Growth and carcass quality of on-growing river catfish Hemibagrus nemurus fed with dietary salted by-catch and fish viscera meal mixtures as fishmeal substitute

Abstract

Dietary salted by-catches and fish viscera meal mixtures could totally replace fishmeal without negative effect on growth performance of small size (4–25 g) river catfish Hemibagrus nemurus, however, their effects on carcass quality and growth of on-growing river catfish remained uninvestigated. The present study therefore was conducted to assess the effects of dietary fishmeal (FM) replacement with salted by-catches and fish viscera meal mixtures (SBVM) on growth, feed utilization, and carcass quality of on-growing (120–300 g) river catfish. Four isoproteic and isocaloric (34% crude protein and 17 Kj g⁻¹ gross energy) diets were prepared, where dietary FM was replaced with SBVM at levels of 0% as control diet (SBVM0), 50% (SBVM50), 75% (SBVM75), and 100% (SBVM100). A commercial pelleted diet (CD) was used as a reference. A total of 750 on-growing river catfish, 118.95 ± 2.19 g in weight was randomly distributed into 5 triplicate net cages (2 m × 2 m × 1.20 m) at a density of 50 fish per cage. The fish was fed at apparent satiation twice a day for a period of 90 days. Substitution of dietary FM with SBVM up to 75% did not affect survival rate, specific growth rate, weight gain, feed and protein efficiency, lipid retention, protein retention, amino acid profile, body proximate composition, edible flesh, carcass waste, dress-out percentage, flesh liquid holding capacity (P > 0.05). The sensory quality of the fish was comparable with the control and reference diets (P > 0.05). Complete substitution of dietary FM by SBVM negatively impacted specific growth rate, weight gain, feed intake, protein retention, body protein and lipid, lipid retention, flesh liquid holding capacity, and fillet appearance and texture (P < 0.05). Therefore, the SBVM can replace FM in the diet of river catfish up to 75%.

Full text

Aquaculture Reports 27 (2022) 101343
Available online 26 September 2022
2352-5134/© 2022 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/).
Growth and carcass quality of on-growing river catsh Hemibagrus nemurus
fed with dietary salted by-catch and sh viscera meal mixtures as
shmeal substitute
Bustari Hasan
a
, Dian Iriani
a
, Trisla Warningsih
a
, Christopher Marlowe A. Caipang
b
,
Zainal A. Muchlisin
c
, Indra Suharman
a
,
*
a
Faculty of Fisheries and Marine Sciences, Universitas Riau, Pekanbaru, Riau 28292, Indonesia
b
Division of Biological Sciences, College of Arts and Sciences, University of the Philippines Visayas, Miag-ao, Iloilo 5023, Philippines
c
Faculty of Marine and Fisheries, Syiah Kuala University, Banda Aceh 23111, Indonesia
ARTICLE INFO
Keywords:
Fishmeal
Growth
River catsh
Salted by-catches and sh viscera mixtures
Sensory quality
ABSTRACT
Dietary salted by-catches and sh viscera meal mixtures could totally replace shmeal without negative effect on
growth performance of small size (4–25 g) river catsh Hemibagrus nemurus, however, their effects on carcass
quality and growth of on-growing river catsh remained uninvestigated. The present study therefore was con-
ducted to assess the effects of dietary shmeal (FM) replacement with salted by-catches and sh viscera meal
mixtures (SBVM) on growth, feed utilization, and carcass quality of on-growing (120–300 g) river catsh. Four
isoproteic and isocaloric (34% crude protein and 17 Kj g
−1
gross energy) diets were prepared, where dietary FM
was replaced with SBVM at levels of 0% as control diet (SBVM0), 50% (SBVM50), 75% (SBVM75), and 100%
(SBVM100). A commercial pelleted diet (CD) was used as a reference. A total of 750 on-growing river catsh,
118.95 ±2.19 g in weight was randomly distributed into 5 triplicate net cages (2 m ×2 m ×1.20 m) at a density
of 50 sh per cage. The sh was fed at apparent satiation twice a day for a period of 90 days. Substitution of
dietary FM with SBVM up to 75% did not affect survival rate, specic growth rate, weight gain, feed and protein
efciency, lipid retention, protein retention, amino acid prole, body proximate composition, edible esh,
carcass waste, dress-out percentage, esh liquid holding capacity (P >0.05). The sensory quality of the sh was
comparable with the control and reference diets (P >0.05). Complete substitution of dietary FM by SBVM
negatively impacted specic growth rate, weight gain, feed intake, protein retention, body protein and lipid,
lipid retention, esh liquid holding capacity, and llet appearance and texture (P <0.05). Therefore, the SBVM
can replace FM in the diet of river catsh up to 75%.
1. Introduction
River catsh Hemibagrus nemurus is a commercially important spe-
cies in Riau Province, Indonesia, as it has a firm flesh with little bone and
delicate flavor; and its market price is much higher than the other catsh
species in the region (Hasan et al., 2016a, 2016b). Catches of this species
from the wild have been reduced due to environmental damage and
overshing; thus, the upcoming supply of the sh will rely on aqua-
culture (Hasan et al., 2016a, 2016b, 2019). The sh exhibits good
growth in cultured ponds and cages, and it is adaptable to articial
pelleted feed; however, the cost of production is relatively higher than
the other cultured catfish species because of higher dietary protein
requirements, around 34–42%, that are needed for optimum growth
(Khan et al., 1993; Hasan et al., 1999; Abidin et al., 2006; Hasan et al.,
2012, 2016a).
