Saudi Journal of Biological Sciences 30 (2023) 103601

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Saudi Journal of Biological Sciences

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Original article

Effects of dietary replacement of fish meal by soybean meal on growth,

feed utilization, and health condition of stinging catfish, Heteropneustes
fossilis
Sumon Howlader a, Kanij Rukshana Sumi a,⇑, Subroto Sarkar a, Sheikh Masum Billah a,
Mohammad Lokman Ali a, Jewel Howlader b, Md Shahjahan c
a
Department of Aquaculture, Patuakhali Science and Technology University, Dumki, Patuakhali-8602, Bangladesh
b
Department of Horticulture, Patuakhali Science and Technology University, Dumki, Patuakhali-8602, Bangladesh
c
Department of Fisheries Management, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh

a r t i c l e i n f o a b s t r a c t

Article history: Soybean meal (SBM) is a cost-effective alternative protein source to replace costly fish meal in aquacul-
Received 14 September 2022 ture. This present study determined to measure the effects of replacing fish meal (FM) protein with SBM
Revised 31 December 2022 on growth, feed utilization, and health condition of stinging catfish, Heteropneustes fossilis. Four isoni-
Accepted 12 February 2023
trogenous (35 %) diets were applied in four treatment groups designed as SBM0, SBM25, SBM50, and
Available online 15 February 2023
SBM75, where 0 %, 25 %, 50 %, and 75 % of FM protein were substituted by SBM, respectively.
Significantly higher mean final weight (g), weight gain (g), percent weight gain (%), specific growth rate
Keywords:
(% day
1), and protein efficiency ratio (PER) were recorded in SBM0, SBM25, and SBM50 groups than SBM75
Diet replacement
Fish meal
group. Consequently, significantly lower feed conversion ratio (FCR) was found in SBM0, SBM25, and
Soybean meal SBM50 groups than SBM75 group. Moreover, protein content of whole-body carcass was significantly
Stinging catfish higher in SBM25 and lower in SBM0 group however, lipid content was significantly higher in SBM0 and
SBM75 than in other groups. Hemoglobin, red blood cells, and white blood cells were significantly higher
in SBM0, SBM25, and SBM50 groups compared to SBM75. However, the higher the substitution of FM pro-
tein by SBM in diets higher the values of glucose. Morphological analysis of the intestine including villi
length (lm), width (lm), and area (mm2); crypt depth (lm); wall thickness (lm); abundance of goblet
cell (GB); and muscle thickness (lm) showed an increasing trend in fish fed diet containing upto 50 %
replacement of FM protein by SBM. Therefore, the results suggest that SBM could replace upto 50 %
FM protein in diets of H. fossilis without compromising growth, feed efficiency, and health status.
Ó 2023 The Author(s). Published by Elsevier B.V. on behalf of King Saud University. This is an open access
article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction survive in less oxygen content water therefore suitable for com-
mercial aquaculture (Haniffa and Sridhar, 2002). The production
Heteropneustes fossilis (stinging catfish), is high-priced and cost is low with high market demand because of its superior qual-
widespread among the air-sac catfishes because of its suitable con- ity flesh having high nutritional and therapeutic value (Alam et al.,
tent of quality protein and iron (Bhatt, 1968; Anon, 1982). It can 2009). As well, H. fossilis are highly fecund and adaptable to artifi-
cial diets at high temperatures and salinity fluctuation
(Radhakrishnan and Sugumaran, 2010; Jhingran, 1991; Thakur,
⇑ Corresponding authors.
1991). Due to these promising characteristics related to produc-
E-mail addresses: [email protected] (S. Howlader), [email protected] (K.
tion, H. fossilis attains considerable attention for culture in South-
R. Sumi), [email protected] (S. Sarkar), [email protected] (S.M. Bill-
ah), [email protected] (M.L. Ali), [email protected] (J. Howlader), mdshahja- east Asia over the past few years.
[email protected] (M. Shahjahan). Feed cost broadly represents around 70 % of the total opera-
Peer review under responsibility of King Saud University. tional cost because proteins are the high-priced dietary source of
semi-intensive or intensive grow-out farming operations
(Hossain et al., 2020a, b). One of the biggest targets of successful
aquaculture is to attain highest growth by investing lowest inputs
Production and hosting by Elsevier at lowest price. Fish meal (FM), a high-priced feed ingredient, is

https://doi.org/10.1016/j.sjbs.2023.103601
1319-562X/Ó 2023 The Author(s). Published by Elsevier B.V. on behalf of King Saud University.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
S. Howlader, K.R. Sumi, S. Sarkar et al. Saudi Journal of Biological Sciences 30 (2023) 103601

