Aquaculture Reports 21 (2021) 100775

Contents lists available at ScienceDirect

Aquaculture Reports
journal homepage: www.elsevier.com/locate/aqrep

Performance of defatted black soldier fly pre-pupae meal as fishmeal

replacement in the diet of lemon fin barb hybrid fingerlings
Mohd Salleh Kamarudin, Suharmili Rosle *, Ina Salwany Md Yasin
Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Malaysia

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

Keywords: This study was conducted to determine the optimal level of defatted black soldier fly pre-pupae (BSFP), Hermetia
Alternative protein source illucens as a fishmeal replacement in lemon fin barb hybrid diet. Triplicate groups of fish (1.52 ± 0.01 g) were
Black soldier fly pre-pupae fed twice a day until apparent satiation with five iso-nitrogenous (30 %) and isocaloric (17 kJ g− 1) diets con­
Body composition
taining varying BSFP levels ranging from 0 to 100 % for 8 weeks. No mortality was found during this study. BSFP
Barb hybrid
Waste management
level used in the diets were significantly affected the growth response of the barb hybrid. The growth perfor­
mance of fish such as body weight gain and specific growth rate improved up to 75 % BSFP and decreased above
this level, while feed conversion ratio and daily feed intake were not affected by BSFP levels. Body protein and
lipid contents of the barb hybrid were significantly affected by dietary replacement levels. The protein retention
decreased and lipid retention increased when the BSFP level increased, while the carbohydrate retention was
extremely low. The most abundant of essential amino acids in the whole body of lemon fin barb hybrid was
valine while glutamic acid was the abundant non-essential amino acids. No pathological changes were observed
among all dietary fed groups. The present study suggested that fishmeal could be replaced up to 75 % or 2.5 %
fishmeal was still required in the lemon fin barb hybrid diet.

1. Introduction profile and improve fish performance.

The rapid growth of the aquaculture industry using fishmeal as major
protein sources has led to an increase in demand and price for this
product (Olsen and Hasan, 2012). However, due to increased awareness
of the scarcity of fishmeal, many researchers and feed manufacturers
have made extensive efforts by looking for alternative protein sources to
minimize dependency on costly fishmeal and to provide adequate
nutrition for animal growth (FAO, 2012; Gasco et al., 2018).
Sing et al. (2014) suggested that alternative protein sources must be
easily available and accessible, contain amino acids similar or better
than fishmeal and have the palatability comparable to fishmeal to avoid
rejection by the fish. Earlier studies by Siddiqui et al. (1988) found that
the difference in protein sources could give different effects on the
growth performance of a fish. Some of the factors that may have
contributed to the variation in the growth are protein composition,
amino acid profile, phosphorus content and palatability of feeds (Ogunji
et al., 2008). Adewolu et al. (2010) suggested that a mixture of different
protein sources for the fishmeal replacement is better rather than having
a single source because these mixtures can contain a better amino acid
Insect meals such as BSFP, common housefly maggots, the yellow
mealworm, the lesser mealworm, silkworm (Bombyx mori) and several
grasshopper species are seen as the most promising candidates to sup­
port the needs of the industry and have long been proposed as a possible
alternative protein to fishmeal (Ramos-Elorduy et al., 1997; van Huis,
2013). Studies on insect meals have been conducted in many fish such as
Oreochromis niloticus (Ogunji et al., 2006; Ogunji et al., 2008; Sing et al.,
2014), Cyprinus carpio (Ogunji et al., 2011) and Clarias gariepinus
(Fasakin et al., 2003; Aniebo et al., 2009; Adewolu et al., 2010).
Bondari and Sheppard (1981) reported that insects in various
developmental stages have been used in aquafeed and animal feed.
Several authors have reported an immense potential of the common
housefly larvae or maggot grown on animal waste as a good protein
source for fish due to its availability, good protein content and provide a
cheaper cost (Sheppard et al., 2002; Ogunji et al., 2006, 2008; Katya
et al., 2017; Li et al., 2017).
In addition, insects show great potential as an environmentally
friendly choice in future food systems as they are extremely efficient at
converting organic matters into animal proteins and dietary energy

* Corresponding author.
E-mail address: suharmili218@gmail.com (S. Rosle).

https://doi.org/10.1016/j.aqrep.2021.100775
Received 26 January 2021; Received in revised form 27 June 2021; Accepted 28 June 2021
Available online 3 July 2021
2352-5134/© 2021 The Author(s). 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/).
M.S. Kamarudin et al. Aquaculture Reports 21 (2021) 100775

2. Materials and methods

2.1. Experimental system

The rearing period was conducted for 8 weeks at the Wet Laboratory,
Department of Aquaculture, Faculty of Agriculture, Universiti Putra
Malaysia. Fifteen 100-L glass aquaria (76 cm × 35 cm × 35 cm) each
equipped rectangular top filters were used for the fish rearing. Dech­
lorinated water (60-L) was used to fill each aquarium. An adequate level
of oxygen was also provided through individual air stones.

2.2. Experimental fish

Lemon fin barb hybrid fingerlings were procured from the Perlok
Aquaculture Extension Centre, Jerantut, Pahang, Malaysia. The F2 fin­
gerlings (1.52 ± 0.01 g) were induced-bred from the F1 hybrid brood­
stock of Hypsibarbus wetmorei male X Barbodes gonionotus female. The
fishes were fed with a 32 % crude protein commercial tilapia diet (Star
Feed (M) Sdn. Bhd., Malaysia) during two weeks of acclimation period.
After the acclimation period, twenty fishes were randomly stocked into
each glass aquarium.
Fig. 1. Hand operated oil press.
Source: http://www.easyoilpress.com. 2.3. Preparation of black soldier fly pre-pupae (BSFP) meal

The BSFP meal was obtained from a local supplier (Entofood.Sdn.

