Aquaculture and Fisheries 9 (2024) 46–51

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Aquaculture and Fisheries

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Evaluation of growth performance, feed efficiency and nutrient digestibility

of red hybrid tilapia fed dietary inclusion of black soldier fly larvae
(Hermetia illucens)
Hasniyati Muin a, Norhidayah Mohd Taufek a, b, *
a
Aqua-Nutri Biotech Laboratory, Institute of Biological Sciences, Universiti Malaya, Kuala Lumpur, 50603, Malaysia
b
Ladang Mini, Institute of Biological Sciences, Faculty of Science, Universiti Malaya, Kuala Lumpur, 50603, Malaysia

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

Keywords: Insects, particularly black soldier fly larvae (BSFM), Hermetia illucens, have been regarded as promising protein
Insect meal and lipid sources in animal feed, including fish. Digestibility is the key factor that affects nutrient utilization,
Black soldier fly larvae feeding physiology and efficiency. In the present work, the effect of BSFM on the digestibility of red hybrid
Red hybrid tilapia
tilapia (RHT) compared to fish meal (FM) was ultimately unveiled. A 56-day growth trial was performed with 60
Digestibility
Hermetia illucens
RHT (~30 g) randomly distributed into six tanks and fed two experimental diets containing FM as a reference
diet and BSFM as a test diet. In addition, faeces were collected to determine their chromium concentration and
proximate composition. The apparent digestibility coefficient (ADC) of dry matter, crude protein and energy in
the BSFM diet were observed to be significantly higher than those in the FM diet. Besides, the growth perfor­
mance of fish fed with the BSFM diet exhibited significantly higher (P < 0.05) weight gain, specific growth rate,
protein efficiency ratio and lower feed conversion ratio than those in the FM group. This study shows that the
BSFM feed was well digested by tilapia and improved its growth performance.

1. Introduction regarded as great candidates for aquafeed ingredients.

Preliminary results have shown that BSFM is a promising protein and
Fishmeal and fish oil (FM and FO) are major aquafeed ingredients lipid source for various fishes (Belghit et al., 2018; Devic et al., 2018;
due to their excellent nutritional value manufactured from wild-caught Henry et al., 2015; Iaconisi et al., 2017; Roncarati et al., 2015; Sudha
fish. However, the market of FM and FO is being heavily exploited as et al., 2022; Zarantoniello et al., 2019). Compared to other insects,
these commodities are being traded internationally at low prices BSFM can be easily reared in limited space with numerous types of the
without meeting the minimum standard and overfishing. As a result of organic waste stream and converted into high-quality biomass within a
the imbalance supply of FM and FO in the past decades, a deliberate short time (Van Huis et al., 2015). However, there is a certain limitation
attempt to introduce alternative sustainable ingredients has gained when supplying insect meal to the fish, particularly chitin’s presence,
wider attention to reduce the dependency on FM and FO. Although the limiting their digestibility and protein utilization (Belforti et al., 2015;
production of FM and FO was reported to be stable recently, it is still Fontes et al., 2019).
unable to fulfil the huge demand of the aquaculture industry (FAO, Red hybrid tilapia is one of the commercial fishes consumed by the
2016). Asian population, particularly in Malaysia. Conventional tilapia farming
Within the animal feed industry, several species have been exten­ that relies on imported FM and FO as a food source is unsustainable and
sively studied, including black soldier fly, mealworm, silkworm, and costly, especially for the small-scale farmers in these regions. Based on
crickets, to replace the expensive and unsustainable FM and FO (Gasco our previous study, BSFM could replace 50% of FM in the tilapia diet
et al., 2016; Henry et al., 2015; Roncarati et al., 2015; Taufek et al., without adverse effects on their growth, feed efficiency and health
2017, 2021). Due to minimal environmental impact, low greenhouse (Muin et al., 2017). Therefore, this study aims to assess the growth and
emission, the proper level of the indispensable amino acid (essential) apparent digestibility in RHT fed with BSFM compared to FM.
and fatty acids, and cost-effective farming process, these insects are