generally considered one of the major sources of protein for aqua- (50 fingerlings in each tank) for 14 weeks in a temporary shed
feed production because of its higher protein along with stable set up on the premises of the Faculty of Fisheries, Patuakhali
amino acids, higher digestible energy, and micronutrients (Tacon Science and Technology University, Dumki, Patuakhali, Bangla-
and Jackson, 1985). The higher prices and irregular supply of FM desh. Detailed procedures of tank preparation were followed as
demand the search for alternatives with lower prices and highly per Billah et al. (2022). Before starting the feeding trial, all the fish
available plant feedstuffs such as soybean, rapeseed meal, moong, were fed for one week with a basal diet to adjust to the experimen-
guar, sorghum, etc. (Robinson and Li, 2007; Uddin et al., 2007). tal systems and conditions. During the trial, the feed was given at
Among all plant protein sources, soybean meal (SBM) repre- the rate of 3 % body weight to all fish daily (2 times at 8:00 and
sents the high protein content, most secured amino acid profile, 18:00 h) (Yang et al., 2011). Based on the recorded data of the total
stable source, and realistic cost (Meng et al., 2020; Pervin et al., weight of fish, the ration was regulated for each treatment at fort-
2020). Several studies reported SBM to replace FM in diets for sev- nightly sampling. Siphoning was performed to remove uneaten
eral fish species owing to the source of quality protein of soybean feeds daily. Water exchange was completed from tap water every
throughout the world (Nyirenda et al., 2000; Kalla et al., 2003). three days intervals. To observe water quality parameters, respec-
Nonetheless, the effects of replacing FM protein with SBM on the tive monitoring systems were applied throughout the experimen-
growth and physiological status of fish are species specific along tal periods. The observed parameters were within a suitable range
with their feeding mechanisms (Zhou et al., 2018). In general, for the culture of fish. The recorded values of temperature, dis-
SBM is better utilized by herbivorous and omnivorous fish than solved oxygen, pH, ammonia–nitrogen, and nitrite-nitrogen were
carnivorous fish species. Moreover, the complete or partial substi- 26.6–31.6 °C, 4.5–6.1 mg l
1, 6.7–8.2, 0.1–0.5 mg l
1, and 0.02–0.
tution of FM with SBM do not affect the growth and physiology of 05 mg l
1, respectively.
various herbivorous and omnivorous species of fish (Liu et al.,
2021). Siddique et al. (2014) suggested that 15 % replacement of 2.3. Analysis of growth, feed utilization, and survival rate
FM protein with SBM did not have any significant difference in
the growth of H. fossilis when compared with 100 % FM- After 14 weeks, data were recorded for the quantity and total
containing diet. Therefore, there had been a possibility of replacing weight of fish in each tank. Individual length (cm) and weight (g)
FM protein with SBM in diets of H. fossilis fry more than 15 %. were measured by randomly collecting fifteen (15) fishes. The
Pervin et al. (2020) reported that 75 % substitution of FM by SBM growth parameters such as weight gain (g), percent weight gain
showed no substantial changes in the growth and physiology (%), and specific growth rate (% day
1), feed utilization parameters
of Oreochromis niloticus. Moreover, Mohammadinafchi et al. such as feed conversion ratio and protein efficiency ratio, and sur-
(2014) reported no considerable variations in Mesopotamichthys vival (%) of H. fossilis were measured with the noted data are as
sharpeyi when the replacement level was 100 %. However, the follows.
effects of the replacement of FM protein with SBM on growth per-
formance and physiology of stinging catfish have not been well-  Weight gain (g) = Mean final weight – Mean initial weight
documented. Moreover, due to the presence of lower content of  Percent weight gain (%) = ðMean final weight - Mean initial weightÞ
 100
Mean initial weight
methionine and higher content of anti-nutrients, there is a limita-
 Specific growth rate (% day
1) = ðLoge W 2 - Loge W1 Þ
 100
tion to using SBM as fish feed (Ollie et al., 1994). Besides, SBM may ðT2 - T1 Þ
fed ðdry weightÞ
be a cost-effective and highly available alternative protein source  Feed conversion ratio (FCR) =Feed
Live weight gain ðgÞ
to replace costly fish meal in aquaculture. Therefore, the present Live weight gain ðgÞ
 Protein efficiency ratio (PER) =Crude protein fed ðgÞ
study was projected to investigate the effects of replacing FM pro-
tein with SBM at different substitution levels on growth, feed effi-  Survival (%) = Total number of fish harvested
Total number of fish stocked
 100
ciency, and health condition of stinging catfish.
2.4. Proximate composition analysis

2. Materials and methods The proximate composition of feed ingredients, feed, and
whole-body carcass from each treatment was analyzed following
2.1. Preparation of diets methods described by AOAC (2000) with little modifications. Trip-
licate samples were used to analyze the moisture, protein, lipid,
Available fresh feed ingredients were used to formulate four ash, and fibre on percent basis (%). Carbohydrate was estimated
isonitrogenous (35 % crude protein) diets where 0 %, 25 %, 50 %, by deducting the total percentages of analyzed compositions from
and 75 % of FM protein were substituted by SBM in SBM0, SBM25, 100 (Castell and Tiews, 1980). The values of crude protein, fat, and
SBM50, and SBM75 groups, respectively. The formulation and prox- carbohydrate were used to calculate the calorific value of the feeds
imate composition of different diets are presented in Table 1. Dry (Jauncey and Ross, 1982).
feedstuffs were first ground with a crusher machine for diet prepa-
ration. After sieving ground ingredients, all ingredients were thor- 2.5. Hemato-biochemical analysis
oughly mixed and added distilled water at 30 % level (El-Saidy and
Gaber, 1997). Pellets were made for all experimental diets with a The value of hemoglobin (Hb), red blood cells (RBCs), white
pellet machine. After that processed pellets (1.0 mm size) were blood cells (WBCs), and blood glucose (Glu) of stinging catfish were
oven dried at 55 °C and refrigerated at 4 °C until further use determined as g/dL, 106 /mm3, 103 /mm3, and mg/dL, respec-
(Yang et al., 2004). tively as per the methods described by Billah et al. (2022).