(Halloran et al., 2016). In developing countries, waste collection and
Bhd) and defatted using hand operated oil press (Fig. 1). The defatted
inadequate treatment of wastes are multidimensional issues as about
meal was ground using an electric grinder (Panasonic, MX-GM0501) and
one to two-thirds of wastes generated are often not collected (Diener
sieve through 500 μm. The meal was kept at − 20 ◦ C before chemical
et al., 2009). In Malaysia, approximately 15,000 tons of food and
analysis and diet formulation.
kitchen wastes are produced daily and 91,251 tons of palm oil feed
wastes are annually generated in the last three years (Thestar, 2013;
2.4. Experimental diets
Index mundi, 2016b). Abdul Rahman et al. (2016) suggested the fly
maggot meal industry shall be developed to use these locally available
Five isonitrogenous and isocaloric diets (30 % protein and 17 kJ g− 1)
agro-industrial by-products (lignocellulosic) and wastes to produce
containing BSFP meal as 0, 25, 50, 75 and 100 % fishmeal replacement
proteins for the least cost of animal feeds. In 2013, a legal change made
were formulated and prepared (Table 1). No oil with high soybean meal
by the European Commission and the European Food Safety Authority
formulation was due to the intention of producing a least-cost practical
(EFSA) to allow insects to be used as feed as they are considered to bring
diet for this hybrid fish. In addition, the price of soybean meal obtained
no risk to human health (Ramsden, 2016). The black soldier fly pupae
from a local supplier (Pk Agro-Industrial Product (M) Sdn. Bhd) was USD
meal is already permitted because its adults are not attracted to human
0.47 as compared to USD 1.02 for fishmeal. The diets were processed
habitats or foods and are not considered a pest (van Huis et al., 2013).
using a single screw extruder (Brabender KE-19) at 2 mm Ø die and
The black soldier fly, Hermetia illucens (BSF) is classified under
barrel temperatures were set at 90, 110 and 120 ◦ C. The pellets were
Diptera order (Barroso et al., 2014). It can be found in warm and
oven-dried at 50 ◦ C for about 4 h. The diets were broken into 1 mm
temperate climates and its larvae can be reared on a wide range of
crumbles and packed in airtight containers with silica gel.
organic waste materials. The suitability of the BSF larval meal as a
protein source in feedstuff had been observed in other aquaculture
2.5. Feeding and sampling of fish
species such as chanel catfish, Pacific white shrimp, Nile tilapia, juvenile
barramundi, European seabass, Atlantic salmon and ornamental fish
Each test diet was randomly assigned to three aquaria (replicates).
(Bondari and Sheppard, 1981; Cummins et al., 2017; Devic et al., 2017;
The fishes were hand-fed to apparent satiation two times daily (0900
Katya et al., 2017; Magalhães et al., 2017; Bruni et al., 2020; Li et al.,
and 1600 h). Samplings were conducted every two weeks to minimize
2020; Sinansari and Fahmi, 2020). However, no studies have been re­
stress to the fish (Ingram et al., 2005). A digital electronic balance was
ported for lemon fin barb hybrid.
used to weigh the fish. The specific growth rate (SGR) and feed con­
Lemon fin barb hybrid is originated from a cross between lemon fin
version ratio (FCR) were calculated at the end of the experiment. For
barb, Hypsibarbus wetmorei and female silver barb, Barbonymus gonio­
whole-body proximate analysis, 30 fishes from the initial stock and 15
notus. This species has been cultured in Indonesia, Thailand, Vietnam,
fishes from each aquarium at the end of the feeding trial were randomly
Bangladesh and also Malaysia (Mohanta et al., 2009). Its production,
sacrificed, put in − 20 ◦ C for further analysis. Water quality parameters
mainly in freshwater cages was 34.97 tons with a wholesale value of
USD 399,062 in 2019 (DOF, 2019). This fish is fed with tilapia or catfish such as water temperature, dissolved oxygen (DO), pH and total
ammonia were measured on non-sampling days and the water was 50 %
commercial feed and supplemented with chopped plant materials such
as napier grass and aquatic plants. This research was thus aimed at changed during samplings (Kamarudin et al., 2011). Water quality pa­
rameters throughout feeding trials were within acceptable limits. Dis­
evaluating defatted black soldier fly pre-pupae (BSFP) meal as a fish­
meal substitute in the diet of lemon fin barb hybrid fingerlings. At solved oxygen was in the range of 6.32–6.43 mg l− 1, the temperature
ranged 27.8–28.9 ◦ C, pH ranged 6.68–6.82 and total ammonia ranged
present, there is a medium-scale commercial production of BSFP meal in
Malaysia which is mainly targeted for the direct feeding of aquarium 0.053–0.101 mg l− 1.
fishes and poultry.
2.6. Chemical analysis

The proximate composition of fish samples and experimental diets

2
M.S. Kamarudin et al. Aquaculture Reports 21 (2021) 100775

Table 1
Feed ingredients, proximate (% as fed basis) and amino acids composition of test diets.
Fishmeal BSFP BSFP meal level (%)

