussuriensis) (5.0 %; Wang et al.,
2012), butter catfish (Ompok pabda) (6.5 %; Paul et al., 2011), walking
catfish (Clarias batrachus) (7.0 %; Anwar, Jafri, 1995), and freshwater
catfish (Mystus montanus) (7.0 %; Raj et al., 2007). The apparent
discrepancy in the dietary lipid requirement is perhaps due to fish
species, fish life stage, water temperature, and dietary protein content
(NRC, 2011). Additionally, previous studies on the energy requirement
of aquatic animals exhibited a relationship between the capacity for
lipid utilization and feeding habits (Mai et al., 1995). Generally,
carnivorous catfish (P. fulvidraco, S. asotus, L. longirostris, and Pseudo­
platystoma sp.) have higher dietary lipid requirements than omnivorous
catfish (O. pabda, C. batrachus, C. gariepinus, and M. montanus).
The digestion and utilization of nutrient largely depend on digestive
enzymes activities in the gastrointestinal tract of fish. Previous studies
have demonstrated that the increased dietary lipid may inhibit the
protease activity in fish (Luo et al., 2010; Li et al., 2015; Trenzado et al.,
2018). Similar result was found in this study, H. wyckioides fed diets with
high lipid content showed an inhibition of proteolytic (pepsin and
trypsin) activities. As is well-known, lipase is produced in response to
the presence of triglycerides in the gut lumen (Zambonino-Infante,
Cahu, 1999). The present study showed that the hepatic lipase activity
positively related to the dietary lipid content, while the amylase activity
did not change. The increased hepatic lipase activity with raising dietary
lipid content has also been observed in Japanese seabass (Lateolabrax
japonicus) (Luo et al., 2010), darkbarbel catfish (Pelteobagrus vachelli)
(Zheng et al., 2010), turbot (Scophthalmus maximus) (Zhang et al., 2015)
and scaleless carp (Gymnocypris przewalskii) (Meng et al., 2017), which
may ascribed to the positive-feedback regulation by dietary lipid. The
hepatopancreatic secretion of digestive enzymes is mainly mediated by
the intestinal hormone cholecystokinin (CCK), which is stimulated
through a CCK-releasing factor by ingesting fat (Qiang et al., 2016). The
existence of such a hormonal mechanism was suggested in European
seabass (Silurus glanis) (Zambonino-Infante, Cahu, 1999) and red drum
(Sciaenops ocellatus) (Buchet et al., 2000) fed diets with increasing lipid
levels.
It is well established that protein utilization can be improved by the

Table 7
Proximate composition (% wet weight) of the whole body of Hemibagrus wyckioides fed diets with different lipid level.
Dietary lipid level (%)

3 5.5 8 10.5 13

Moisture 73.42 ± 0.30b 72.56 ± 0.10b 71.68 ± 0.45ab 70.44 ± 0.58a 69.89 ± 0.59a
Crude protein 15.75 ± 0.14 16.05 ± 0.14 16.32 ± 0.17 16.10 ± 0.07 16.38 ± 0.24
Crude lipid 7.64 ± 0.09a 8.46 ± 0.06ab 9.14 ± 0.26bc 10.09 ± 0.33cd 10.92 ± 0.44d
Ash 3.24 ± 0.09 3.17 ± 0.07 3.37 ± 0.02 3.35 ± 0.04 3.16 ± 0.04

Values are presented as means ± SE, n = 3. Means in the same row with different superscripts are significantly different from each other (P < 0.05).

6
J. Deng et al.
Fig. 3. Allometric analysis (a) log body moisture versus log fish weight, (b) log body protein versus log fish weight, (c) log body lipid versus log fish weight, (d) log
body ash versus log fish weight, of Hemibagrus wyckioides fed diets with different lipid levels.
increased dietary lipid due to the protein-sparing effect in many fish
species (NRC, 2011). Similarly, the increased PER and protein retention
of H. wyckioides caused by dietary lipid have been found in this study.