* Corresponding author. Aqua-Nutri Biotech Laboratory, Institute of Biological Sciences, Universiti Malaya, Kuala Lumpur, 50603, Malaysia.
E-mail address: [email protected] (N.M. Taufek).

https://doi.org/10.1016/j.aaf.2022.09.006
Received 30 January 2022; Received in revised form 16 May 2022; Accepted 26 September 2022
Available online 12 October 2022
2468-550X/© 2022 Shanghai Ocean University. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co. Ltd. This is an open access article under
the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
H. Muin and N.M. Taufek Aquaculture and Fisheries 9 (2024) 46–51

2. Material and method Universiti Malaya, over 56 days.

Juvenile tilapia weighed 30.0 ± 1.0 g obtained from the Fisheries
2.1. Experimental diet Research Institute, Jelebu were acclimatised for 2 weeks and fed com­
mercial pellets twice per day. Before the feeding trial, the fish were
The BSFM used within this study was cultivated in the laboratory by weighed and randomly distributed into six tanks, each with 10 fish per
utilising soybean curd residue as the food source. They were harvested tank with triplicate treatments. The fish were fed twice daily at 0900 and
after 14 days of the feeding period before the prepupal stage and 1500, and the feed was given at the amount of 3% body weight (BW)
sacrificed before being oven-dried at 50 ◦ C for 24 h. Consequently, the daily during the feeding trial. Feed intake (FI) was recorded by
dried larvae were grounded into homogenous powder using the feed mill observing the uneaten feed after 15 min of feeding. The feed percentage
machine and stored at 4 ◦ C until further use. was adjusted according to BW fortnightly. Any mortality was observed
Fish feed ingredients including fishmeal soybean meal, corn meal, and recorded every day. The water was changed at a 50% rate every two
rice bran meal, dicalcium phosphate (DCP), vitamins and minerals days to maintain water quality. Dissolved oxygen (DO), pH and tem­
premixes were purchased from a local feed supplier. First, the dry in­ perature were monitored every day according to the Standard Methods
gredients were grounded to a fine powder using a hammer mill (Disk for the examination of water and wastewater (APHA 1992). The water
mill FFC 454). Next, chromic oxide (Cr2O3) (Sigma) was added to the temperature was maintained at pH 6.0 and 28.13 ± 0.15 ◦ C, DO above
diet at a 1% concentration as an inert marker. The BSFM, FM and other 4.0 mg L− 1, ammonia <1.0 mg L− 1, and nitrate <1.7 mg L− 1.
ingredients were then subjected to proximate composition and amino The faecal materials in each tank were siphoned 2 h after the feeding
acid analysis to assist in the diet formulation. session and oven-dried for 24 h at 50 ◦ C before being ground into
Two diets were formulated based on 30% crude protein (iso­ powder. Daily samples were pooled together from each tank and stored
nitrogenous) content. The reference diet (with FM as the primary pro­ at − 20 ◦ C for further analysis. The faecal samples were analysed to es­
tein source) and test diet (with BSFM as the primary protein source) timate the nutrient proximate composition and chromium
were formulated (Table 1) using WinFeed 2.8 software. All the raw in­ concentration.
gredients were homogenously mixed before being pelleted with a 1 mm
diameter using a mini pellet machine (KCM-Y123M-4) and oven-dried to
constant weight for 24 h at 60 ◦ C. The feed was then refrigerated at 4 ◦ C 2.3. Proximate and chemical analyses
for further use.