0 (Control) 25 50 75 100

Ingredients
Fishmeal 10 7.5 5.0 2.5 0
Black soldier fly pre-pupae (BSFP) 0 2.5 5.0 7.5 10
Soybean meal 43.76 43.76 43.76 43.76 43.76
Rice bran 22.21 22.21 22.21 22.21 22.21
Tapioca starch 20 20 20 20 20
Vitamin premixa 1 1 1 1 1
Mineral premixb 1 1 1 1 1
α-cellulose 2.03 2.03 2.03 2.03 2.03
Proximate composition
Moisture 6.99 7.20 7.57 ± 0.10 7.60 ± 0.09 7.63 ± 0.11 7.74 ± 0.08 7.74 ± 0.05
Protein 62.73 60.11 29.74 ± 0.15 29.68 ± 0.15 29.11 ± 0.33 28.72 ± 0.35 28.33 ± 0.16
Lipid 7.09 5.57 5.48 ± 0.05 5.39 ± 0.08 5.35 ± 0.10 5.27 ± 0.04 5.15 ± 0.06
Ash 21.20 13.31 8.14 ± 0.21 7.96 ± 0.17 7.71 ± 0.15 7.18 ± 0.17 7.02 ± 0.09
Crude fibre 0.08 7.51 3.03 ± 0.04 3.06 ± 0.07 3.12 ± 0.06 3.27 ± 0.20 3.35 ± 0.17
NFEc 1.90 6.30 46.05 ± 0.40 46.31 ± 0.33 47.07 ± 0.53 47.82 ± 0.30 48.41 ± 0.32
( )
Gross energy kJ g− 1 18.17 19.32 17.38 ± 0.05 17.36 ± 0.07 17.23 ± 0.06 17.21 ± 0.04 17.03 ± 0.06
( )
P:E mg protein kJ− 1 d 34.53 31.12 17.12 ± 0.13 17.10 ± 0.11 16.90 ± 0.16 16.69 ± 0.24 16.64 ± 0.15

Amino acid composition

Essential Amino Acids (EAA)
Arginine 11.01 6.17 2.04 ± 0.03 1.99 ± 0.03 1.89 ± 0.06 1.61 ± 0.05 1.52 ± 0.04
Histidine 8.28 1.94 1.21 ± 0.04 1.10 ± 0.03 0.97 ± 0.09 0.89 ± 0.11 0.78 ± 0.11
Isoleucine 1.99 1.43 0.91 ± 0.03 0.76 ± 0.03 0.67 ± 0.11 0.63 ± 0.04 0.53 ± 0.09
Leucine 1.64 4.54 1.07 ± 0.02 1.19 ± 0.04 1.25 ± 0.09 1.31 ± 0.03 1.40 ± 0.03
Lysine 6.58 1.23 3.01 ± 0.04 2.91 ± 0.02 2.54 ± 0.05 2.14 ± 0.09 2.05 ± 0.03
Methionine 1.47 0.94 0.91 ± 0.04 0.86 ± 0.05 0.82 ± 0.02 0.78 ± 0.04 0.75 ± 0.08
Phenylalanine 0.07 0.65 0.22 ± 0.03 0.25 ± 0.03 0.28 ± 0.02 0.31 ± 0.03 0.34 ± 0.03
Threonine 0.08 2.57 1.67 ± 0.05 1.82 ± 0.17 1.91 ± 0.02 2.10 ± 0.07 2.21 ± 0.04
Tyrosine 0.35 4.10 2.14 ± 0.03 2.20 ± 0.04 2.30 ± 0.03 2.37 ± 0.10 2.40 ± 0.30
Valine 5.99 6.08 0.90 ± 0.04 1.03 ± 0.03 1.05 ± 0.06 1.09 ± 0.04 1.14 ± 0.03
Non-essential Amino Acids (NEAA)
Alanine 0.99 6.35 1.27 ± 0.02 1.34 ± 0.04 1.41 ± 0.08 1.48 ± 0.03 1.61 ± 0.06
Aspartic acid 7.01 7.57 5.12 ± 0.04 5.16 ± 0.08 5.20 ± 0.05 5.23 ± 0.04 5.28 ± 0.07
Cystine 0.14 1.98 0.73 ± 0.04 0.81 ± 0.03 0.91 ± 0.04 1.09 ± 0.09 1.17 ± 0.11
Glutamic acid 11.33 9.61 4.16 ± 0.32 4.12 ± 0.25 3.88 ± 0.24 3.81 ± 0.15 3.50 ± 0.17
Glycine 1.98 4.43 2.14 ± 0.07 2.17 ± 0.05 2.21 ± 0.05 2.30 ± 0.06 2.39 ± 0.04
Serine 3.80 0.53 2.25 ± 0.09 1.98 ± 0.14 1.81 ± 0.19 1.58 ± 0.27 1.28 ± 0.06
a
Vitamin premix (g kg− 1premix): ascorbic acid, 45; myo-inositol, 5;choline chloride, 75; niacin, 4.5; riboflavin, 1; pyridoxine, 1; thiamin mononitrate, 0.9; Ca-
pantothenate, 3; retinyl acetate, 0.6; cholecalciferol, 0.08; vitamin K menadione, 1.7; a-tocopheryl acetate (500 IU g 1), 8; biotin, 0.02; folic acid, 0.1; vitamin
B12, 0.001;cellulose, 845.1.
b
Mineral premix (g kg− 1premix): KCl, 90; KI, 0.04; Ca(H2PO4).H20,500; NaCl, 40; CuSO4.5H2O, 3; ZnSO4.7H2O, 4; CoSO4, 0.02;FeSO47H2O, 20; MnSO4.H2O, 3;
CaCo3, 215; MgOH, 124; Na2SeO3, 0.03; NaF, 1.
c
Nitrogen-free extract (NFE) = 100 − (protein + lipid + ash + fiber + moisture).
d
P:E = protein to energy ratio in mg protein kJ− 1.

Table 2
Growth performance and feed utilization of lemon fin barb hybrid fed on test diets for 8 weeks.
Parameter BSFP meal level (%)

0 (Control) 25 50 75 100

Survival (%) 100 100 100 100 100

Body weight
Initial (g) 1.53 ± 0.01a 1.52 ± 0.01a 1.52 ± 0.02a 1.51 ± 0.02a 1.52 ± 0.01a
Final (g) 6.78 ± 0.42a 6.39 ± 0.39ab 6.27 ± 0.20ab 6.12 ± 0.29ab 5.61 ± 0.50b
Gain
(g) 5.25 ± 0.42a 4.88 ± 0.23ab 4.75 ± 0.21ab 4.60 ± 0.28ab 4.09 ± 0.49b
(%) 343.13 ± 27.78a 321.80 ± 16.47ab 311.20 ± 15.61ab 301.23 ± 16.47ab 269.02 ± 31.94b
( )
SGR % d− 1 2.48 ± 0.10a 2.40 ± 0.07ab 2.36 ± 0.06ab 2.31 ± 0.07ab 2.17 ± 0.14b