2.2. Feeding trials 2.6. Histological examination

The experimental fish (H. fossilis) was gathered from a After 14 weeks, two randomly selected H. fossilis were used for
renowned hatchery in the Jashore division of Bangladesh named each treatment to perform morphological analysis of the intestine
‘‘Maa Fatima Hatchery”. Six hundred fingerlings of H. fossilis (aver- as per the procedures followed by Billah et al. (2022). The follow-
age size 1.55 ± 0.00 g fish
1) were stocked in twelve plastic tanks ing morphological parameters as villus length (lm), villus width
(150 L capacity each) under four groups with three replications (lm), villus area (mm2), crypt depth (lm), thickness of the intesti-
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S. Howlader, K.R. Sumi, S. Sarkar et al. Saudi Journal of Biological Sciences 30 (2023) 103601

Table 1
Ingredients and nutrient composition of experimental diets fed to H. fossilis.

Ingredients (g 100 g
1) Diets

SBM0 SBM25 SBM50 SBM75
a
Fish meal 46.23 34.68 23.11 11.57
b
Soybean meal 0.00 17.85 35.68 53.53
Mustard oil cake 15.34 19.72 24.49 28.77
Rice bran 15.17 9.14 7.24 0.60
Wheat bran 18.29 13.63 4.52 0.58
*Premix 1.00 1.00 1.00 1.00
Molasses 4.00 4.00 4.00 4.00
Nutrient composition (%)
Moisture 12.85 12.82 13.64 14.36
Crude protein 35.57 35.54 35.04 35.23
Crude lipid 7.87 7.34 7.56 7.33
Ash 13.38 13.04 10.42 8.54
Crude fibre 4.20 4.36 5.13 5.34
Nitrogen free extract 26.13 26.90 28.21 29.20
Energy (kcal/g) 3.81 3.80 3.84 3.87

*Premix supplied the following vitamins and minerals (mg or g or IU/2.5 kg of diet): A, 12,500 IU; B1, 2.5 g; B2, 5 g; B6, 4 g; B12, 12 mg; D3, 2,500,000 IU; E, 20 g; K3, 4 g;
Nicotinic acid, 12.5 g; Folic acid, 800 mg; Biotin, 100 mg; Cobalt, 400 mg; Copper, 10 g; Iron, 60 g; Iodine, 400 mg; Manganese, 60 g; Zinc, 50 g; Selenium, 150 g.
a
Fish meal (56.46 % crude protein), supplied by Blueline Foods (India) Pvt. ltd.
b
Soybean meal (36.58 % crude protein), supplied by Fresh, Meghna Group of Industries (Narayanganj, Bangladesh).

nal wall (lm), abundance of goblet cell (GB), and thickness of mus- 3.2. Proximate composition of experimental fish
cle (lm) were determined for this experiment.
The proximate composition of the whole-body carcass is pre-
sented in Table 3. The significantly higher moisture content (%)
2.7. Statistical analysis was found in SBM25 and SBM50 groups and it was significantly
lower in SBM0 and SBM75 groups (P < 0.05). However, a reverse
A statistical comparison of data obtained from the proposed condition was observed in case of lipid content (%). The protein
study was made with SPSS software. The normality and homogene- content (%) was significantly higher in SBM25 group compared to
ity of variances of data were confirmed before any statistical anal- other groups (P < 0.05) and significantly lower protein content
ysis. ANOVA (one-way analysis of variance) was applied to observe (P < 0.05) was found in SBM0 group (Table 3). While significantly
significant variations (P < 0.05) among diets. Presentation of data higher content of ash (%) was found in the SBM50 group and lower
was done as mean ± SE (standard error). Moreover, the Tukey test in the SBM25 group (P < 0.05) (Table 3). No significant difference
was selected for detecting variations between diets. was observed in crude fibre (P > 0.05) content (%) of whole-body
carcass among different groups (Table 3). Nitrogen-free extract
was found significantly higher in SBM0, SBM25, and SBM75 groups
3. Results and significantly lower in SBM50 group (P < 0.05).

3.1. Growth performance, feed utilization and survival

3.3. Hemato-biochemical study
After 14-week feeding trials, the performance of growth, utiliza-
tion of feed, and survival of H. fossilis were calculated (Table 2). Sig- Hemato-biochemical analysis of stinging catfish for instance
nificantly (P < 0.05) higher mean final weight (g), weight gain (g), hemoglobin (Hb), red blood cells (RBCs), white blood cells (WBCs),
percent weight gain (%), specific growth rate (% day
1), and protein and blood glucose (Glu) were calculated for all the fish groups
efficiency ratio (PER) was recorded in SBM0, SBM25, and SBM50 (Table 4). The SBM0, SBM25, and SBM50 groups showed significantly
groups than SBM75 group. The FCR values were significantly higher content of Hb, RBCs, and WBCs, however, the SBM75 group
(P < 0.05) lower in SBM0, SBM25, and SBM50 groups compared to detected significantly lower values of these blood parameters
SBM75 group. Moreover, there were no significant variations (P < 0.05). Moreover, glucose showed significantly higher and
(P > 0.05) in the survival rate of H. fossilis among different feeding lower (P < 0.05) values in the SBM75 and SBM0 groups, respectively
groups (Table 2). than in other groups (Table 4).

Table 2
Growth and feed utilization of H. fossilis fed different experimental diets (mean ± SE).

Parameters Diets
SBM0 SBM25 SBM50 SBM75
Initial weight (g) 1.55 ± 0.00 1.55 ± 0.00 1.55 ± 0.00 1.55 ± 0.00
Final weight (g) 8.91 ± 0.64a 8.33 ± 0.28a 8.28 ± 0.05a 6.10 ± 0.25b
Weight gain (g) 7.36 ± 0.64a 6.78 ± 0.28a 6.73 ± 0.05a 4.55 ± 0.25b
Percent weight gain (%) 475.05 ± 41.63a 437.38 ± 18.41a 433.91 ± 3.59a 293.55 ± 16.13b
Specific growth rate (% day
1) 1.74 ± 0.07a 1.67 ± 0.03a 1.66 ± 0.01a 1.36 ± 0.04b
Feed conversion ratio (FCR) 3.15 ± 0.7b 3.29 ± 0.08b 3.03 ± 0.07b 3.87 ± 0.06a
Protein efficiency ratio (PER) 0.77 ± 0.01a 0.76 ± 0.02a 0.76 ± 0.01a 0.58 ± 0.01b
Survival (%) 97.63 ± 0.63 94.50 ± 3.50 96.80 ± 0.58 95.61 ± 2.64

The values in the same row that are followed by the different superscript letters are significantly different (P < 0.05).