Additionally, the allometric analysis of whole-body protein content
versus fish weight showed that the whole-body protein content was
making up an increasing portion of the fish weight (b = 1.1342 > 1,
Fig. 3a), indicating that protein deposition improved with the increased
dietary lipid content. An imbalance resulting from modulation of either
protein synthesis or protein degradation is the cause of protein reten­
tion. Protein synthesis is primarily regulated by the insulin/IGF-1 and
mammalian target of rapamycin (mTOR) signaling pathway, while
protein degradation is largely controlled by the ubiquitin-proteasome
pathway (Zhang et al., 2019). IGF-1 is a mitogenic polypeptide that
stimulates protein synthesis by activating TOR signaling pathway. In
this study, the plasma IGF-1 level increased with the dietary lipid con­
tent up to 8 % and thereafter reached a plateau, indicating that the di­
etary lipid content of 8–13 % might support the protein synthesis of
juvenile H. wyckioides in captivity. AMPD can catalyze the irreversible
hydrolytic cleavage of AMP to IMP and NH+ 4 . Therefore, AMPD has been
identified as one of three main sources of ammonia production (Walton,
Cowey, 1977). Besides, aminotransferases (ALT, AST) catabolize amino
acids and transfer amino groups to α-keto acids (Kumar et al., 2017).
Thus, AMPD, AST and ALT generally be considered as biomarkers for
protein utilization and/or ammonia excretion. In this study, the plasma
AMPD, AST and ALT activities depressed with the dietary lipid content
up to 13 %, and the hepatic AMPD activity decreased with the dietary
lipid content up to 10.5 %. These results indicated that the dietary lipid
content of 10.5–13 % will contribute to promote protein synthesis and
inhibit protein degradation, and thereby enhance protein retention of
H. wyckioides.
Triglycerides are the most common type of fat that can be used later
by the body for energy (Tocher, 2003). In this study, the TAG level in
serum, liver and muscle generally enhanced with the dietary lipid con­
tent up to 10.5 %. Similar observations were reported in grass carp
7
Aquaculture Reports 20 (2021) 100666
(Ctenopharyngodon Idella) (Du et al., 2005; Jin et al., 2013), hybrid
sturgeon (Acipenser baerii ♀ × A. gueldenstaedtii ♂) (Guo et al., 2011),
N. coibor (Huang et al., 2016), silver barb (Puntius gonionotous) (Nayak
et al., 2018), and largemouth bass (Micropterus salmoides) (Guo et al.,
2019), indicating a more active endogenous lipid transport in response
to the higher dietary lipid level. Further, serum components such as TC,
TAG, LDL-C and HDL-C play an important role in body health, so the
dynamic balance of these substances is very important to health of the
organisms. The elevated blood TC and LDL-C levels and LDL-C/HDL-C
ratio are measured as the index of risk for arteriosclerosis lesion and
liver damage (Chrostek et al., 2013; Deng et al., 2015). In this study, no
differences were observed in the serum TC, HDL-C and LDL-C levels and
LDL-C/HDL-C ratio. These results indicated that dietary lipid content up
to 10.5 % was conducive to energy storage, meanwhile high dietary lipid
content would not be detrimental to liver function and serum lipid
profile in juvenile H. wyckioides.
The antioxidant capacity includes enzymatic and non-enzymatic
antioxidant activities. Antioxidant enzymes include SOD, CAT, POD,
GPx and GR that constitute the first line of the enzymatic defense
mechanism against free radicals in organisms. MDA is the end-product
of lipid peroxidation, which causes toxic stress in cells and is used as a
biomarker to measure the level of oxidative stress (Deng et al., 2015).
Previous studies showed that the suitable dietary lipid level was
conducive to improve the antioxidant capacity of fish, but an excessive
amount of dietary lipid resulted in the depression of antioxidant ca­
pacity (Qiang et al., 2016; Meng et al., 2017; Gou et al., 2019). Similar
results were observed in this study, the hepatic CAT, GPx, AKP and POD
activities generally increased with the increase of dietary lipid level
from 3 % to 10.5 % and then decreased thereafter. Further, dietary lipid
level of 13 % led to lower plasma POD, GR, AKP and TAC activities and
higher hepatic MDA content. These results suggested that the dietary
lipid level up to 10.5 % effectively enhanced the antioxidant capacity by
depressing lipid peroxidation and raising the resistance to oxidative
stress in juvenile H. wyckioides, but which may be restrained by higher
J. Deng et al.
dietary lipid.