Daily feed intake(% BW d− 1 ) 6.11 ± 0.20a 5.72 ± 1.06a 6.11 ± 0.26a 6.35 ± 0.29a 6.37 ± 0.98a
a a a a
FCR 1.76 ± 0.11 1.79 ± 0.11 1.84 ± 0.88 1.87 ± 0.23 2.14 ± 0.47a

Means (± SD) value within a row with the same superscripts are not significant (p > 0.05).

were analyzed in triplicates (AOAC, 1990). Dry matter analysis was
conducted using the oven drying technique where the samples were kept
at 105 ◦ C till a constant weight and percentage of crude protein was
estimated using a protein analyzer (Foss 2400 Kjeltec Analyzer Unit).
Lipid was determined by solvent extraction with petroleum ether
(Soxtec system, Foss Tecator Lipid Analyzer). Analysis of total ash
content was done by combustion of the samples for 6 h at 600 ◦ C.
Estimation of crude fibre content was done by acid digestion followed by
alkaline digestion technique (Fibertec 2010 Hot Extractor Foss Tecator).
The gross energy content of the samples was analyzed using a bomb

3
M.S. Kamarudin et al. Aquaculture Reports 21 (2021) 100775

Table 5
Whole-body amino acid composition (% wet weight) in lemon fin barb hybrid
fingerlings during 8 weeks rearing period.
Amino acid Initial BSFP meal level (%)

0 (Control) 25 50 75 100

EAA
Arginine 0.94 ± 1.18 ± 1.16 ± 1.17 1.11 ± 1.08 ±
0.06 0.02a 0.02ab ± 0.03bc 0.02c
0.02a
Histidine 0.24 ± 0.44 ± 0.38 ± 0.30 0.38 ± 0.38 ±
0.04 0.10a 0.12a ± 0.07a 0.10a
0.15a
Isoleucine 0.40 ± 0.66 ± 0.50 ± 0.50 0.56 ± 0.47 ±
Fig. 2. Polynomial relationship between fish body weight gain (%) and dietary 0.01 0.07a 0.02b ± 0.02ab 0.02b
BSFP meal level (%) for lemon fin barb hybrid fingerlings. 0.04b
Leucine 1.11 ± 1.48 ± 1.30 ± 1.22 1.30 ± 1.27 ±
0.04 0.02a 0.02b ± 0.01b 0.02bc
0.03c
Table 3 Lysine 0.32 ± 0.53 ± 0.51 ± 0.49 0.52 ± 0.46 ±
Whole-body proximate composition (% wet weight basis) of lemon fin barb 0.07 0.04a 0.08a ± 0.10a 0.04a
hybrid fingerlings after 8 weeks culture period. 0.03a
Methionine 0.34 ± 0.40 ± 0.50 ± 0.50 0.36 ± 0.35 ±
BSFP meal level (%) 0.03 0.03b 0.03a ± 0.03b 0.03b
Initial 0 (Control) 25 50 75 100 0.02a
Phenylalanine 0.14 ± 0.17 ± 0.19 ± 0.18 0.18 ± 0.16 ±
Moisture 74.75 72.09 ± 73.61 73.15 72.58 71.10 0.05 0.05a 0.02a ± 0.02a 0.02a
± 0.65 1.33a ± 1.28a ± 2.33a ± 1.77a ± 1.67a 0.02a
Crude 15.21 19.00 ± 17.21 16.94 17.00 16.83 Threonine 0.69 ± 0.80 ± 0.71 ± 0.69 0.67 ± 0.65 ±
protein ± 0.08 0.98a ± ± 0.91b ± 0.51b ± 0.59b 0.08 0.02a 0.02b ± 0.03b 0.03b
0.16ab 0.02b
Crude 5.04 ± 6.03 ± 6.26 ± 6.81 ± 7.39 ± 9.12 ± Tyrosine 0.49 ± 0.60 ± 0.58 ± 0.56 0.53 ± 0.51 ±
lipid 0.05 0.58c 0.20bc 0.48bc 0.59b 0.66a 0.01 0.02a 0.05a ± 0.02a 0.02a
Total ash 2.12 ± 1.14 ± 1.22 ± 1.24 ± 1.36 ± 1.30 ± 0.05a
0.12 0.11a 0.13a 0.25a 0.13a 0.16a Valine 1.34 ± 1.96 ± 1.65 ± 1.56 1.71 ± 1.47 ±
Crude 0.11 ± 0.04 ± 0.03 ± 0.03 ± 0.02 ± 0.04 ± 0.04 0.02a 0.04b ± 0.04b 0.02d
fibre 0.02 0.01a 0.01a 0.01a 0.01a 0.01a 0.03c
NFE 2.77 ± 1.70 ± 1.67 ± 1.84 ± 1.64 ± 1.62 ± NEAA
0.72 0.57a 1.22a 1.56a 1.33a 1.20a Alanine 1.29 ± 1.72 ± 1.51 ± 1.50 1.55 ± 1.59 ±
Gross 5.58 ± 6.24 ± 5.85 ± 6.00 ± 6.35 ± 6.86 ± 0.05 0.10a 0.12a ± 0.12a 0.14a
energy 0.20 0.25a 0.31a 0.52a 0.49a 0.18a 0.11a
( )
kJ g− 1 Aspartic acid 1.88 ± 2.21 ± 1.96 ± 1.92 1.92 ± 2.02 ±
0.02 0.01a 0.06bc ± 0.01c 0.01b
Mean values with the same superscripts in each row are not significant (p > 0.01c
0.05). Values are means of three replicates of each experimental diet ± standard Cystine 0.75 ± 0.80 ± 0.73 ± 0.76 0.78 ± 0.83 ±
deviation (SD). 0.05 0.02a 0.05a ± 0.02a 0.04a
0.05a
Glutamic acid 2.79 ± 3.33 ± 3.05 ± 2.96 2.93 ± 2.95 ±
0.03 0.08a 0.04b ± 0.03b 0.03b
Table 4 0.05b
Protein retention (%), lipid retention (%) and carbohydrate retention (%) of test Glycine 1.28 ± 1.46 ± 1.40 ± 1.51 1.40 ± 1.40 ±
diets containing a varying percentage of BSFP meal as a fishmeal replacement in 0.04 0.05ab 0.04b ± 0.02b 0.04b
lemon fin barb hybrid fingerlings. 0.03a
Serine 1.20 ± 1.26 ± 1.10 ± 1.12 1.09 ± 1.23 ±
BSFP meal level Protein Lipid retention Carbohydrate
0.08 0.09a 0.10a ± 0.06a 0.11a
(%) retention (%) (%) retention (%)
0.07a
0 (Control) 58.32 ± 9.21a 98.99 ± 12.26a 2.66 ± 0.28a
25 52.32 ± 8.58a 107.25 ± 17.16a 2.52 ± 0.37a EAA = essential amino acids.
50 46.66 ± 1.90a 106.78 ± 1.81a 2.55 ± 0.19a NEAA = non-essential amino acids.
75 44.64 ± 6.02a 115.85 ± 24.46a 1.90 ± 0.21ab
100 40.43 ± 9.38a 136.67 ± 37.80a 1.63 ± 0.44b
2.7. Histological examination
Mean values with the same superscripts in each column are not significant (p >
0.05) Values are means of three replicates of each experimental diet ± standard At the final sampling, three fishes from each aquarium were
deviation (SD). randomly taken for histopathological analysis and the fish were anaes­
thetized with 0.03 mL l− 1 clove oil (Hamackova et al., 2006). The liver
and intestine of fish were dissected under dissecting microscope. The
histopathological were carried out using the standard procedure as
described by Luna (1968). The samples were sent to the Faculty of
calorimeter (Leco AC-350, USA).
Veterinary Medicine, Universiti Putra Malaysia for further analysis. A
light microscope (Leica DM750, Leica Application Suite, LAS EZ Version
2.6.1. Amino acid analysis
1.7.0, Switzerland Limited) was used to observe for any abnormality on
All the samples were sent for amino acid analysis at Nutrition
the liver and intestine when fish fed BSFP meal.
Analytical Laboratory, Department of Animal Science, Universiti Putra
Malaysia. The amino acid profile was determined using High Perfor­
mance Liquid Chromatography, Agilent 1100 HPLC with a fluorescence
detector.