Fishmeal is a conventional protein source for farm-raised sh,
especially among carnivorous species, because their protein and fatty
acid composition are high in quality, and their proportions match the
nutritional requirements of the cultured sh (Hu et al., 2013; Buentello
et al., 2015; Hasan et al., 2019). However, shmeal is expensive and
most of the supply is from import (Luhur et al., 2021). Therefore, there is
a need to develop locally available protein sources to substitute shmeal
in feeds for an efcient and sustainable aquaculture.
Marine shery by-catches are good potential as shmeal alternatives
* Corresponding author.
E-mail address: indra70s@yahoo.com (I. Suharman).
Contents lists available at ScienceDirect
Aquaculture Reports
journal homepage: www.elsevier.com/locate/aqrep
https://doi.org/10.1016/j.aqrep.2022.101343
Received 8 July 2022; Received in revised form 20 September 2022; Accepted 21 September 2022

Aquaculture Reports 27 (2022) 101343
2
because these have protein contents of 50–60%, which are similar to the
protein content of shmeal (Hasan et al., 2016b, 2019, 2021). There is
an abundance in supply, wherein more than 4,392,000 tons are pro-
duced annually, or 63% of the total marine catches in Indonesia (Anon,
2010). The problems on the use of shery by-catches as shmeal sub-
stitute are the seasonality of their production and the supply is
geographically scattered in small amounts. As the by-catches are easily
perishable, these are mostly converted to dry salted products before
being processed into sh feed.
Salt preservation is considered a practical and economical method to
maintain good quality by-catches because the price of salt is cheap, and
its preservation technique is easily practiced by shermen (Hasan et al.,
2016b, 2019, 2021). However, the high salt concentration of salted
products at 15–25% is an important limitation when these are included
in the sh diet. Our previous study indicated that salted by-catches alone
could replace shmeal in river catsh diet at a level up to 75% without
yielding a negative effect on growth and esh quality (Hasan et al.,
2016b, 2019), but higher inclusion levels reduced growth performance.
The high salt content of dietary salted by-catch was believed to be reason
for the low acceptability of this diet by the sh.
Fish viscera from lleted and smoked sh processing plants is
another alternative protein source because of its high protein content,
around 40–45%, and is readily available (Hasan et al., 2020). Animal
viscera is usually of low digestible quality and less palatable to sh; thus,
high inclusion in the diet will result in adverse effects on growth per-
formance and nutrient utilization (Ju et al., 2013; Ok´
e and Abou, 2016).
Blending mixtures of sh viscera and salted by-catches may contribute
synergistic benets to the mixture as feed ingredients, and help improve
the digestibility, palatability, and nutritional quality of the diets. The
mixing of different feed ingredients has been practiced to reduce or mask
unpalatable components in feeds, balance dietary nutritional composi-
tion, and complement dietary amino acid prole (Lee et al., 2010; Kader
et al., 2011; Kader and Koshio, 2012, 2017). Another advantage of
combining salted by-catch and sh visceral meal is increasing the pro-
tein content of the ingredients; thus, can be used in diet formulations for
shmeal substitution.
A previous study on small-sized (4–25 g) river catsh for 60 days
showed that total substitution of dietary shmeal with salted by-catches
and sh viscera meal mixtures did not affect growth performance
(Hasan et al., 2020). However, the effects of shmeal substitution by
these alternative ingredients on carcass quality and growth of
on-growing river catsh remain uninvestigated. The carcass quality of
the sh as a result of the dietary inclusion of these new ingredients needs
to be evaluated to ensure consumer acceptance. Therefore, the objective
of the present study was to determine the effects of substituting shmeal
with salted by-catch and sh viscera meal mixtures on growth and
carcass quality of on-growing (120–300 g) river catsh.
2. Materials and methods
2.1. Ethical statement
All experimental procedures involving sh have been approved by
Syiah Kuala University Research and Ethics Guidelines, Section of Ani-
mal Care and Use in Research, and adhered to the national policies on
responsible handling of sh in research.
2.2. Ingredients and diet formulations
Salted by-catches, shmeal (FM), rice bran (RB), tofu by-products
(TBM), palm oil (PO), and vitamin and mineral mixes were bought
from a local supplier. Fish viscera was obtained from a local smoked sh
(Pangasius hypophthalmus) processing plant. All individual ingredients
were dried and nely ground through a 246 µm mesh and analyzed for
proximate composition. Proximate analyses were made using standard
procedures (AOAC, 2006). Moisture was analyzed by oven drying the
sample to constant weight at 105 ◦C for a day; ash was determined by
combusting the samples in a muffle furnace at 550 ◦C for ve hours. The
total nitrogen content (N ×6.25) was used to calculate crude protein
using the micro-Kjeldahl equipment. The crude lipid content of the
sample was measured by Soxhlet extraction with petroleum ether. The
salt content was measured by combusting the sample at 500 ◦C and
titrating it with 0.1 N AgNO
3
. Amino acid proles were determined
using high-performance liquid chromatography (HPLC), following the
procedures of Cohen et al. (1989). The assessment was conducted after
hydrolyses of the sample under nitrogen in 6 N hydrochloric acid (HCl)
at 110 ◦C for 24 h, and the amino acid calculation was made in a 100 g
−1
sample. The proximate composition of the ingredients is shown in
Table 1.