The increase in dietary lipid level usually resulted in the total carcass
fat deposition in fish (Anwar, Jafri, 1995; Pei et al., 2004; Sivar­
amakrishnan et al., 2016). Similar result was observed in this study, the
whole-body lipid content increased with increasing dietary lipid level.
Further, the allometric analysis of the body component versus fish
weight showed that the body lipid content was making up an increasing
portion of fish weight (b = 3.017 > 1, Fig. 3c), indicating that dietary
lipid level may influence the carcass fat content of H. wyckioides. This is
supported by the allometric analysis of body composition data as
explained by Shearer (1994) and applied by Deng et al. (2015). Whether
the dietary lipid level was the sole reason for the variations in
whole-body composition needs further study because the crude lipid
content in this study was increased at the expense of microcrystalline
cellulose. Therefore, the body compositions of H. wyckioides may be
related to endogenous factors such as fish size as well as exogenous
factors such as diet composition (e.g. dietary lipid level) in this study.
5. Conclusion
In conclusion, the present results showed that the optimum lipid
content was 9.4–11.1 % of diet containing 42 % protein based on the
single-slope broken-line regression analysis of DGC and FCR in
H. wyckioides. The suitable dietary lipid level (10.5 %) enhanced the
protein retention by promoting protein synthesis and inhibiting protein
degradation, and improved the antioxidant capacity by depressing lipid
peroxidation and increasing the resistance to oxidative stress in
H. wyckioides. The allometric analysis indicated that the body lipid
content of H. wyckioides may be related to endogenous factor (e.g. fish
size) as well as exogenous factor (e.g. dietary lipid content). Future re­
searches are still needed to determine the optimum protein/energy ratio
in diets for this species.
Ethical approval
The study was performed by the Regulations for the Administration
of Affairs Concerning Experimental Animals approved by the State
Council of the People’s Republic of China on October 31, 1988 (amen­
ded on January 8, 2011, July 18, 2013, and March 1, 2017,
respectively).
CRediT authorship contribution statement
Junming Deng: Conceptualization, Data curation, Formal analysis,
Investigation, Methodology, Project administration, Validation, Visual­
ization, Writing - original draft, Writing - review & editing. Xindang
Zhang: Visualization, Investigation, Formal analysis. Yan Sun: Visual­
ization, Investigation, Formal analysis. Lu Zhang: Conceptualization,
Funding acquisition, Project administration, Resources, Supervision,
Writing - review & editing. Haifeng Mi: Conceptualization, Funding
acquisition, Project administration, Resources, Supervision, Writing -
review & editing.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
This work was financially supported by the National Key R&D Pro­
gram of China (2018YFD0900400); National Natural Science Founda­
tion of China (31760761); Natural Science Foundation of Yunnan
Province (2018FA018); and Foundation of Tongwei Co., Ltd.
(TA2019A003).
8
Aquaculture Reports 20 (2021) 100666
References
Ahmad, M.H., 2008. Response of African catfish, Clarias gariepinus, to different dietary
protein and lipid levels in practical diets. J. World Aquac. Soc. 39, 541–548.
Anwar, M.F., Jafri, A.K., 1995. Effect of dietary lipid levels on growth, feed conversion,
and muscle composition of the walking catfish, Clarias batrachus. J. Appl. Aquac. 5,
61–71.
AOAC, 2000. Official Methods of AOAC International. Association of Official Analytical
Chemists, 17th ed. AOAC international, Gaithersburg, MD.
Arslan, M., Dabrowski, K., Ferrer, S., Dietrich, M., Rodriguez, G., 2012. Growth, body
chemical composition and trypsin activity of South American catfish, surubim
(Pseudoplatystoma sp.) juveniles fed different dietary protein and lipid levels. Aquac.
Res. 44, 760–771.
Bradford, M., 1976. A rapid and sensitive method for the quantitation of microgram
quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.
72, 248–254.
Buchet, V., Zambonino-Infante, J., Cahu, C., 2000. Effect of lipid level in a compound
diet on the development of red drum (Sciaenops ocellatus) larvae. Aquaculture 184,
339–347.
Chang, J., Niu, H.X., Jia, Y.D., Li, S.G., Xu, G.F., 2017. Effects of dietary lipid levels on
growth, feed utilization, digestive tract enzyme activity and lipid deposition of
juvenile Manchurian trout, Brachymystax lenok (Pallas). Aquac. Nutr. 24, 694–701.