4
M.S. Kamarudin et al. Aquaculture Reports 21 (2021) 100775

Fig. 3. Relationship between dietary and body amino acids (% of total amino acids) of lemon fin barb hybrid fed varying dietary percentage of BSFP as fishmeal
replacement for 8 weeks.

2.8. Statistical analysis 3.2. Body composition

Data on survival, growth performance and feed utilization of fish
were analyzed using one-way analysis of variance (ANOVA) and Tukey’s
test was used to test mean differences between dietary treatments in
Statistical Analysis System (SAS 9.3). All percentage data were then
arcsine transformed before analysis.
Table 3 presented the whole-body proximate compositions of lemon
fin barb hybrid. The results showed that body protein and lipid were
affected by the dietary BSFP levels. Fish fed with a 100 % BSFP had the
lowest protein and highest body lipid (p < 0.05) compared to other
groups.

3. Results
3.3. Nutrient retention
3.1. Growth, survival and feed performance
The present study showed carbohydrate retention of hybrid finger­
lings was significantly affected by the dietary BSFP level (Table 4). In
Fish were observed to actively feed on all the test diets. The growth
general, the protein retention decreased when the BSFP level increased.
performance and feed utilization of lemon fin barb hybrid fed varying
However, no significant differences were found among the dietary
dietary defatted BSFP meal level are shown in Table 2. No mortality was
treatments. Despite the increasing trend in lipid retention with the
observed in all treatments during the feeding trial. In general, the
percentage increase of BSFP meal inclusion, the retentions were similar
growth of lemon fin barb hybrid fish decreased with the increase of BSFP
for all treatments. The carbohydrate retentions were extremely low (<
meal level (Fig. 2). However, the differences were not significant (p >
3%).
0.05) except among the control and those fed 100 % BSFP meal. No
Body histidine, lysine, phenylalanine, alanine, cystine, serine and
significant differences in FCR were observed among the treatments. The
tyrosine were not significantly (p > 0.05) affected by the dietary BSFP
daily feed intake was not significantly affected (p > 0.05) by the BSFP
level (Table 5). The most abundant EAA in the whole body of lemon fin
meal level.
barb hybrid was valine while glutamic acid was the abundant NEAA.
Fig. 3 summarizes the dietary and whole-body amino acid compositions
of lemon fin barb hybrid. Tyrosine and lysine in the whole body