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S. Howlader, K.R. Sumi, S. Sarkar et al. Saudi Journal of Biological Sciences 30 (2023) 103601

Table 3
Proximate composition of H. fossilis fed different experimental diets (mean ± SE).

Proximate composition (%) Diets

SBM0 SBM25 SBM50 SBM75
Moisture 76.11 ± 0.12b 76.60 ± 0.02a 76.70 ± 0.05a 76.00 ± 0.01b
Crude protein 14.44 ± 0.01c 14.91 ± 0.10a 14.61 ± 0.01bc 14.81 ± 0.02ab
Crude lipid 2.13 ± 0.02a 1.98 ± 0.03b 1.88 ± 0.01b 2.15 ± 0.02a
Ash 2.69 ± 0.06b 2.23 ± 0.02d 3.15 ± 0.01a 2.47 ± 0.03c
Crude fibre 0.90 ± 0.20 1.12 ± 0.01 1.13 ± 0.01 0.96 ± 0.17
Nitrogen free extract 3.73 ± 0.06a 3.16 ± 0.19a 2.53 ± 0.01b 3.61 ± 0.02a

The values in the same row that are followed by the different superscript letters are significantly different (P < 0.05).

Table 4
Hemato-biochemical parameters of H. fossilis fed different experimental diets (mean ± SE).

Blood parameters Diets

SBM0 SBM25 SBM50 SBM75
Hb (g/dL) 12.33 ± 0.03a 12.25 ± 0.01a 12.23 ± 0.03a 10.38 ± 0.03b
RBC (106 / mm3) 1.33 ± 0.02a 1.31 ± 0.04a 1.32 ± 0.03a 1.09 ± 0.01b
WBC (103 / mm3) 1.60 ± 0.02a 1.59 ± 0.07a 1.62 ± 0.01a 1.25 ± 0.02b
Glucose (mg/ dL) 52.22 ± 0.04d 54.00 ± 0.04c 57.5 ± 0.07b 72.00 ± 0.03a

The values in the same row that are followed by the different superscript letters are significantly different (P < 0.05).

3.4. Histological study SBM upto 40 % in the diet of Pseudobagras ussuriensis had no
negative effects on growth, while best feed utilization was
The intestinal histo-morphological measurements of H. fossilis obtained upto 50 % substitution level. Conversely, in this present
such as length (lm), width (lm), and area of the villi (mm2), crypt study, upto 50 % replacement level showed better growth perfor-
depth (lm), thickness of wall (lm), abundance of goblet cell (GB), mance and this replacement level was somewhat lower than other
and thickness of muscle (lm) are presented in Table 5 and Fig. 1. studies for instance blue catfish (Webster et al., 1995) and rainbow
The values of these parameters varied significantly (P < 0.05) trout (Yang et al., 2011), where 60 % of FM protein can be substi-
among the SBM0, SBM25, SBM50, and SBM75 groups. The increasing tuted with SBM without compromising growth. These differences
trend of histological parameters was observed with increasing vary from species to species, size, types of ingredients and process
dietary soybean meal and it continued upto 50 % replacement level of formulation, inclusion and value of SBM, and different culture
and then declined to 75 %. The examined values of histo- systems (Wang et al., 2015). Shukla et al. (2018) suggested that
morphological parameters were significantly (P < 0.05) higher in 100 % substitution of FM protein with SBM improved growth per-
the SBM50 group. An importantly similar tendency was detected formance in H. fossilis when the protein content of the FM (23.76 %)
also in the case of the number of goblet cells (immune response was less than SBM (37.83 %), which means that the deteriorative
variable). quality of the fish meal. In this present study, the protein content
of FM was higher (56.46 %) than SBM (36.58 %).
At large, FM can be partly substituted by SBM without hamper-
4. Discussion ing development in some aquatic animals. In this study, 75 %
replacement of FM protein with SBM decreased the growth of sting-
The growth performance of stinging catfish, H. fossilis was sig- ing catfish. Liu et al. (2021) showed that SBM above 75 % in the diet
nificantly higher in SBM0, SBM25, and SBM50 groups compared to of Liza haematocheila reduced the growth and feed efficiency. Simi-
SBM75. Moreover, efficient feed utilization was also found in lar reports were also suggested by Yang et al. (2011), where 80 %
SBM0, SBM25, and SBM50 groups than SBM75 group. This means that dietary inclusion level of SBM significantly reduced the growth of
replacement of FM protein with SBM upto 50 % did not show any Oncorhynchus mykiss. Diet containing SBM protein reduce growth
significant difference in growth and feed utilization. Liu et al. and feed efficiency because of the existence of anti-nutrients, bitter
(2021) reported that SBM can replace upto 50 % of fish meal in taste, lower digestibility of protein, scarcity of essential amino acid
juvenile Liza haematocheila based on weight gain and feed effi- (Francis et al., 2001; Wang et al., 2006; Yang et al., 2011). In the pre-
ciency. Wang et al. (2015) reported substitution of FM protein with sent study, the reduced growth rate of stinging catfish found from

Table 5
Changes in intestinal morphology of H. fossilis fed different experimental diets (mean ± SE).