Chrostek, L., Supronowicz, L., Panasiuk, A., Cylwik, B., Gruszewska, E., Flisiak, R., 2013.
The effect of the severity of liver cirrhosis on the level of lipids and lipoproteins.
Clin. Exp. Med. 14, 417–421.
Deng, J.M., Mai, K.S., Ai, Q.H., Zhang, W.B., Tan, B.P., Xu, W., Liufu, Z.G., 2010.
Alternative protein sources in diets for Japanese flounder (Paralichthys olivaceus): II.
Effects on nutrient digestibility and digestive enzyme activity. Aquac. Res. 41,
861–870.
Deng, J., Mai, K., Chen, L., Mi, H., Zhang, L., 2015. Effects of replacing soybean meal
with rubber seed meal on growth, antioxidant capacity, non-specific immune
response, and resistance to Aeromonas hydrophila in tilapia (Oreochromis niloticus ×
O. aureus). Fish Shellfish Immun. 44, 436–444.
Deng, J., Zhang, X., Bi, B., Kong, L., Kang, B., 2011. Dietary protein requirement of
juvenile Asian red-tailed catfish Hemibagrus wyckioides. Anim. Feed Sci. Tech. 170,
231–238.
Du, Z.Y., Liu, Y.J., Tian, L.X., Wang, J.T., Wang, Y., Liang, G.Y., 2005. Effect of dietary
lipid level on growth, feed utilization and body composition by juvenile grass carp
(Ctenopharyngodon idella). Aquac. Nutr. 11, 139–146.
Folch, J., Lees, M., Sloane-Stanley, G.H., 1957. A simple method for the isolation and
purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509.
Friedewald, W.T., Levy, R.I., Fredrickson, D.S., 1972. Estimation of the concentration of
low-density lipoprotein cholesterol in plasma, without use of the preparative
ultracentrifuge. Clin. Chem. 18, 499–502.
Gatlin I.I.I., D.M., Stickney, R.R., 1982. Fall-winter growth of young channel catfish in
response to quantity and source of dietary lipid. T. Am. Fish. Soc. 111, 90–93.
Gou, N., Chang, Z., Deng, W., Ji, H., Zhou, J., 2019. Effects of dietary lipid levels on
growth, fatty acid composition, antioxidant status and lipid metabolism in juvenile
Onychostoma macrolepis. Aquac. Res. 50, 3369–3381.
Guo, J., Zhou, Y., Zhao, H., Chen, W.Y., Chen, Y.J., Lin, S.M., 2019. Effect of dietary lipid
level on growth, lipid metabolism and oxidative status of largemouth bass,
Micropterus salmoides. Aquaculture 506, 394–400.
Guo, Z., Zhu, X., Liu, J., Han, D., Yang, Y., Xie, S., Lan, Z., 2011. Dietary lipid
requirement of juvenile hybrid sturgeon, Acipenser baerii ♀ × A. gueldenstaedtii ♂.
J. Appl. Ichthyol. 27, 743–748.
Han, Q., Tian, Z., Xia, W., Luo, Y., Wu, M., 2005. Optimal dietary lipid requirement of
yellow catfish (Pelteobagrus fulvidraco). Fish. Sci. 24, 8–11 (in Chinese with English
abstract).
Huang, Y., Wen, X., Li, S., Li, W., Zhu, D., 2016. Effects of dietary lipid levels on growth,
feed utilization, body composition, fatty acid profiles and antioxidant parameters of
juvenile chu’s croaker Nibea coibor. Aquac. Int. 24, 1229–1245.
Hung, L.T., Binh, V.T.T., Thanh Truc, N.T., Tham, L.H., Ngoc Tran, T., 2015. Effects of
dietary protein and lipid levels on growth, feed utilization and body composition in
red-tailed catfish juveniles (Hemibagrus wyckioides, Chaux & Fang 1949). Aquac.
Nutr. 23, 367–374.
Jin, Y., Tian, L., Zeng, S., Xie, S., Yang, H., Liang, G., Liu, Y., 2013. Dietary lipid
requirement on non-specific immune responses in juvenile grass carp
(Ctenopharyngodon idella). Fish Shellfish Immun. 34, 1202–1208.