5
M.S. Kamarudin et al. Aquaculture Reports 21 (2021) 100775

Table 6 The wider ranges may be due to differences in the processing, drying or
Mean values of amino acid retention (% of dietary respective amino acids) in storage methods used (Ogunji et al., 2008). The nutrient composition of
lemon fin barb hybrid fingerling fed varying dietary percentage of BSFP as defatted BSFP meal used in this study compared favourably with fish­
fishmeal replacement for 8 weeks. meal especially with crude protein of 60.11 % and low lipid (<6 %).
Amino acids BSFP meal level (%) Most fish species can be fed with a maggot meal-based diet but the
0 (Control) 25 50 75 100 effect will vary in different fish species and maggot meal quality (Devic
et al., 2013). The incorporation of a 75 % defatted BSFP meal was found
EAA
Arginine 52.66 ± 54.61 ± 51.19 ± 52.58 ± 48.57 ±
to be as good as the control diet (100 % fishmeal) for the survival and
1.72a 11.14a 2.26a 2.48a 7.04a growth of lemon fin barb hybrid fingerlings. The good performance
Histidine 35.60 ± 33.94 ± 25.86 ± 35.04 ± 36.43 ± might be due to the de-fattening which probably influenced nutrient
1.16ab 6.92ab 1.14b 1.65ab 5.28a availability, palatability and utilization of the meals (Fasakin et al.,
Isoleucine 69.76 ± 61.53 ± 63.68 ± 70.99 ± 61.49 ±
2003). Lemon fin barb hybrid has a low optimal dietary lipid require­
2.28a 12.55a 2.82a 3.35a 8.92a
Leucine 127.76 ± 100.21 ± 78.32 ± 75.70 ± 61.46 ± ment of 4% while dietary lipid of more than 8% suppresses its growth
4.18a 20.44ab 2.46bc 3.58bc 8.91c (Ismail et al., 2016). Ogunji et al. (2011) suggested that there seems to
Lysine 16.96 ± 17.21 ± 16.77 ± 19.99 ± 16.41 ± be a form of nutrient fortification when fishmeal is combined with
0.55a 3.51a 0.74a 0.94a 2.38a maggot meal in the diet of carps up to a certain level. The present
Methionine 39.43 ± 55.95 ± 52.30 ± 34.12 ± 30.76 ±
1.29bc 11.41a 2.31ab 1.61c 4.46c
findings were similar to the results of Cyprinus carpio when fed maggot
Phenylalanine 64.78 ± 71.97 ± 53.57 ± 45.24 ± 32.11 ± meal as 50–75 % fishmeal replacement. A lower percentage of 20–50 %
2.12ab 14.68a 2.37ab 2.14bc 4.66c fishmeal replacement has been reported for other species such as
Threonine 42.82 ± 34.46 ± 28.11 ± 22.93 ± 19.15 ± rainbow trout, Pacific white shrimp and juvenile barramundi (Stamer
1.40a 7.02ab 1.24bc 1.08cd 2.78d
et al., 2014; Cummins et al., 2017; Katya et al., 2017).
Tyrosine 25.50 ± 24.32 ± 19.81 ± 16.33 ± 14.16 ±
0.83a 4.96a 0.88ab 0.77b 2.05b Adenji (2007) also found that housefly maggot meal can only replace
Valine 204.41 ± 148.43 ± 119.82 ± 122.01 ± 86.85 ± fishmeal up to 50 % in chicken feed. Nevertheless, successful total re­
6.68a 30.28b 5.30b 5.76b 12.60c placements of fishmeal (100 %) by maggot meals have reported for
NEAA tilapia, Oreochromis niloticus (Fashina-Bombata and Balogun, 1997;
Alanine 125.07 ± 102.47 ± 86.65 ± 80.40 ± 69.07 ±
4.09a 20.90ab 3.83bc 3.80bc 10.02c
Ogunji et al., 2006; Sing et al., 2014). These researchers concluded that
Aspartic acid 38.76 ± 33.73 ± 28.96 ± 27.06 ± 25.64 ± the biological values of maggot meals are equivalent to that of fishmeal
1.27a 6.88ab 1.28ab 1.28b 3.72b and the meals contain no anti-nutritional or toxic factors which are
Cystine 95.55 ± 77.91 ± 64.97 ± 52.38 ± 47.71 ± commonly found in alternative protein sources of vegetable origin. A
3.12a 15.89ab 2.87bc 2.47bc 6.92c
study by Ogunji et al. (2011) found that maggot meals have balanced
Glutamic acid 72.37 ± 66.32 ± 60.24 ± 56.77 ± 56.14 ±
2.37a 13.53a 2.66a 2.68a 8.14a amino acid profiles over many other alternative protein sources.
Glycine 60.62 ± 57.87 ± 55.63 ± 45.33 ± 39.31 ± Although fish fed 100 % BSFP resulted in poorer growth performances in
1.98a 11.80a 2.46ab 2.14ab 5.70b the present study, neither signs of nutrient deficiency nor mortality were
Serine 48.91 ± 47.42 ± 47.18 ± 48.56 ± 63.42 ± observed.
1.60a 9.67a 2.09a 2.99a 9.20a
De Silva et al. (2002) stressed that a lower FCR value improves
EAA = essential amino acids. feeding outcome. FCR values in the present study ranged 1.76–2.14 that
NEAA = non-essential amino acids. were better compared to those observed in juvenile red tilapia fed
Mean values with the same superscripts in each row are not significant (p > blowfly maggot meal and juvenile barramundi fed black soldier fly
0.05). Values are means of triplicate of each experimental diet ± standard de­ larval meal (Sing et al., 2014; Katya et al., 2017) but slightly higher than
viation (SD).
rainbow trout fed maggot meals and Siberian sturgeon fed full-fat black
soldier fly larval meal (Stamer et al., 2014; Rawski et al., 2020). Olaniyi
decreased as their dietary compositions increased while body valine and Salau (2013) observed the maximum utilisation of nutrients when
increased as its dietary percentage decreased. In general, the higher African catfish are fed a diet containing a high level of maggot meal.
inclusion of BSFP meal led to lower amino acid retentions except for The inclusion of BSFP meal in the lemon fin barb hybrid diet would
arginine, isoleucine, lysine, glutamic acid and serine (Table 6). likely lower the feed cost, enhance optimal growth, provide economic
advantage and thus contribute more to the profitability for fish farmers.
3.4. Histopathological examination Fashina-Bombata and Balogun (1997) stated that the cost of producing
one kg of maggot meal is less than 20 % of the cost for 1 kg of fishmeal.
No pathological changes were observed in the livers and intestines of In this study, a kilogram of maggot meal cost about USD 0.19 (Viala,
all fish groups. The liver showed normal hepatic lobules and sinusoid pers. communication) compared to USD 1.29 kg− 1 for fishmeal (Index
structure among all treatment groups (Fig. 4 a, b, c, d and e). Meanwhile, mundi, 2016a). The inclusion of BSFP meal significantly reduced the
normal structures of intestinal tissues had been observed for all groups feed cost by 22.9 % kg− 1. Based on the cost, availability, biological value
when the microvilli were prominent and observed among all treatment and feed conversion ratio, BSFP meal could be a viable alternative
groups (Fig. 5 a–e). protein source to fishmeal in the diet of barb hybrid. The utilization of
maggots offers a good opportunity for the development of low-cost fish
4. Discussion feeds, especially in developing countries where fishmeal is usually im­
ported at a very expensive price. A high concentration of fibre (8–30 %)
The introduction of alternative ingredients such as insect meal in suppresses fish growth because most fish can only tolerate up to 8 %
aquafeed to minimize the use of costly fishmeal has been widely re­ fibre in their diets (Hilton and Atkinson, 1982). Lall and McCrea (2007)
ported but results are still inconclusive (Katya et al., 2017; Zarantoniello found that high levels of fibre in fish diets impair calcium, lipid and
et al., 2019). The common housefly, Musca domestica, maggot meal fat-soluble nutrient absorption. All test diets in the present study con­
contains 45.42 % crude protein, 15.2 % lipid and 28.8 % ash (Dong tained less than 3.4 % fibre.
et al., 2013) meanwhile blowfly maggot meal contains 55.5 % crude The lower growth performance among fish fed with 100 % BSFP
protein, 25.4 % lipid and 1.3 % ash (Sing et al., 2014) and BSFP meal meal might be due to excessive chitin content. Kroeckel et al. (2012)
comprises of 40–61.4 % crude protein, 12.5 21 % lipid, 5.8–8.2 % crude attributed the reduced feed intake, nutrient availability and growth
fibre and 0.93–11 % ash (Teotia and Miller, 1974; Fasakin et al., 2003). performance of turbot (Psetta maxima) fed a higher inclusion level of