Parameters Diets
SBM0 SBM25 SBM50 SBM75
Villus length (lm) 97.0 ± 6.24b 101.02 ± 4.06b 147.30 ± 6.40a 91.55 ± 3.10b
Villus width (lm) 62.67 ± 3.90b 73.33 ± 5.07ab 96.67 ± 4.53a 64.36 ± 2.20b
Villus area (mm2) 7.75 ± 0.39b 10.87 ± 1.26ab 14.68 ± 1.57a 8.02 ± 0.41b
Crypt depth (lm) 22.67 ± 3.73ab 23.33 ± 1.33ab 34.67 ± 1.32a 21.38 ± 0.74b
Thickness of wall (lm) 9.00 ± 0.84b 10.33 ± 1.13b 18.00 ± 1.85a 9.09 ± 0.73b
Abundance of goblet cell (GB) 71.30 ± 3.25b 90.00 ± 6.70ab 112.00 ± 7.00a 78.09 ± 1.78b
Thickness of muscle (lm) 5.09 ± 0.08c 8.10 ± 0.03b 13.86 ± 0.85a 7.00 ± 0.30bc

The values in the same row that are followed by the different superscript letters are significantly different (P < 0.05).

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S. Howlader, K.R. Sumi, S. Sarkar et al. Saudi Journal of Biological Sciences 30 (2023) 103601

Fig. 1. Histological changes of the intestine of H. fossilis fed different experimental diets for 14 weeks; (a) control (SBM0) diet, (b) GC = Goblet cell, (c) VA = Villus area,
VL = Villus length, VW = Villus width, (d) CD = Crypt depth, TW = Thickness of wall, TM = Thickness of muscle.

high soybean meal-containing diet (SBM75) could be due to their Hemato-biochemical studies are commonly used for the evalu-
morphological and physiological variations for diets high in animal ation of different physical conditions of fish (Pradhan et al., 2012;
protein. Moreover, the FCR values of this present study were slightly Sharmin et al., 2016; Jahan et al., 2019; Billah et al., 2022). In this
higher because of the culture systems and removal of uneaten feeds. present experiment, there was no significant variation observed in
At times, leftover feeds were not possible to collect because of sus- Hb, RBCs, and WBCs upto 50 % replacement of FM protein by soy-
pension in water, and this situation leads to excess feeding. While, bean meal in diets and then there was a decreasing trend of these
in the nutritional study, the supply of feed should be smooth values at 75 % replacement level. Dawood et al. (2015) obtained Hb
enough, therefore overfeeding is better than underfeeding (Tacon and Glu levels of 10.7 to 12.5 g/dL and 68 to 97.3 mg/dL, respec-
and Cowey, 1985). Billah et al. (2022) reported the FCR values of tively in Amberjack juveniles fed 0 to 45 % soybean meal-
stinging catfish 3.55 to 4.35 when FM protein was totally replaced containing diets. The increasing level of Hb in fish blood may have
by SBM. In this study, the survival rate found around 94 to 98 % is had better oxygen transport in tissues leading to improved growth
similar to the results of 92 to 100 % reported by Liu et al. (2021), (Esmaeili, 2021; Hossain et al., 2022). Hosseini and Khajepour
where FM protein was replaced with various percentages of soy- (2013) reported that a higher level of replacement of FM protein
bean meal protein. by soybean meal lowers the value of Hb, RBC, and WBC in beluga.
Substitution of FM protein with SBM in diets of H. fossilis af- In this study, the blood glucose level was reversed with blood
fected the values of whole-body carcass composition such as mois- hemoglobin. Moreover, in this study, the higher the replacement
ture, crude protein, crude lipid, ash, crude fibre, and nitrogen-free of FM protein by soybean meal in diets higher the values of glucose
extract. Comparable results were also reported in Ussuri catfish in stinging catfish. Parallel reports were also stated by Liu et al.
(Wang et al., 2015), Nile tilapia (Ajani et al., 2016), and European (2021) in juvenile redlip mullet and Hosseini and Khajepour
seabass (Kaushik et al., 2004). While some other studies showed (2013) in beluga. Previous reports suggested that the hematology
that the replacement of FM protein with SBM in diets did not affect of fish varies on fish species, size, physical and environmental con-
the proximate composition of rainbow trout (Yang et al., 2011) and ditions, feed ingredients and formulation, source of quality protein,
European sea bass (Tibaldi et al., 2006). In this study, significantly vitamins, and probiotics (Osuigwe et al., 2005).
higher and lower whole-body carcass protein was found in the The morphological changes in the intestine have been observed
SBM25 and SBM0 groups, respectively. However, lipid content was in some fish species owing to the inclusion of SBM in the diets
significantly higher in SBM0 and SBM75 groups than in other (Shiu et al., 2015; Garcia-Ortega et al., 2016). The present study
groups. Moreover, moisture and lipid content also showed reverse showed that the dietary replacement of FM protein with SBM upto
conditions. 50 % increased intestinal shape with increasing the histo-