Jiwyam, W., Nithikulworawong, N., 2014. Stocking density-dependent growth and
survival of Asian red-tailed catfish (Hemibagrus wyckioides) fries: early nursing in
cages. Int. Aquat. Res. 6, 245–250.
Kim, L.O., Lee, S.M., 2005. Effects of the dietary protein and lipid levels on growth and
body composition of bagrid catfish, Pseudobagrus fulvidraco. Aquaculture 243,
323–329.
Kim, K.D., Lim, S.G., Kang, Y.J., Kim, K.W., Son, M.H., 2012. Effects of dietary protein
and lipid levels on growth and body composition of juvenile Far Eastern catfish
Silurus asotus. Asian-Australas. J. Anim. Sci. 25, 369–374.
Kumar, S., Sándor Zs, J., Nagy, Z., Fazekas, G., Havasi, M., Sinha, A.K., De Boeck, G.,
Gál, D., 2017. Potential of processed animal protein versus soybean meal to replace
fish meal in practical diets for European catfish (Silurus glanis): growth response and
liver gene expression. Aquac. Nutr. 23, 1179–1189.
Li, S., Mai, K., Xu, W., Yuan, Y., Zhang, Y., Zhou, H., Ai, Q., 2015. Effects of dietary lipid
level on growth, fatty acid composition, digestive enzymes and expression of some
lipid metabolism related genes of orange-spotted grouper larvae (Epinephelus coioides
H.). Aquac. Res. 47, 2481–2495.
J. Deng et al.
Liu, X.Y., Wang, Y., Ji, W.X., 2011. Growth, feed utilization and body composition of
Asian catfish (Pangasius hypophthalmus) fed at different dietary protein and lipid
levels. Aquac. Nutr. 17, 578–584.
Luo, G., Xu, J., Teng, Y., Ding, C., Yan, B., 2010. Effects of dietary lipid levels on the
growth, digestive enzyme, feed utilization and fatty acid composition of Japanese
sea bass (Lateolabrax japonicus L.) reared in freshwater. Aquac. Res. 41, 210–219.
Mai, K., Mercer, J.P., Donlon, J., 1995. Comparative studies on the nutrition of two
species of abalone, Haliotis tuberculata L. and Haliotis discus hannai Ino. III. Response
of abalone to various levels of dietary lipid. Aquaculture 134, 65–80.
Meng, Y., Li, C., Qin, Q., Tong, Y., Zhu, R., Xu, G., Shi, Y., Shi, Y., Ma, R., 2017. Dietary
lipid levels affect the growth performance, lipid deposition, and antioxidative
capacity of juvenile scaleless carp, Gymnocypris przewalskii, on the Qinghai-Tibetan
Plateau. J. World Aquac. Soc. 49, 788–797.
Nayak, M., Saha, A., Pradhan, A., Samanta, M., Mohanty, T.K., Giri, S.S., 2018. Influence
of dietary lipid levels on growth, nutrient utilization, tissue fatty acid composition
and desaturase gene expression in silver barb (Puntius gonionotous) fingerlings.
Comp. Biochem. Phys. 226B, 18–25.
Ng, H.H., Rainboth, W.J., 1999. The bagrid catfish genus Hemibagrus (Teleostei:
siluriformes) in central Indochina with a new species from the Mekong River. Raffles
B. Zool. 47, 555–576.
NRC, 2011. Nutrient Requirements of Fish and Shrimp. National Research Council of the
National Academies. The National Academies Press, Washington, D.C., USA.
Paul, B.N., Datta, A.K., Das, S., Chattopadhay, D.N., Giri, S.S., Mohanty, S.N., 2011.
Effect of dietary lipid levels on growth and carcass composition of Ompok pabda
(Siluridae) fry. Indian J. Anim. Nutr. 28, 198–202.
Pei, Z., Xie, S., Lei, W., Zhu, X., Yang, Y., 2004. Comparative study on the effect of dietary
lipid level on growth and feed utilization for gibel carp (Carassius auratus gibelio) and
Chinese longsnout catfish (Leiocassis longirostris Günther). Aquac. Nutr. 10, 209–216.
Prasertwattana, P., Manee, N., Namtum, S., 2005. Culture of red-tail mystus, Hemibagrus
wyckioides, in earthen ponds with different stocking densities. In: Proceeding of 7th
Technical Symposium on Mekong Fisheries, Ubon Ratchathani, Thailand. November
15–17, pp. 213–216.