6
M.S. Kamarudin et al.
Fig. 4. Cross-section of liver and intestine of lemon fin barb hybrid fed varying BSFP level during 8 weeks rearing period. (a) Liver of fish fed with control diet (b)
Liver of fish fed with 25 % BSFP diet (c) Liver of fish fed with 50 % BSFP diet (d) liver of fish fed with 75 % BSFP diet (e) Liver of fish fed with 100 % BSFP diet. Scale
bar = 100 μm. H&E.
BSFP meal to the presence of chitin. Chitin is a polymer of glucosamine
that is insoluble in nearly all solvents and it has been proven as a causing
factor for the declining growth performance and protein utilization in
African catfish (Ng et al., 2001). Halver and Hardy (2002) and Barroso
et al. (2014) stated that chitin may have adverse effects on the di­
gestibility of nutrients. Chitosan, a derivative of chitin, is commonly
used as a supplement for weight loss program in human (Mhurchu et al.,
2005).
The lower apparent digestibility coefficients of dry matter, protein,
average amino acid, lipid and energy occur in tilapia when it is fed
crayfish exoskeleton meal and gammarid meal that contain high ash and
chitin (Koprucu and Ozdemir, 2005). Fasakin et al. (2003) related the
reduction in growth performance of African catfish fed full-fat maggot
meal to low protein digestibility of maggot meal.
In this study, the whole-body protein and lipid of fish were affected
by the BSFP inclusion level. A study by St-Hilaire et al. (2007b) in
rainbow trout, Oncorhynchus mykiss found no difference in the
whole-body protein with an increase in the dietary black soldier fly
7
Aquaculture Reports 21 (2021) 100775
inclusion. Another study by Cummins et al. (2017) stated that the
whole-body profile of Pacific white shrimp has not much affected by
dietary black soldier fly larval meal. Nevertheless, Katya et al. (2017)
reported a high body lipid content of juvenile barramundi fed with 100
% BSP larval meal.
Suhenda and Tahapari (1997) stated that lipid retention in the body
does not come from the dietary lipid in a given diet but also the
bioconversion of dietary carbohydrate and protein respectively. Dietary
lipid and carbohydrate could affect utilization of each other in fish as
lipid could be converted to glucose via gluconeogenesis and it depends
on the fish ability to oxidize glucose and store it as glycogen or fat (Zhou
et al., 2015; Li et al., 2019). Another study by Rahman et al. (2017)
found that higher levels of carbohydrate in feeds increases the
whole-body lipid of fish through de novo lipogenesis. The body lipid
retention values of more than 100 % indicated that lemon fin barb
hybrid was able to convert dietary carbohydrate into body lipid. The
extremely low body fibre and carbohydrate retention in this hybrid fish
indicated that the species had efficiently converted most of the dietary
M.S. Kamarudin et al.
Fig. 5. Cross-section of the intestine of lemon fin barb hybrid fed varying BSFP level during 8 weeks rearing period. (a) Intestine of fish fed with control diet (b)
Intestine of fish fed with 25 % BSFP diet (c) Intestine of fish fed with 50 % BSFP diet (d) Intestine of fish fed with 75 % BSFP diet (e) Intestine of fish fed with 100 %
BSFP diet. Scale bar = 100 μm. H&E.
carbohydrate to body lipid. This study showed the presence of crude
fibre in the whole body of lemon fin barb hybrid. This is parallel to the
findings by Gatlin (2010) that liver and muscle tissue of animals contain
small concentrations of soluble carbohydrate in the form of glycogen,
which is structurally similar to starch and the body could rapidly utilize
this glycogen as glucose when needed.
The retention values of more than 100 % were observed for essential
valine and leucine. Ahmed and Khan (2006) stated that valine, along
with the other branched-chain amino acid isoleucine and leucine are
used to produce certain biochemical compounds in the body that help
energy production and reduce twitching and tremors in animals. Mag­
nus (2007) suggested that the increment of valine may be due to the
conversion of the leucine through leucine pathway since the valine
transamination reaction has A = O and may go either direction. Body
valine in this study ranged 1.47–1.96 % which were higher compared to
those of other wild-caught species likes Cyprinus carpio (0.3 %), Puntius
8
Aquaculture Reports 21 (2021) 100775
sophore (0.2 %) and Sperata seenghala (0.4 %) (Mohanty et al., 2014).
The use of 100 % BSFP meal as fishmeal replacement did no effect on
the retention of arginine, isoleucine, lysine, glutamic acid and serine.
Reduced retentions of other amino acid like histidine, leucine, methio­
nine, phenylalanine, threonine, valine, alanine, aspartic acid, cystine,
glycine and tyrosine were probably due to the utilisation by the fish for
metabolism (Cowey, 1994; Lovell, 1998). Kaushik (1998) and Peres and