A mixture of salted marine by-catches and sh viscera meal (SBVM)
was prepared by blending salted by-catches meal and sh visceral meal
at a ratio of 3:1 (w/w dry basis). The ratio was based on the maximum
inclusion level of individual salted by-catch meal in the river catsh diet
which was 75% (Hasan et al., 2016b, 2019) and visceral meal was 25%
(Ok´
e and Abou, 2016). The mixture was used as FM replacement in the
sh diets. Four diet formulations were made to contain 34% crude
protein (isoproteic) and 16.7 Kj gross energy g
−1
(isocaloric) to fulll the
dietary protein needs for river catsh (Hasan et al., 1999, 2012). A
control diet (C) contained 44% FM and no SBVM. The other three diets
(SBVM50, SBVM75, and SBVM100) contained FM which was reduced
and replaced with SBVM at levels of 50%, 75%, and 100%. A commer-
cial pelleted diet of unidentied ingredients (CD) was used as a refer-
ence. The formulated diets were meticulously blended and processed
into dry sinking pellets (3 mm in diameter) via a pelleting machine,
where they were oven-dried at 60 ◦C for about 12 h until their moisture
content was about 10%. All diets were determined for proximate
composition, amino acids, and salt concentration, with their values
presented in Tables 2 and 3. The diets were stored in a refrigerator at
5 ◦C until use.
2.3. Fish samples and the feeding experiment
A total of 750 river catsh, 118.95 ±2.19 g in initial weight, were
purchased from a local commercial hatchery in Sungai Paku, Riau,
Indonesia. The sh were transported to the experimental station (Alam
Bendungan, Riau) and acclimated in a 4 m x 4 m x 1.2 m oating cage for
a week. They were fed a commercial diet during this interval. Ten fishes
were randomly sampled for initial whole-body proximate and amino
acid prole analyses. The feeding experiment was conducted in tripli-
cate oating cages (2 m x 2 m x 1.20 m). The sh were placed at a
Table 1
Proximate and salt composition of the ingredients.
Ingredients Proximate Composition (% dry weight)
a
Protein Lipid Ash NFE
b
Salt
(NaCl)
FM
c
60.02 ±
0.23
11.51 ±
0.10
24.53 ±
0.13
3.94 ±
0.04
3.01 ±
0.06
SBVM
d
55.01 ±
0.32
14.28 ±
0.04
22.43 ±
0.09
8.28 ±
0.20
11.87 ±
0.37
TBM
e
28.27 ±
0.84
4.09 ±
0.43
2.39 ±
0.17
65.25 ±
1.44
–
RB
f
12.32 ±
0.01
9.84 ±
0.96
11.06 ±
0.08
66.77 ±
1.05
–
a
Values are means of triplicate ±S.E.
b
NFE: Nitrogen Free Extract, was calculated as 100-
(ash+moisture+protein+lipid).
c
FM: Fishmeal
d
SBVM: Salted by-catch and viscera mixture: 3:1 w/w dry basis (3 part of
salted by-catches and 1 part of sh viscera)
e
TBM: Tofu by-product meal
f
RB: Rice bran
B. Hasan et al.

Aquaculture Reports 27 (2022) 101343
3
density of 50 individuals cage
−1
in triplicate ve cages. Each of the diets
was randomly given to each cage, and the sh were fed until satiation.
Feeding was performed twice a day at 08:00 AM and 4:00 PM, for a
period of 90 days. Water temperature, pH, and dissolved oxygen were
measured every three days during the feeding experiment. At the end of
the feeding trial, the sh were weighed and the following zootechnical
parameters, growth performance (survival rate, weight gain, and spe-
cic growth rate) and feed utilization (feed intake and efciency ratio,
protein efciency ratio and retention, and lipid retention) were calcu-
lated as follows:
Survival rate (%) =100 ×(final fish number/initial fish number).
Weight gain (g) =nal body weight ₋ initial body weight.
Specific growth rate (%/day) =100 ×[Ln (final body weight) ₋ Ln
(initial body weight)]/.
days.
Feed intake (%/day) =100 ×total feed consumed/[(initial body
weight +final body weight)/2]/days.
Feed efficiency ratio =wet weight gain (g)/total feed consumed (g).
Protein efficiency ratio =wet weight gain (g)/total protein
consumed.
Protein retention (%) =100 ×body wet protein gain (g)/total pro-
tein consumed (g).
Lipid retention (%) =100 ×body wet lipid gain (g)/total lipid
consumed (g).
Hepatosomatic index (%) =100 ×weight of liver/weight of fish.
Viscerasomatic index (%) =100 ×weight of viscera /weight of fish.
2.4. Carcass quality analysis
Thirty fish from every cage at the nal feeding experiment were
randomly sampled. Ten sh were kept at −20 ◦C for proximate
composition and amino acid analyses, and another 20 sh were evalu-
ated for llet yield, dress-out percentage, carcass waste, esh liquid
holding capacity, and llet sensory quality. Liquid holding capacity
analysis was made using the centrifuging method developed by Rora and
Einen (2003). Triplicate samples of 15 g fresh llet were weighed and
put in a tube with a weighted lter paper (Schleicher and Scheilcher and
Schuell GmbH, Dassel, Germany) (V1). The tubes were centrifuged at
500 x g at 4 ◦C for 10 min, and the wet paper was weighted (V2).
Liquid-holding capacity was estimated as percent loss of liquid which
was calculated as 100 (V1–V2) S
−1
, where S=weight of muscle sample.
The liquid loss was expressed as percentage of muscle wet weight.
Sensory evaluation was carried following the methods of Hasan et al.