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S. Howlader, K.R. Sumi, S. Sarkar et al. Saudi Journal of Biological Sciences 30 (2023) 103601

morphological factors of the intestine and then decline to 75 % Billah, S.M., Sumi, K.R., Howlader, S., Sarkar, S., Ferdous, Z., Islam, S.M., Shahjahan,
M., 2022. Effects of supplemental L-methionine for total replacement of fish
replacement level. Increased intestinal shape (villus length, width,
meal by soybean meal on growth, feed utilisation and health status of stinging
area, and thickness) designates the evaginations of the intestinal catfish, Heteropneustes fossilis fry. Aquacult. Fish Fish., 1–9
mucosa, which increases the absorption of intestinal nutrients Castell, J.D., K. Tiews (eds.), 1980. Report of the EIFAC, IUNS and ICES working group
and improves fish growth performance and feed consumption on standardization of methodology in fish nutrition research. EIFAC Technical
Paper 36, Hamburg, Federal Republic of Germany, 21-23 March, 1979. 24 pp.
(Ferguson et al., 2010; Pirarat et al., 2011; Khojasteh, 2012; Jahan Dawood, M.A., Koshio, S., Ishikawa, M., Yokoyama, S., 2015. Effects of partial
et al., 2021; Islam et al., 2021). In general, plant feedstuff contains substitution of fish meal by soybean meal with or without heat-killed
cellulose (plant fiber), which is digested by cellulase produced by Lactobacillus plantarum (LP20) on growth performance, digestibility, and
immune response of amberjack. Seriola dumerili juveniles, BioMed Res. Int.,
the gut bacteria of many fish species such as chitinase in crus- p. 2015.
taceans. Moreover, herbivorous and some omnivorous fishes are El-Saidy, D.M.S., Gaber, M.M.A., 1997. Total replacement of fish meal by soybean
more able to digest cellulose than carnivorous fishes. For this rea- meal, with various percentages of supplemental L-methionine, in diets for Nile
tilapia, Oreochromis niloticus fry. Ann. Agric. Sci. Moshtohor 35, 1223–1238.
son, in this present study, the shape of the intestine was increased Esmaeili, M., 2021. Blood performance: a new formula for fish growth and health.
by replacing FM protein with SBM upto 50 % in the diet. Further Biology (Basel) 10, 1–17.
replacing of SBM in the diet reduced the intestinal shape of sting- Ferguson, R.M.W., Merrifield, D.L., Harper, G.M., Rawling, M.D., Mustafa, S.,
Picchietti, S., Balcázar, J.L., Davies, S.J., 2010. The effect of Pediococcus
ing catfish. Comparable effects were also described in orange- acidilactici on the gut microbiota and immune status of on-growing red
spotted grouper (Wang et al., 2017) and Japanese seabass (Zhang tilapia (Oreochromis niloticus). J. Appl. Microbiol. 109, 851–862.
et al., 2018). In this study, the abundance of goblet cells increased Francis, G., Makkar, H.P.S., Becker, K., 2001. Antinutritional factors present in plant-
derived alternate fish feed ingredients and their effects in fish. Aquaculture 199,
by substituting FM protein with SBM upto 50 % level, which is
197–227.
responsible for the production of mucus that provides gel coating Garcia-Ortega, A., Kissinger, K.R., Trushenski, J.T., 2016. Evaluation of fish meal and
over the surface layer of epithelium and defends from bacterial fish oil replacement by soybean protein andalgal meal from schizochytrium
invasion (Johansson et al., 2008). limacinum in diets for giant grouper Epinephelus lanceolatus. Aquaculture 452,
1–8.
Based on the results it was suggested that SBM could replace Haniffa, M.A., Sridhar, S., 2002. Induced spawning of spotted murrel (Channa
upto 50 % FM protein in diets of H. fossilis without compromising punctatus) and catfish (Heteropneustes fossilis) using human chorionic
growth, feed efficiency, and health status. More studies should be gonadotropin and synthetic hormone (ovaprim). Vet. Arhiv 72, 51–56.
Hossain, M.M., Ali, M.L., Khan, S., Haque, M.M., Shahjahan, M., 2020a. Use of Asian
carried out in production trials for a longer duration on H. fossilis watergrass as feed of grass carp. Aquacult. Rep. 18, 100434.
by using 50 % replacement of FM protein with SBM in the diet. Hossain, M.K., Hossain, M.M., Mim, Z.T., Khatun, H., Hossain, M.T., Shahjahan, M.,
2022. Multi-species probiotics improve growth, intestinal microbiota and
morphology of Indian major carp mrigal Cirrhinus cirrhosus. Saudi J. Biol. Sci.
Author contributions 9, 103399.
Hossain, M.M., Rahman, M.H., Ali, M.L., Khan, S., Haque, M.M., Shahjahan, M., 2020b.
Development of a low-cost polyculture system utilizing Hygroryza aristata
Sumon Howlader experimented, collected, and tabulated the
floating grass in the coastal wetlands of Bangladesh. Aquaculture 527, 735430.
data; Kanij Rukshana Sumi planned the study, designed, super- Hosseini, S.A., Khajepour, F., 2013. Effect of partial replacement of dietary fish meal
vised, analyzed data, and wrote the manuscript; Subroto Sarkar with soybean meal on some hematological and serum biochemical parameters