All dry ingredients, including experimental diets and faecal mate­
rials, were analysed for moisture, dry matter, protein, lipid and fibre
2.2. Experimental design content using the standard proximate analysis method (AOAC, 2003)
(Table 2). Crude protein content was determined via the Kjeldahl
A total of six plastic (4′ x 3′ x 1’) tanks filled with dechlorinated 120 L technique (FOSS Tecator Digestor Auto - Sweden). The crude lipid
water equipped with a top filter pump and oxygen supply at 25 L min− 1 content was determined by the Soxtec System (petroleum ether extrac­
flow rate were used during the feeding trial. The experiment was con­ ted). Dry matter was calculated after the weight loss due to the 24-h
ducted at the Institute of Biological Sciences, Faculty of Science, drying process at 105 ◦ C. Ash was determined after being oven-dried
at 600 ◦ C until its weight became constant. Crude fibre analysis was
Table 1 carried out using a fibre cap procedure. Chromium concentration in
Ingredients of formulated diets (g/kg) of diet and its nutrient composition. faecal materials and experimental feed were determined following the
Ingredients Reference diet (FM) Test diet (BSFM) Furukawa and Tsukahara (1966). The ADC of dry matter, protein, lipid,
Fish meal 36.56 12.27 ash and fibre in the diets were determined based on the study by
Soybean meal 30.68 13.68 Köprücü and Özdemir (2005). Chitin was estimated using the acid
Rice bran meal 15.85 19.39
Corn meal 12.91 20.66
Table 2
DCP 1 1
Premix Vitamina 1 1 Nutrient compositions and amino acids of FM and BSFM.
Premix Mineralb 1 1 Proximate composition (%) FM BSFM
Chromic oxide 1 1
BSFM 0 30 Dry Matter 86.02 93.06
Total 100 100 Ash 19.31 6.76
Nutrient content (%) Crude Protein 52.09 43.17
Dry matter 99.21 97.20 Crude Lipid 2.36 31.08
Ash 13.00 12.81 Crude Fibre 6.47 16.19
Crude protein 30.14 30.47 Chitina – 3.32
Crude lipid 9.44 12.78 NFEb 19.78 2.80
Fibre 2.89 4.85 Gross Energy (kJ/g)c 16.87 23.18
Chitinc – 1.00 Essential amino acid (% protein) Nutritional requirementd
NFEd 44.52 39.09
Gross energy(kJ/g)e 18.80 19.25 Histidine 1.66 1.00 0.48
Arginine 3.55 1.71 4.0
a
The vitamin premix supplied the following per 100g diet: Vitamin A, 500IU; Threonine 2.43 1.39 1.05
Vitamin D3, 100IU; Vitamin E, 0.75 mg; Vitamin K, 0.02 mg; Vitamin B1, 1.0 Valine 2.89 2.41 0.78
mg; Vitamin B2, 0.5 mg; Vitamin B3, 0.3 mg; Vitamin B6, 0.2 mg; Vitamin B12, Methionine 1.79 0.72 0.75
0.001 mg; Vitamin C, 0.1 mg; Niacin, 0.2 mg; Folic Acid, 0.1 mg; Biotin, 0.235 Isoleucine 2.41 1.71 0.87
mg; Pantothenic acid, 1.0 mg, Inositol, 2.5 mg. Leucine 4.03 2.70 0.95
b Phenylalanine 2.29 1.60 1.05
The mineral premix supplied the following per kg diet: Selenium, 0.2 mg;
Lysine 4.15 2.08 1.43
Iron, 8 mg; Manganese 1.0 mg; Zinc, 8.0 mg; Copper, 0.15 mg; Potassium
a
Chloride, 0.4 mg; Magnesium Oxide, 0.6 mg; Sodium Bicarbonate, 1.5 mg; Chitin (%) = ash-free ADF (%) - ADIP (%) according to Marono et al. (2015).
b
Iodine, 1.0 mg; Cobalt, 0.25 mg. NFE = 100- (% crude protein + % crude lipid + % ash+ % crude fiber).
c c
Chitin (%) = ash free ADF (%) - ADIP (%) according to Marono et al. (2015). Gross Energy was calculated as 23.9, 39.8, 17.6 kJ/g for protein, lipid and
d
NFE = 100- (% crude protein + % crude lipid + % ash+ % crude fiber). NFE, respectively (Schulz et al., 2005).
e d
Gross Energy was calculated as 23.9, 39.8, 17.6 kJ/g for protein, lipid and The Tilapia amino acid nutritional requirement, according to Santiago and
NFE, respectively (Schulz et al., 2005). Lovell (1988).