(2019). A trained panel of six teaching staff at the Fish Processing
Technology Department, Universitas Riau, evaluated the appearance,
texture, odor, and overall quality of the fresh llets. For the evaluation
of avor, the llets were steamed at 100 ◦C for 10 min prior to the
evaluation. The sensory examination was performed in a separate room
with individual booths. The panelists discussed the sensory qualities to
agree on the denitions and scores of each attribute. The qualities were
as follows: appearance, reddish whiteness and lightness in color; texture,
elasticity, and softness; avor, the intensity of fresh specic avor and
off-avor (earthy musty avor, oily, and waste avor); odor, the in-
tensity of fresh specic odor and off-odor (earthy musty odor, oily, and
waste odor); and overall quality. A sh quality score sheet was used for
sensory quality assessment on a scale of 1 – 9. A score 9 was the highest
quality value, which was characterized by appearance, very intense
reddish whiteness and lightness in color, solid and elastic in texture; and
odor, very intense fresh odor and no off-odor; avor, very intense fresh
avor and no off-avor. A score of 1 was the lowest quality value, which
was characterized by appearance, very intense discoloration and dark-
ness; texture, very intense softness and darkness; odor, very intense
off-odor; and avor, very intense off-avor. Fillet yield was the weight of
Table 2
Formulation (%), proximate composition (%), and energy content (KJ g
−1
) of
experimental diets.
Ingredients SBVM0 SBVM50 SBVM75 SBVM100 CD
1
FM
2
44 22 11 0 –
SBVM
3
0 22 33 44 –
TBM
4
16 17 18 16 –
RB
5
35.50 35.50 34 38 –
PO
6
4.00 3.00 3.50 1.50
Vitamin and
mineral mix
7
0.50 0.50 0.50 0.50 –
Proximate analysis
Protein 34.09 ±
0.09
a
34.04 ±
0.10
a
33.57 ±
0.37
a
33.75 ±
0.22
a
31.79 ±
0.28
b
Lipid 14.09 ±
0.36
a
14.28 ±
0.28
a
14.74 ±
0.26
b
15.08 ±
0.36
b
11.40 ±
0.23
c
Ash 9.69 ±
0.11
a
9.73 ±
0.15
a
9.80 ±
0.13
a
10.33 ±
0.10
b
8.62 ±
0.08
c
NFE 32.24 ±
1.12
a
32.78 ±
0.61
a
32.97 ±
0.37
a
32.18 ±
0.45
a
40.60 ±
0.35
b
Salt (NaCl) 1.18 ±
0.16
a
3.29 ±
0.21
b
4.22 ±
0.19
c
5.37 ±
0.23
d
1.16 ±
0.11
a
Gross energy
(KJ g
−1
)
c
16.37 ±
0.09
a
16.53 ±
0.10
a
16.65 ±
0.20
a
16.68 ±
0.10
a
16.38 ±
0.01
a
1
CD: Commercial diet
2
FM: Fishmeal
3
SBVM: Salted by-catch and viscera mixture
4
TBM: Tofu by-product meal
5
RB: Rice bran
6
PO: Palm oil
7
Vitamin and mineral mix: Vit A, 2750 IU; Vit D, 550,000 IU; Vit E, 25,000 IU;
Vit K, 5000 mg; Choline, 250,000 mg; Niacin, 50,000 mg; Riboavin, 10,000
mg; Pyridoxine, 10,000 mg; Calcium D-pantothenate, 25,000 mg; Biotin, 50 mg;
Folacin, 2500 mg; Cyanocoblamin, 10 mg; Ascorbic acid, 50,000 mg; K
2
HPO
4
,
30%; KCL, 8.4%; MgSO
4
, 14.8%; CaHPO
4
0.2 H
2
O, 27.4%; FeCL
3
, 1.4%;
MnSO
4
0.7 H
2
O, 0.2%; CaCO
3
, 16.8%.
cGross energy was calculated as 16.7, 16.7, and 37.7 kJ/g for protein, carbo-
hydrate, and lipids.
Means (triplicate ±S.D) in same raw with different superscript are signicantly
different (P <0.05).
Table 3
Individual essential amino acids and total essential amino acid ratios (IEAA/TEAA) of the river catsh esh and experimental diets.
Essential Amino Acid River catsh SBVM0 SBVM50 SBVM75 SBVM100 CD
Histidine 7.46 7.64 9.50 9.95 8.48 8.78
Arginine 6.92 6.95 6.87 9.09 6.90 7.95
Threonine 6.63 7.68 7.66 6.65 6.03 7.07
Alanine 6.90 6.83 6.65 7.60 6.78 6.18
Valine 8.07 8.37 8.32 10.33 8.19 7.87
Methionine 6.47 7.02 6.98 6.74 6.08 7.17
Isoleucine 12.12 11.98 12.08 11.79 12,10 12.74
Leucine 17.97 17.90 18.47 16.42 18.22 18.10
Phenylalanin 7.47 7.57 9.17 4.79 8.32 8.37
Lysine 14.62 15.39 15.14 14.85 14.43 15.77
Tryptophane ND
a
ND ND ND ND ND
a
ND=Not determined. Amino prole was done on pooled samples of 15 sh (5 sh/replicate) in each treatment.
B. Hasan et al.

Aquaculture Reports 27 (2022) 101343
4
lleted muscle divided by whole body weight. Dress-out percentage was
the weight of the sh without head, ns, skin and viscera divided by
whole body weight; and carcass waste was the total weight of head,
bone, ns, skin and viscera divided by whole body weight. Fillet yield,
dress out and carcass waste was expressed as percent weight.
2.5. Statistical analysis
A completely randomized design with four treatments and replicated
thrice was utilized for the experiment. One-way ANOVA and the least
signicant difference test at the significance value of 95% (P <0.05)
were utilized to determine the significant differences among the treat-
ments. The data analyses were made using SPSS software, version 17
(SPSS Inc., Chicago, USA).