and Sheikh Masum Billah assisted Sumon Howlader in conducting of juvenile beluga, Huso huso. Iran. J. Fish. Sci. 12 (2), 348–356.
Islam, S.M.M., Rohani, M.F., Shahjahan, M., 2021. Probiotic yeast enhances growth
the experiments and data collection; Mohammad Lokman Ali performance of Nile tilapia (Oreochromis niloticus) through morphological
assisted Sumon Howlader to conduct the experiments and revised modifications of intestine. Aquac. Reports 21, 100800.
the manuscript; Md. Shahjahan facilitated the laboratory to ana- Jahan, N., Islam, S.M.M., Rohani, M.F., Hossain, M.T., Shahjahan, M., 2021. Probiotic
yeast enhances growth performance of rohu (Labeo rohita) through upgrading
lyze histology and hematology and edited the manuscript; Jewel hematology, and intestinal microbiota and morphology. Aquaculture 545,
Howlader helped in data analysis and revised the manuscript; All 737243.
authors read and approved the final manuscript. Jahan, A., Nipa, T.T., Islam, S.M., Uddin, M.H., Islam, M.S., Shahjahan, M., 2019.
Striped catfish (Pangasianodon hypophthalmus) could be suitable for coastal
aquaculture. J. Appl. Ichthyol. 35 (4), 994–1003.
Declaration of Competing Interest Jauncey, K., Ross, B., 1982. A guide to tilapia feeds and feeding. University of Stirling,
Stirling, Institute of Aquaculture.
Jhingran, V.G., 1991. Nutrition of cultivated fishes. In: Jhingran, V.G. (Ed.), Fish and
The authors declare that they have no known competing finan-
Fisheries of India. Hindustan published corporation, Delhi, India, pp. 572–576.
cial interests or personal relationships that could have appeared Johansson, M.E., Phillipson, M., Petersson, J., Velcich, A., Holm, L., Hansson, G.C.,
to influence the work reported in this paper. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is
devoid of bacteria. Proc. Natl. Acad. Sci. U.S.A. 105 (39), 15064–15069.
Kalla, A., Garg, S.K., Kaushik, C.P., Arasu, A.R.T., Dinodia, G.S., 2003. Effect of
Acknowledgement replacement of fishmeal with processed soybean on growth, digestibility and
nutrient retention in Mugil cephalus (Linn.) fry. Indian J. Fish. 50 (4), 509–518.
This research work was supported by the Research and Training Kaushik, S.J., Cove‘s, D., Dutto, G., Blanc, D., 2004. Almost total replacement of
fishmeal by plant protein sources in the diet of a marine teleost, the European
Centre (Grant no. 5921, Fish-1 and 4829, Fish-90), Patuakhali seabass, Dicentrarchus labrax. Aquaculture 230, 391–404.
Science and Technology University. Khojasteh, S.M.B., Mahdi, S., Khojasteh, B., 2012. The morphology of the post-gastric
alimentary canal in teleost fishes: a brief review. Int. J. Aquat. Sci. 3, 2008–8019.
Liu, T., Han, T., Wang, J., Liu, T., Bian, P., Wang, Y., Cai, X., 2021. Effects of replacing
fish meal with soybean meal on growth performance, feed utilization and
References physiological status of juvenile redlip mullet Liza haematocheila. Aquac. Rep. 20,
100756.
Meng, F., Li, B., Xie, Y., Li, M., Wang, R.X., 2020. Substituting fishmeal with extruded
Ajani, E.K., Orisasona, O., Omitoyin, B.O., Osho, E.F., 2016. Total replacement of
soybean meal in diets did not affect the growth performance, hepatic enzyme
fishmeal by soybean meal with or without methionine fortification in the diets
activities, but hypoxia tolerance of Dolly Varden (Salvelinus malma) juveniles.
of Nile tilapia, Oreochromis niloticus. J. Fish. Aquat. Sci. 11 (3), 238–243.
Aquac. Res. 51 (1), 379–388.
Alam, M.S., Jahan, M., Hossain, M.M., Islam, M.S., 2009. Population genetic structure
Mohammadinafchi, F., Mohammadiazarm, H., Yavari, V., 2014. Evaluation effect of
of three major river populations of rohu, Labeo rohita (Cyprinidae;
soybean meal and baker’syeast on resistance to anoxia stress and blood
Cypriniformes) using icrosatellite DNA markers. Genes Genom. 31, 43–51.
biochemical parameters of fingerlings (Mesopotamichthys sharpeyi Günther,
Anon, 1982. Pakistan National Report. In: Spagnesi, M. (ed.), Proc. Conference on
1874). Int. J. Biosci. 5 (8), 215–222.
Conservation of Wetlands of International Importance especially as Waterfowl
Nyirenda, J., Mwabumba, M., Kaunda, E., Sales, J., 2000. Effect of substituting animal
Habitat, cagliari, Italy, 24–29 November 1980. Suppl. Richerche di Biologia della
protein sources with soybean meal in diets of Oncorhynchus karongae (Trewavas
Selvaggina, VIII 1, 893–905
1941). Naga, The ICLARM Quarterly, Volume 23, No. 4, October-December.
AOAC, 2000. Official methods of Analysis, 17th ed. Association of Official Analytical
Ollie, J.J., Krogdahl, A., Hjelmeland, K., 1994. Soybean trypsin inhibitors in diets for
Chemist, Washington DC, pp. 2200
Atlantic salmon (Slmo salar) effects on nutrient digestibilities and trypsin in
Bhatt, V.S., 1968. Studies on the biology of some fresh water fishes. part -Vll. H.
fossilis (Bloch). Indian J. Fish. 15, 99–115.