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H. Muin and N.M. Taufek Aquaculture and Fisheries 9 (2024) 46–51

detergent fibre (ADF) and protein linked to ADF (ADIP) according to depends on the quality and quantity of food ingested (Barroso et al.,
Marono et al. (2015). Nitrogen-free extract (NFE) was calculated as; 2014; Newton et al., 2005), the stage of development, and the pro­
NFE: 100% - (crude protein % + crude fat % + crude fibre % + crude ash cessing method of the larvae (Aniebo & Owen, 2010). In terms of amino
%). Meanwhile, the gross energy was calculated using the following acids, the values for BSFM were lower than FM. This is due to different
factors according to Schulz et al. (2005): crude protein = 23.9 kJ/g, protein content in both FM and BSFM, where FM has the highest protein
crude lipids = 39.8 kJ/g, and NFE = 17.6 kJ/g. compared to BSFM. Although AA values in BSFM were less than FM,
The amino acid (AA) content of the raw fish meal (FM) and BSFM Henry et al. (2015) confirm that the AA profiles of Diptera are consid­
was determined using the high-performance liquid chromatography ered close to FM.
(HPLC) with PICOTAG™ method, and the contents were analysed by
comparing the peak retention times to a known standard according to 3.2. Growth performance and feed utilization
Heinrikson and Meredith (1984).
The growth performance and feed utilization of the tilapia fed with
2.4. Analysis of the experimental data the experimental diets are shown in Table 3. All fish involved in the
experiment survived until the end of the feeding trial. Looking at the
At the end of the study, all fish from each treatment were weighed to growth parameters, fish supplemented with the BSFM diet exhibited
determine the following indices: significantly higher weight gain, SGR, and PER than those in the FM
group. On the other hand, FCR was significantly lower in those fed with
● Body weight gain (BWG) = Final weight (g) – Initial weight (g) BSFM than the FM group, which highlighted the efficiency of BSFM to
● Feed conversion ratio (FCR) = Body weight gain (g)/Feed intake (g) improve the growth performance of RHT.
● Specific growth rate (SGR) = [(ln final weight – ln initial weight)/ Numerous trials have been conducted where FM was replaced with
feeding period in days] x 100 BSFM at different inclusion levels show a positive effect on growth and
● Protein efficiency ratio (PER) = wet weight gain (g)/total protein feed utilization in different fish species (Abdel-Latif et al., 2021;
intake (g) Abdel-Tawwab et al., 2020; Alfiko et al., 2021; Belghit et al., 2019;
● Survival rate (%) = (final number of the remaining fish/initial Bondari & Sheppard, 1987; Bruni et al., 2020; Karapanagiotidis et al.,
number of fish) x 100 2014; Li et al., 2017; Magalhães et al., 2017; Rawski et al., 2020; Renna
et al., 2017; Taufek et al., 2021; Yamamoto et al., 2022). However,
The apparent digestibility coefficients (ADC) of crude protein, lipid, Kroeckel et al. (2012) reported reducing the growth of juvenile turbot
dry matter and energy in the fish were calculated as (Rahman et al., with the increasing amount of BSFM in their diet. The negative effect
2016): was recorded due to the low palatability of the diet. A similar finding
The ADC of protein, lipid and energy: was reported by Muin et al. (2017), where weight gain of red tilapia
decreased as the inclusion of BSFM increased further. The result in­