3. Results
3.1. Ingredient and diet composition
Salted by-catch and sh visceral meal mixture (SBVM) was slightly
lower in crude protein and ash, even though it was higher in nitrogen-
free extract (NFE) as well as salt concentration compared with FM
(Table 1). All experimental diets (Table 2) contained similar crude
protein, NFE, and energy (P >0.05), but crude lipid and ash tended to
increase with higher levels of SBVM in the diets; with values signi-
cantly higher (P <0.05) for the SBVM100 diet than with the control
(SBVM0). Salt concentrations also increased (P <0.05) with higher
SBVM in the diets, with values at 1.18%, 3.29%, 4.22%, and 5.37% for
SBVM0, SBVM50, SBVM75, and SBVM100 diets, respectively. The ratio
of individual essential amino acid and total essential amino acid (IEAA/
TEAA ratio), which was considered as an indicator for amino acid bal-
ance in the fish diets, slightly varied among the experimental diets.
Lysine, methionine, and threonine diminished with the corresponding
decrease of FM in the diet, and the values in SBVM100 diet were much
lower than the values obtained in the esh of river catsh. In compar-
ison with the reference diet (CD), the experimental diets (SBVM0,
SBVM50, SBVM75, and SBVM100) were higher in protein, lipid, ash
contents and energy, but lower in NFE.
3.2. Water quality, growth, and feed utilization
Water temperature during the experiment was within 27.8–32.50 ◦C,
pH 6.2–7.40, and dissolved oxygen 5.6–7.23 mg L
−1
. Growth perfor-
mance and feed utilization data are shown in Table 4. The control diet
(SBVM0) gave similar growth and feed utilization values in all param-
eters (P >0.05) to the reference diet. Survival rate (SR) in all treatments
ranged from 97.62% to 98.58%, and the values were maintained among
the dietary treatments (P >0.05). Weight gain (WG) and specic growth
rate (SGR) of the sh were not affected by replacing FM with SBVM up to
75% (P >0.05), but total substitution (100%) reduced WG and SGR (P
<0.05). Feed intake (FI) and protein retention (PR) maintained the
same pattern with WG and SGR; however, lipid retention (LR) increased
as the FI increased (P <0.05). Food efciency ratio (FER) and protein
efciency ratio (PER) were not affected by partial or total replacement
of dietary FM by SBVM (P >0.05). Total replacement of FM by SBVM
neither affected the hepatosomatic index (HSI) nor the viscerasomatic
index (VSI) (P >0.05).
3.3. Fish body composition and amino acid proles
Whole-body protein (Table 5) decreased, while body lipid increased
as the FM was substituted by SBVM in the diets, and the signicant
decrease in body protein or increase in body lipid was evident when
dietary FM was replaced entirely by SBVM (P <0.05). However, whole-
body moisture and ash were not affected by partial or total replacement
of FM by SBFVM in the diets (P >0.05). The proximate composition of
the sh esh maintained a similar pattern to whole-body composition.
The total amino acids in the sh esh ranged from 46.73% to 46.39%;
with the values were quite similar among all the experimental diets
(Table 6).
3.4. Fillet yield, dress-out percentage, liquid-holding capacity, and
sensory quality
The substitution of FM by SBVM up to 75% in the sh diet did not
affect the llet yield, dress-out percentage, liquid-holding capacity, and
sensory quality of sh esh (P >0.05) (Table 7). However, complete
substitution of shmeal by SBVM reduced liquid-holding capacity and
appearance as well texture values of the esh (P <0.05).
Inclusion of SBVM by replacing shmeal in the sh diets of up to 75%
did not inuence the appearance, texture, avor, odor, and overall
quality of the sh esh (Table 5) (P >0.05). Their quality values were
Table 4
Growth and feed utilization of river catsh fed experimental diets for 90 days.
Parameter SBVM0 SBVM50 SBVM75 SBVM100 CD
Initial weight (g) 116.38
±3.86
116.19
±1.35
120.95
±5.87
120.95 ±
1.35
120.28
±2.69
Final weight (g) 296.97
±10.58
296.89
±6.85
288.38
±14.88
272.15 ±
10.32
301.91
±10.39
Survival rate (%) 98.58 ±
9.90
97.62 ±
4.36
98.24 ±
4.96
98.10 ±
3.30
98.11 ±
1.65
Weight gain (g) 180.59
±6.76
a
180.71
±7.99
a
169.34
±20.41
a
151.20 ±
9.06
b
181.63
±8.06
a
Specic growth
rate (%/day)
1.04 ±
0.01
a
1.04 ±
0.04
a
0.98 ±
0.11
ab
0.90 ±
0.03
b
1.02 ±
0.02
a
Feed intake (%) 1.82 ±
0.13
a
1.80 ±
0.087
a
1.68 ±
0.08
a
1.49 ±
0.05
b
1.82 ±
0.15
a
Feed efciency
ratio
2.40 ±
0.19
2.38 ±
0.16
2.39 ±
0.32
2.44 ±
0.03
2.45 ±
0.25
Protein efciency
ratio
0.82 ±
0.06
0.81 ±
0.05
0.80 ±
0.11
0.82 ±
0.01
0.78 ±
0.08
Protein retention
(%)
20.01 ±
0.88
a
20.07 ±
1.38
a
20.31 ±
2.73
a
16.09 ±
0.36
b
20.90 ±
2.02
ab
Lipid retention
(%)
61.03 ±
6.45
a
61.02 ±
1.71
a
64.57 ±
9.59
a
78.37 ±
3.94
b
69.52 ±
5.97
ab
Hepatosomatic
index (%)
1.51 ±
0.12
1.52 ±
0.09
1.51 ±
0.20
1.52 ±
0.14
1.50 ±
0.16
Viscerasomatic
index (%)
3.20 ±
0.17
3.19 ±
0.09
3.20 ±
0.02
3.20 ±
0.13
3.19 ±
0.05
Means (triplicate ±S.D) in the same row with different superscripts are signif-
icantly different (P <0.05).