Qiang, J., He, J., Yang, H., Sun, Y., Tao, Y., Xu, P., Zhu, Z., 2016. Dietary lipid
requirements of larval genetically improved farmed tilapia, Oreochromis niloticus (L.),
and effects on growth performance, expression of digestive enzyme genes, and
immune response. Aquac. Res. 48, 2827–2840.
Raj, A.J.A., Haniffa, M.A., Seetharaman, S., Appelbaum, S., 2007. Effect of dietary lipid
levels on survival and growth of the threatened freshwater catfish Mystus montanus.
Ege J. Fish Aquatic Sci. 24, 51–54.
Aquaculture Reports 20 (2021) 100666
Robbins, K.R., Saxton, A.M., Southern, L.L., 2006. Estimation of nutrient requirements
using broken-line regression analysis. J. Anim. Sci. 84, E155–E165.
Shearer, K.D., 1994. Factors affecting the proximate composition of cultured fishes with
emphasis on salmonids. Aquaculture 119, 63–88.
Sivaramakrishnan, T., Sahu, N.P., Jain, K.K., Muralidhar, A.P., Saravanan, K.,
Ferosekhan, S., Praveenraj, J., Artheeswaran, N., 2016. Optimum dietary lipid
requirement of Pangasianodon hypophthalmus juveniles in relation to growth, fatty
acid profile, body indices and digestive enzyme activity. Aquac. Int. 25, 941–954.
Tocher, D.R., 2003. Metabolism and functions of lipids and fatty acids in teleost fish. Rev.
Fish. Sci. 11, 107–184.
Trenzado, C.E., Carmona, R., Merino, R., García-Gallego, M., Furné, M., Domezain, A.,
Sanz, A., 2018. Effect of dietary lipid content and stocking density on digestive
enzymes profile and intestinal histology of rainbow trout (Oncorhynchus mykiss).
Aquaculture 497, 10–16.
Walton, M.J., Cowey, C.B., 1977. Aspects of ammoniogenesis in rainbow trout. Salmo
gairdneri. Comp. Biochem. Phys. 57B, 143–149.
Wang, L., Lu, Q., Luo, S., Zhan, W., Chen, R., Lou, B., Xu, D., 2016. Effect of dietary lipid
on growth performance, body composition, plasma biochemical parameters and liver
fatty acids content of juvenile yellow drum Nibea albiflora. Aquac. Rep. 4, 10–16.
Wang, Y.Y., Ma, G.J., Shi, Y., Liu, D.S., Guo, J.X., Yang, Y.H., Chen, C.D., 2012. Effects of
dietary protein and lipid levels on growth, feed utilization and body composition in
Pseudobagrus ussuriensis fingerlings. Aquac. Nutr. 19, 390–398.
Yi, X., Zhang, F., Xu, W., Li, J., Zhang, W., Mai, K., 2014. Effects of dietary lipid content
on growth, body composition and pigmentation of large yellow croaker Larimichthys
croceus. Aquaculture 434, 355–361.
Zambonino-Infante, J.L., Cahu, C.L., 1999. High dietary lipid levels enhance digestive
tract maturation and improve Dicentrarchus labrax larval development. J. Nutr. 129,
1195–1200.
Zhang, H., Sun, J., Liu, H., Zhao, W., Yang, Z., 2015. The effect of dietary lipid levels on
growth performance, lipid deposition, and antioxidant status of juvenile turbot,
Scophthalmus maximus, fed isonitrogenous and isoenergetics diets. Isr. J. Aquac.-
Bamid. 67. IJA_67.2015.1142.
Zhang, X., Zhang, J., Wang, H., Lin, B., Chen, L., Li, G., Wang, Q., Deng, J., 2019.
Evaluation of soybean meal as alternative to fish meal in diet for juvenile Asian red-
tailed catfish (Hemibagrus wyckioides). Aquac. Nutr. 25, 1036–1049.
Zheng, K., Zhu, X., Han, D., Yang, Y., Lei, W., Xie, S., 2010. Effects of dietary lipid levels
on growth, survival and lipid metabolism during early ontogeny of Pelteobagrus
vachelli larvae. Aquaculture 299, 121–127.