● ADC = 1 – (% dietary Cr2O3/% faecal Cr2O3 × % faecal nutrient/% dicates that red tilapia fish could optimally accept the BSFM up to 50%
dietary nutrient) inclusion level. On the other hand, a study on juvenile hybrid grouper
shows that BSFM could be incorporated at least 30% into their diet
The ADC of dry matter: without any adverse effect on growth performance(Mohamad-Zulkifli
et al., 2019).
● ADC = 100 – [100 × (% dietary Cr2O3)/(% faecal Cr2O3)]
3.3. Digestibility trial
2.5. Statistical analysis
The ADC provides information on how much of the feed was digested
Statistical analysis was performed using the SPSS version 20.0 sta­
and absorbed by the fish. Hence, the digestibility of the feed ingredients
tistical package. All data for growth performance, feed efficiency and
is the basis for assessing their bioavailability and sustainability to be
ADC were subjected to an independent t-test, and the differences were
included in fish diets (Fontes et al., 2019). In addition, the ADC of the
regarded as significantly different between the treatment groups (P <
feedstuff will help precisely formulate cost-effective feeds that satisfy
0.05). Confidence intervals were calculated as mean ± SEM (standard
fish requirements and maximize feed utilization and profit (Li et al.,
error mean) with triplicates in each treatment.
2013). However, high outcome variability was observed in fish di­
gestibility when consuming insect meals. In the current study, the ADC
3. Results and discussion
of FM and BSFM diets summarised in Table 4 demonstrated significantly
higher ADC components (protein, ash and dry matter) in BSFM except
3.1. Nutrient content of BSFM, FM and experimental diets
for lipid. In this study, the BSFM diets resulted in significantly higher
ADC protein and similar outcome was also reported by Tippayadara
The nutrient composition illustrated in Table 1 shows that both diets
are isonitrogenous (30% protein). In regard to nutrient composition,
Table 3
lipid composition in the test diet was higher (12.78%) compared to the
Growth performance and feed utilization of tilapia fed with experimental diets.
reference diet (9.44%) due to the high lipid content in the BSFM
(31.08%). The chitin content in the BSFM diet (1%) was estimated ac­ Variables Reference diet Test diet
cording to the raw BSFM composition (3.32%) after ADF analysis. In − 1)
Initial weight (g fish 31.29 ± 0.35a
30.40 ± 0.09a
general, all essential amino acids (EAA) are present in both diets and Final weight (g fish− 1) 74.57 ± 0.93a 90.92 ± 0.83b
sufficient for tilapia requirement except for arginine, which is the only Weight gain (g fish− 1) 43.28 ± 1.16a 60.52 ± 0.75b
Feed intake (g fish− 1) 105.14 ± 1.19a 102.15 ± 0.29a
EAA observed to have a lower level than the ideal amount required for SGR (%/day) 1.55 ± 0.04a 1.96 ± 0.01b
tilapia. FCR 2.43 ± 0.09a 1.69 ± 0.02b
The proximate composition in this study shows that BSFM contains PER 1.37 ± 0.05a 1.97 ± 0.02b
43.17% protein and 31.08% lipid (Table 2). This data was similar to Survival rate (%) 100a 100a
previous studies that reported that the prepupae of black soldier fly 1
The results represent means ± SEM of ten fish per tank.
contained approximately 40% protein and 30% fat (Muin et al., 2017; 2
Mean values in the same row with different superscripts are significantly
Newton et al., 2005). Generally, the nutrient composition of BSFM different (P < 0.05).