Table 5
Body proximate composition (%) of river catsh fed experimental diets.
Proximate
Composition
SBVM0 SBVM50 SBVM75 SBVM100 CD
Whole body
Moisture 70.37 ±
1.04
69.28 ±
0.55
69.04 ±
0.99
68.82 ±
0.30
70.03 ±
0.55
Ash 2.48 ±
0.39
2.51 ±
0.38
2.51 ±
0.11
2.52 ±
0.35
2.50 ±
0.19
Protein 15.99 ±
0.29
a
15.94 ±
0.17
a
15.79 ±
0.20
a
14.24 ±
0.15
b
15.89 ±
0.10
a
Lipid 9.87 ±
0.37
a
10.24 ±
0.24
a
10.27 ±
0.29
a
11.68 ±
1.29
b
10.37 ±
0.05
a
Flesh
Moisture 70.41 ±
0.80
70.34 ±
0.36
70.36 ±
0.54
70.15 ±
0.20
70.13 ±
0.15
Ash 1.21 ±
0.06
1.31 ±
0.08
1.33 ±
0.13
1.32 ±
0.42
1.23 ±
0.14
Protein 17.77 ±
0.338
a
17.82 ±
0.26
a
17.71 ±
0.42
a
15.88 ±
0.58
b
16.69 ±
0.11
ab
Lipid 8.75 ±
0.70
a
9.91 ±
0.24
ab
10.03 ±
0.68
ab
10.50 ±
1.07
b
8.64 ±
0.42
a
Means (triplicate ±S.D) in the same row with different superscripts are signif-
icantly different (P <0.05).
B. Hasan et al.

Aquaculture Reports 27 (2022) 101343
5
similar to the llets of sh fed commercial diet (CD). However,
appearance, texture, and overall values decreased (P <0.05) as the FM
was substituted with SBVM in the sh diets.
4. Discussion
The survival rate (SR) ranged 97.62–98.58% in all treatments, and
did not signicantly vary among the dietary treatments, illustrating that
the experimental diets did not negatively impact the health of the sh.
Final weight, weight gain (WG), and specic growth rate (SGR) of sh
were neither affected by the substitution of dietary FM by SBVM up to
75% and their values were similar to sh fed a commercial diet (CD).
This indicates that SBVM can be added in the diet of river catsh up to
75%. The substitution values of dietary SBVM for FM in this study were
comparable to animal by-product blends (80%) in the diet for juvenile
grouper, Epinephelus coioides (Millamena et al., 2002), combined
rendered animal protein sources (75%) for rainbow trout, Oncorhynchus
mykiss (Lu et al., 2015), but higher than blended animal by-product
meals and soy protein concentrate (50%) for Atlantic salmon, Salmo
salar (Hatlen et al., 2014), tuna by-product (30%) for juvenile olive
flounder, Paralichthys olivaceus (Kim et al., 2014), animal protein blend
(18.9%) for Japanese seabass, Lateolabrax japonicas (Hu et al., 2013),
sh hydrolysate (15%) for juvenile pike silverside, Chirostoma estor
(Ospina-Salazar et al., 2016), shrimp by-catch meal (25%) for juvenile
red drum, Sciaenops ocellatus (Li and Wang, 2004). However, compared
with earlier studies on juvenile river catsh (5–21 g), the substitution
value of FM by SBVM in this study on bigger sized sh (120–300 g) was
slightly lower (75% in this study as compared to 100% in the earlier
study using small-sized sh). The reason might be that the dietary SBVM
used in the present study was slightly lower in quality, higher in salt
concentration and lower in lysine, methionine, and threonine as
compared with dietary SBVM that was used in the previous study. Fish
by-catches as the main protein source in the SBVM diets usually vary in
nutritional quality, depending on species and freshness of the by-catches
(Hasan et al., 2016a, 2019).
Complete substitution of FM by SBVM in this study reduced growth
(WG and SGR), and feed intake (FI). The effects of the total replacement
of FM by alternative ingredients on growth were found in most species,
including red drum, Sciaenops ocellatus (Li et al., 2004), Atlantic salmon,
Salmo salar L. (Pratoomyot et al., 2010, 2011); turbot, Scophthalmus
maximus (Xu et al., 2016); Senegalese sole, Solea senegalensis (Cabral
et al., 2013); olive ounder, Paralichthys olivaceus (Kim et al., 2014; Yi
et al., 2015). Feed intake (FI) in this study had a similar decreasing trend
with SGR, indicating that the slower SGR of sh fed SBVM100 diet was
correlated with lower FI. Poor growth due to significantly reduced FI
was also reported in Japanese seabass, Lateolabrax japonicas and Sine-
gale sole, Solea senegalensis when FM was excessively substituted with
plant protein diets (Hu et al., 2010; Wang et al., 2012; Cabral et al.,
2013) and steam-dried fish meal (Hu et al., 2013), and spotted rose
snapper, Lutjanus guttatus when fed high-level dietary tuna muscle
by-product (Uyan et al., 2006). The inverse relationship of FI with
increasing FM substitution levels using by-product meals was also re-
ported by Kader et al. (2010, 2011) and Pratoomyot et al. (2010). FI
usually correlates with the palatability of the diets, and diets become
less palatable to sh due to imbalance of amino acid content (Cabral
et al., 2011, 2013, 2012), and the presence of bitter or salty taste sub-
stances in the diets (Pratoomyot et al., 2011; Hasan et al., 2016b, 2019).