6
S. Howlader, K.R. Sumi, S. Sarkar et al. Saudi Journal of Biological Sciences 30 (2023) 103601

pyloric caeca homogenate and intestinal content. Comp. Biochem. Physiol. A Thakur, N.K., 1991. Possibilities and problem of catfish culture in India. J. Inland
109, 923–928. Fish. Soc. India 23, 80–90.
Osuigwe, D.I., Obiekezie, A.I., Onuoha, G.C., 2005. Some haematological changes in Tibaldi, E., Hakim, Y., Uni, Z., Tulli, F., de Francesco, M., Luzzana, U., Harpaz, S., 2006.
hybrid catfish (Heterobranchus longifilis  Clarias gariepinus) fed different Effects of the partial substitution of dietary fish meal by differently processed
dietary levels of raw and boiled jackbean (Canavalia ensiformis) seed meal. Afr. J. soybean meals on growth performance, nutrient digestibility and activity of
Biotechnol. 4, 1017–1021. intestinal brush border enzymes in the European sea bass (Dicentrarchus
Pervin, M.A., Jahan, H., Akter, R., Omri, A., Hossain, Z., 2020. Appraisal of different labrax). Aquaculture 261, 182–193.
levels of soybean meal in diets on growth, digestive enzyme activity, Uddin, M.N., Rahman, Shahjahan, M., 2007. Effects of duckweed (Lemna minor) as
antioxidation, and gut histology of tilapia (Oreochromis niloticus). Fish supplementary feed on monoculture of gift strain of tilapia (Oreochromis
Physiol. Biochem. 46 (4), 1397–1407. niloticus). Progress. Agric. 18, 183–188
Pirarat, N., Pinpimai, K., Endo, M., Katagiri, T., Ponpornpisit, A., Chansue, N., Maita, Wang, Y., Kong, L.J., Li, C., Bureau, D.P., 2006. Effect of replacing fish meal with
M., 2011. Modulation of intestinal morphology and immunity in nile tilapia soybean meal on growth, feed utilization and carcass composition of cuneate
(Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res. Vet. Sci. 91, e92– drum (Nibea miichthioides). Aquaculture 261, 1307–1313.
e97. Wang, Y.R., Wang, L., Zhang, C.X., Song, K., 2017. Effects of substituting fishmeal
Pradhan, S.C., Patra, A.K., Sarkar, B., Pal, A., 2012. Seasonal changes in hematological with soybean meal on growth performance and intestinal morphology in
parameters of Catla catla (Hamilton 1822). Comp. Clin. Path. 21 (6), 1473–1481. orange-spotted grouper (Epinephelus coioides). Aquac, Rep. 5, 52–57.
Radhakrishnan, M.V., Sugumaran, E., 2010. Effect of sugarcane bagasse and Wang, Y., Yu, S., Wang, Y., Che, J., Zhao, L., Bu, X., Yang, Y., 2015. Effect of replacing
supplemental feed on certain reproductive characteristics of the catfish fish meal with soybean meal on growth, feed utilization and nitrogen and
Heteropneutes fossilis (Bloch). J. Fish. Int. 5 (4), 58–60. phosphorus excretion of juvenile Pseudobagrus ussuriensis. Aquac. Res. 47 (10),
Robinson, E.H., Li, M.H., 2007. Catfish Protein Nutrition (Revised). Bulletin 1153. 3145–3155.
office of Agricultural Communications. Mississippi State University, USA. Webster, C.D., Goodgame-Tiu, L.S., Tidwell, J.H., 1995. Total replacement fish meal
Sharmin, S., Salam, M.A., Haque, F., Islam, M.S., Shahjahan, M., 2016. Changes in by soybean meal, with various percentages of supplemental L-methionine, in
hematological parameters and gill morphology in common carp exposed to fish diets for blue catfish, Ictalurus furcatus (Leseur). Aquac. Res. 26, 299–306.
sub-lethal concentrations of malathion. Asian J. Med. Biol. Res. 2 (3), 370–378. Yang, Y.H., Wang, Y.Y., Lu, Y., Li, Q.Z., 2011. Effect of replacing fish meal with
Shiu, Y.L., Hsieh, S.L., Guei, W.C., Tsai, Y.T., Chiu, C.H., Liu, C.H., 2015. Using bacillus soybean meal on growth, feed utilization and nitrogen and phosphorus
subtilis e20-fermented soybean meal as replacement for fish meal in the diet of excretion on rainbow trout (Oncorhynchus mykiss). Aquac. Int. 19, 405–419.
orange-spotted grouper (Epinephelus coioides, Hamilton). Aquacult. Res. 46 (6), Yang, Y., Xie, S., Cui, Y., Lei, W., Zhu, X., Yang, Y., Yu, Y., 2004. Effect of replacement of
1403–1416. dietary fish meal by meat and bone meal and poultry by-product meal on
Shukla, A., Kaur, V.I., Kumar, P., Ansal, M.D., Dhawan, A., Mishra, V., 2018. Utilization growth and feed utilization of gibel carp. Carassius auratus gibelio. Aquac. Nutr.
of dietary soybean meal and groundnut meal as fish meal replacement in 10 (5), 289–294.
Heteropnuestes fossilis (Bloch.). Int. J. Curr. Microbiol. App. Sci. 7 (6), 734–746. Zhang, C., Rahimnejad, S., Wang, Y.R., Lu, K., Song, K., Wang, L., Mai, K., 2018.
Tacon, A.G.J., Jackson, A.J., 1985. Utilization of conventional and unconventional Substituting fish meal with soybean meal in diets for Japanese seabass
protein sources in practical fish feeds, in: Cowey, C.B., Mackie, A.M., Bell, J.G. (Lateolabrax japonicus): Effects on growth, digestive enzymes activity, gut
(Eds.), Nutrition and Feeding of Fish. Academic Press, London, UK, pp. 119–145. histology, and expression of gut inflammatory and transporter genes.
Tacon, A.G., Cowey, C.B., 1985. Protein and amino acid requirements. In: Tytler, P., Aquaculture 483, 173–182.
Calow, P. (Eds.), Fish Energetics-New Perspectives. Croom Helm, London, pp. Zhou, Z., Ringø, E., Olsen, R.E., Song, S.K., 2018. Dietary effects of soybean products
155–183. on gut microbiota and immunity of aquatic animals: a review. Aquac. Nutr. 24,
644–665.