48
H. Muin and N.M. Taufek Aquaculture and Fisheries 9 (2024) 46–51

Table 4 4. Conclusion
Apparent Digestibility Coefficient (ADC %) of crude protein, crude lipid, dry
matter and gross energy of tilapia fed with the experimental diets. The results obtained in this study indicate that BSFM is well accepted
Components Reference diet Test diet by tilapia with higher nutrient digestibility than the fishmeal. Further­
Dry matter 64.85 ± 0.04a 67.89 ± 0.04b
more, the results were supported by the increase in growth of the fish
Crude protein 62.02 ± 1.28a 73.03 ± 0.14b supplied with BSFM, suggesting that the inclusion of insect meal in
Crude lipid 80.28 ± 1.55a 81.88 ± 0.73a tilapia feed will increase the palatability, nutrient availability and di­
Energy 59.76 ± 0.27a 63.38 ± 0.11b gestibility to fulfill the nutrition requirement. However, further research
Values are means ± SEM of triplicate groups of 10 fish. Mean values in the same is required to reduce the lipid composition in BSFM by partially defat­
row with different superscripts are significantly different (P < 0.05). ting the larvae before processing, hence resulting in a high crude protein
level.
et al. (2021). They found higher ADC protein was observed in Nile
tilapia (Oreochromis niloticus) fed BSFM compared to FM diets. Overall, Funding
the results were in line with previous studies on rainbow trout (Dumas
et al., 2018; Renna et al., 2017), and Atlantic salmon (Fisher et al., 2020; This research was sponsored by the Ministry of Higher Education
Lock et al., 2016), where BSFM significantly increases the ADC nutrients Malaysia for Fundamental Research Grant Scheme (FRGS) (FRGS/1/
compared to those given only FM. Although there was no significant 2019/WAB01/UM/02/3) and [FP073-2019A] awarded to Dr Norhi­
difference in ADC lipid for both diets, BSFM fed fish shows numerically dayah Mohd Taufek.
higher ADC lipid than FM, suggesting that the lipid in BSFM is easily
absorbed and digested by tilapia. However, high lipid content in the Availability of data and material
BSFM diet might influence the poor ADC lipid of RHT in the present
study compared to other fish species, including hybrid grouper and The authors confirm that the data are available upon request.
rainbow trout as described by Mohamad-Zulkifli et al. (2019) and Renna
et al. (2017). Authors’ contributions
With regard to the digestibility of BSFM, Zhou et al. (2018) reported
that the full replacement of the FM diet with the BSFM in the Jian carp Hasniyati Muin: Conceptualization, Methodology, Visualization,
diet does not affect their growth and digestibility. Furthermore, Moha­ Investigation, Writing – original draft, preparation Norhidayah Mohd
mad-Zulkifli et al. (2019) also observed highly digestible BSFM when Taufek: Supervision, Project administration, Writing – review & editing.
oven-dried when fed to hybrid grouper. However, studies by Belghit
et al. (2018) reported that replacing the dietary FM and soy protein Ethics approval
concentrate with BSFM significantly reduces the ADC of protein, lipid
and all amino acids in Atlantic salmon even though they are still highly Ethical clearance in handling the animal was obtained from Insti­
digestible. In addition, several fishes such as turbot (Kroeckel et al., tutional Animal Care and Use Committee, Universiti Malaya (Ethics
2012), meagre (Guerreiro et al., 2021), sea bream (Takakuwa et al., Reference Number: S/03102019/10,052,019-01/R).
2022) and rainbow trout (Belforti et al., 2015) have shown unsatisfac­
tory ADC after being fed with insect meal. Fontes et al. (2019) reported Declaration of competing interest
the decrease of ADC due to the presence of higher chitin in insect meals.
Chitin is hypothesised to reduce the access to chitinase and pro­ The authors declare that there are no conflicts of interest associated
teinases, affecting intestines’ protein and lipid absorption, thus pre­ with this publication.
venting the absorption of proteins and lipids by the intestine (Lock et al.,
2018). Furthermore, according to Taufek et al. (2016), chitin might Acknowledgement
influence the fish feed intake and nutrient digestibility, resulting in
growth suppression. Chitin content in raw BSFM in this study was within We want to thank the Ministry of Higher Education Malaysia for the
the range of 2.86%–5.50%, as reported by Marono et al. (2015), who Fundamental Research Grant Scheme (FRGS/1/2019/WAB01/UM/02/
examined six different samples of dried BSFL collected from different 3) and FP073-2019A awarded to Dr Norhidayah Mohd Taufek. We also
laboratories. However, the value obtained was lower than the one re­ want to thank Mr Hanan Mohd Yusof and his team in Freshwater Fish­
ported by Finke (2013) (5.41%) and Kroeckel et al. (2012), who re­ eries Research Institute, Glami-lemi, Jelebu, Malaysia, for their tech­
ported 96 g kg− 1 dry matter of the Hermetia illucens larvae. nical assistance. Finally, our appreciation goes to the Institute of
The potential of chitin digestibility varies between fishes. In certain Biological Science for providing the necessary laboratory facilities for
species, chitin is deemed to have immunostimulant property (Lock et al., this research.
2018)that is useful to prevent fishes from contracting the disease and
bacterial infection (Esteban et al., 2000; Gopalakannan & Arul, 2006; References
Sakai et al., 1992). This study’s BSFM diet with 1% chitin does not affect
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