Therefore, the presence of an imbalance amino acid content and higher
salt concentration in the SBVM100 diet could have been the major
factors that resulted in the lower palatability of the diets.
In this study, dietary FM partially or totally replaced by SBVM did
not signicantly affect FER or PER, and this was also reported in Atlantic
salmon, Salmo salar L. (Pratoomyot et al., 2011). However, there was a
reduction in PR and an increase in LR when dietary FM was completely
replaced with SBVM. The reduced PR that was obtained in this study,
indicated that some dietary protein was utilized for energy production
(catabolic process) instead of protein synthesis (anabolism process).
This was supported by Day and Gonz´
alez (2000) and Arnason et al.
(2017) in their study on feeding turbot, Scophthalmus maximus L. with
soybean protein concentrate as a replacement for dietary FM. PR is
usually correlated with nutritional quality and digestibility of the sh
diet; and the reduction of PR in the sh fed SBVM100 diet might be due
to lower IEAA/TEAA ratio of dietary lysine, methionine, and threonine
in the SBVM100 diet in comparison with the IEAA/TEAA ratio of lysine,
methionine, and threonine in the esh of the sh. In most of the cheap
alternative protein sources, the amounts of lysine, methionine, and
threonine are the limiting factors, and a decit in one of them will result
in poor utilization of the available dietary protein (Luo et al., 2006;
Peres and Oliva-Teles, 2009; Hu et al., 2013; Baki et al., 2017). Salt
concentration and ash, which were higher in the SBVM100 than in other
experimental diets negatively affected the palatability and digestibility
of the diets; thus, reducing growth and nutrient utilization of the sh.
Previous studies on river catsh (Hasan et al., 2016b, 2019) and juvenile
ounder, Paralichthys olivaceus, found unfavorable impacts on growth
and protein utilization due to higher salt concentrations in the diets
(Park et al., 2000). Rainbow trout, Oncorhynchus mykiss (Watanabe and
Pongmaneerat, 1991), gilthead sea bream, Sparus aurata (Nengas et al.,
1995), Siberian sturgeon, Acipenser baerii (Liu et al., 2009), and spotted
Table 6
Flesh amino acid proles of river catsh (% sample) fed experimental diets.
Amino Acid Prole SBVM0 SBVM50 SBVM75 SBVM100 CD
Aspartic acid 4.36 4.67 4.87 4.46 3.92
Glutamic acid 7.30 7.82 8.34 8.43 8.99
Serine 1.53 1.86 1.65 1.28 1.79
Glycine 2.13 2.36 2.60 2.53 2.40
Histidine 1.40 1.51 1.44 1.65 1.76
Arginine 1.24 0.99 1.21 1.28 1.45
Threonine 2.50 2.64 2.29 2.37 2.15
Alanine 2.00 1.62 1.21 1.14 1.60
Proline 3.25 3.50 3.49 3.97 3.00
Tyrosine 1.76 1.52 1.58 1.50 1.95
Valine 2.88 2.32 2.49 2.38 2.33
Methionine 1.84 1.72 1.80 1.74 1.79
Cysteine 1.32 1.29 1.06 1.44 1.35
Isoleucine 2.29 2.29 1.84 2.11 2.24
Leucine 5.20 5.10 4.77 4.75 4.72
Phenylalanine 2.08 2.09 2.11 2.10 2.08
Lysine 3.63 3.42 3.81 3.25 3.00
Total 46.71 46.73 46.55 46.39 46.51
Table 7
Carcass quality of river catsh fed experimental diets.
Carcass
Characteristics
SBVM0 SBVM50 SBVM75 SBVM100 CD
Fillet yield (%) 47.46 ±
0.75
47.03 ±
2.41
46.77 ±
0.60
46.74 ±
0.45
47.57
±1.67
Dress-out (%) 59.72 ±
1.39
59.86 ±
0.87
60.36 ±
0.90
59.79 ±
1.99
60.76
±1.10
Carcass waste
(%)
52.54 ±
0.75
52.97 ±
2.41
53.23 ±
0.60
53.26 ±
0.45
52.43
±1.68
Liquid holding
capacity (%)
88.96 ±
0.29
a
88.23 ±
0.62
a
88.03 ±
0.20
a
87.41 ±
0.62
b
88.61
±0.12
a
Sensory quality
Appearance 8.75 ±
0.12
a
8.75 ±
0.18
a
8.72 ±
0.04
ab
8.19 ±
0.38
b
8,69 ±
0.10
a
Texture 8.81 ±
0.10
a
8.78 ±
0.08
a
8.78 ±
0.10
a
8.53 ±
0.14
b
8.75 ±
0.07
a
Odor 8.67 ±
0.14
8.39 ±
0.16
8.33 ±
0.14
8.22 ±
0.16
8.50 ±
0.36
Flavor 8.61 ±
0.16
8.59 ±
0.19
8.63 ±
0.11
8,57 ±
0.18
8.61 ±
0.21
Overall 8.61 ±
0.08
a
8.59 ±
0.07
a
8.59 ±
0.19
a
8.24 ±
0.15
b
8.65 ±
0.03
a
Means (triplicate ±S.D) in the same row with different superscripts are signif-
icantly different (P <0.05).
B. Hasan et al.

Aquaculture Reports 27 (2022) 101343
6
rose snapper, Lutjanus guttatus, have all been found to have a negative
relationship between dietary ash content and dietary protein di-
gestibility (Hernandez et al., 2014). Increased LR in sh fed SBVM100
diet as compared with those fed SBVM0 diets could be attributed to the
differences in energy sources of the diets. Although all experimental
diets were formulated with similar energy levels, the energy source in
the SBVM100 diet was predominantly from the viscera meal and salted
by-catches, which might be more readily convertible to body lipid as
compared with palm oil, which was the predominant energy source in
the SBVM0 diet. This agrees with our ndings on feeding river catsh
with a co-dried sh silage diet, where palm oil was used as the energy
source for dietary energy balance (Hasan et al., 2001). HSI and VSI are
usually used as biological indices (Ha et al., 2020) and similar HSI or VSI
between among sh fed SBVM diets with the control diet indicated that
there was no change in the biological status of sh fed SBVM diets.
Whole body moisture and ash were not impacted by partial or
complete replacement of FM with SBVM; however, body protein
decreased and body lipid increased as the dietary FM was completely
substituted with SBVM (SBVM100). Proximate composition of the esh
in sh fed experimental diets maintained the same pattern with the
whole body composition. A negative change in the body composition of
the sh as dietary FM was substituted with alternative protein sources
has been reported in many species, including Oncorhynchus mykiss (Lee
et al., 2010), Sparus macrocephalus (Zhou et al., 2011), Salmo salar
(Pratoomyot et al., 2011), Ictalurus punctatus (Peterson et al., 2012),
Paralichthys olivaceus (Lee et al., 2012; Kader and Koshio, 2012; Kim
et al., 2014), Rachycentron canadum (Watson et al., 2014), Larimichthys
croceus (Yi et al., 2015) and Clarias gariepinus (Arnauld et al., 2016).
Signicantly lower body protein and higher body lipid of sh fed with
SBVM100 diet were probably associated with lower protein retention
and higher lipid retention values of the SBVM100 diets. The total amino
acid proles of the sh esh were quite similar among the sh fed
experimental diets, reecting that there was no effect from partial or
complete substitutions of dietary FM with SBVM. Similar results were
also demonstrated in previous studies on river catsh, Hemibagrus
nemurus (Hasan et al., 2016b, 2019), rainbow trout, Oncorhynchus mykiss
(Hernandez et al., 2014) and Asian seabass, Lates calcarifer (Hong et al.,
2021) when dietary FM was substituted with sh or poultry by-products.
Fillet yield, dress-out percentage, carcass waste, liquid-holding capacity,
and sensory quality of sh meat were not affected by substituting SBVM
for shmeal in the sh diet up to 75%, and the results were comparable
with those of sh fed a commercial diet. However, complete substitution
of dietary FM with SBVM reduced liquid-holding capacity and appear-
ance as well as texture values of the esh. These could be correlated with
the lipid content of esh in sh fed higher SBVM levels. Lower
liquid-holding capacity values of the sh esh are related with the lipid
content of the esh, yet maintain an inverse relationship with the pro-
tein composition of the esh. Feeding river catsh with low protein and
high lipid diets showed an increase in esh lipid and lower
water-holding capacity compared with sh fed high-protein and
low-lipid diets (Hasan et al., 2016a), thus, a lower esh liquid holding
capacity is a result of a high lipid content in the esh.
Inclusion of SBVM replacing shmeal in the sh diets up to 75%
(SBVM75) did not inuence the appearance, texture, avor, odor, and
overall quality of the sh llet; the value did not either differ from the
llet of sh fed a commercial diet (CD). However, the appearance,
texture, and overall values decreased when shmeal was totally
substituted with SBVM (SBVM100) in the sh diets. Lower appearance
and texture values of the llets of sh fed SBVM100 diet may correlate to
higher lipid composition and lower water-holding capacity of the llets
of sh fed SBVM100 diet. Lower appearance and texture values of the
llets of sh containing high body lipid were also reported in our pre-
vious study on river catsh fed high dietary lipid and lower protein
(Hasan et al., 2016a).
5. Conclusion
Substitution of dietary shmeal (FM) with salted by-catch and sh
viscera meal (SBVM) up to 75% did not affect overall growth perfor-
mance, feed utilization, and carcass quality of river catsh. However,
complete substitution of dietary FM with SBVM negatively affected
weight gain, specic growth rate, feed intake, lipid retention, body
protein, body lipid, liquid-holding capacity, esh appearance and
texture. Therefore, SBVM can be included in the river catsh diet to
replace conventional FM up to 75%.
Ethical approval
All experimental procedures involving sh have been approved by
Syiah Kuala University Research and Ethics Guidelines, Section of Ani-
mal Care and Use in Research, and adhered to the national policies on
responsible handling of sh in research.
CRediT authorship contribution statement
Bustari Hasan was involved in Conceptualization, Methodology,
Data gathering, Writing – analysis, original draft, review & editing,
Supervision, Resources. Dian Iriani was involved in Conceptualization,
Methodology and Data gathering. Trisla Warningsih was involved in
Conceptualization and Data gathering. Christopher Marlowe A. Cai-
pang was involved in Writing – analysis, original draft, review & edit-
ing. Zainal A. Muchlisin was involved in Conceptualization, Writing –
review & editing. Indra Suharman was involved in Conceptualization,
Methodology, Data gathering, Writing – analysis, original draft, review
& editing.
Data availability
The datasets generated during and/or analyzed in the study are
available from the corresponding author on reasonable request.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
The authors would like to thank the Director of the Institute of
Research and Extension Universitas Riau Pekanbaru for the research
financial support. We immensely appreciate the Director of Research
and training center Alam Bendungan, Sungai Paku Riau for experi-
mental facilities and valuable assistance during the experimental period.
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