Oliva-Teles (2005) found that the essential amino acid composition in
the whole body of Dicentrarchus labrax, Sparus aurata, Psetta maxima and
Scophthalmus maximus are relatively constant and slightly influenced by
fish size or diet. Similar observations were made in this study.
Healthy and good development of the gastrointestinal tract is one of
the key performance indicator of favourable growth to all farmed ani­
mals including poultry (Adibmoradi et al., 2006). No abnormality was
observed in the liver and intestinal tissue of barb hybrid in this study.
The findings were similar to those reported by Lock et al. (2016) in
M.S. Kamarudin et al.
Atlantic salmon fed BSFP meal. Feeding BSFP meal also does not affect
the taste of salmon fillets. FAO (2012) projected that the minimum di­
etary fishmeal requirement for carps can be reduced to 1% of the diet by
2020. This study showed that a minimal dietary inclusion of 2.5 %
fishmeal was required by the barb hybrid when a BSFP meal-fishmeal
mixture was used in its diet. In other maggot meal-fishmeal studies, a
much higher minimal fishmeal requirement (20–30 %) has been re­
ported (Ogunji et al., 2011; Idowu and Afolayan, 2013) but the degra­
dation of growth performance in Atlantic salmon when fed with
fishmeal free-diet (Rawski et al., 2020).
The use of commercially produced insect meals in aquafeeds has not
been objected to by FAO and European Union (FAO, 2013; 4ento, 2015).
Devic et al. (2013) stated that insect farming can be set up in natural
environments using sustainable energy sources. However, consistency in
the production of the meal is needed as the nutritional profile of fly
larvae can fluctuate depending on the species, the phenological stage
and the feeding substrate (Aniebo et al., 2009). In this study, defatted
BSFP meal had almost similar protein content as fishmeal (>60 %).
Kroeckel et al. (2012) and St-Hilaire et al. (2007a) proposed that this
characteristic shall provide good protein retention and growth of fish.
The fatty acid profile of fly larvae can be simply manipulated because it
is extremely associated with the larvae feeding substrate (Devic et al.,
2013). However, the fatty acid content of the BSFP meal was not
analyzed in this study as most of its lipids had been removed during the
defatting. Furthermore, a recent study showed vegetable oils perform
better in the tropical riverine carps including lemon fin barb hybrid
(Kamaruddin et al., 2012; Kamarudin et al., 2015).
5. Conclusion
Up to 75 % of BSFP meal is required as the main animal protein
source in the diet of lemon fin barb hybrid fingerlings without giving any
negative effects on their growth performance and health.
Author contributions
Mohd Salleh Kamarudin: Conceptualization, methodology, supervi­
sion, project administration, data curation, validation, funding acqui­
sition, writing-review & editing.
Suharmili Rosle: Experimentation, resources, data curation, formal
analysis, writing-original draft
Ina Salwany Md Yasin: Supervision, validation, writing-review &
editing.
Funding
This study was funded by the Ministry of Higher Education Malaysia
through FRGS Grant no. 07-01-12-1122 FR.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
The authors would like to thank the staffs of Perlok Aquaculture
Extension Centre, Jerantut Pahang, Malaysia for their cooperation and
fry supply.
References
4ento, 2015. Protein Alternatives: Insects as Mini-Livestock - #Insectmeal. Insects as a
Sustainable Commercial Protein Feed Alternative for Livestock. Retrieved 23 October
2016 from: http://4ento.com.
Abdul Rahman, K.H., Mohd Yusof, S.J.H., Zakaria, Z., 2016. Bioproteins production from
palm oil agro-industrial wastes by Aspergillus terreus UniMAP AA-1. Pertanika J.
Trop. Agric. Sci. 39 (1), 29.
9
Aquaculture Reports 21 (2021) 100775
Adenji, A.A., 2007. Effect of replacing groundnut cake with maggot meal in the diet of
broilers. Int. J. Poult. Sci. 6 (11), 822–825. https://doi.org/10.3923/
ijps.2007.822.825.
Adewolu, M.A., Ikenweiwe, N.B., Muler, S.M., 2010. Evaluation of an animal protein
mixture as a replacement for fishmeal in practical diets for fingerlings of Clarias
gariepinus (Burchell, 1822). Isr. J. Aquac. 62 (4), 237–244.
Adibmoradi, M., Navidshah, B., Seifdavati, J., Royan, M., 2006. Effect of dietary garlic
meal on histological structure of small intestine in broiler chickens. J. Poult. Sci. 43
(4), 378–383. https://doi.org/10.2141/jpsa.43.378.
Ahmed, I., Khan, M.A., 2006. Dietary branched-chain amino acid valine, isoleucine and
leucine requirements of fingerling Indian major carp, Cirrhinus mrigala (Hamilton).
Br. J. Nutr. 96 (3), 450–460. https://doi.org/10.1079/BJN20061845.
Aniebo, A.O., Erondu, E.S., Owen, O.J., 2009. Replacement of fishmeal with maggot
meal in African catfish (Clarias gariepinus) diets. Revista Cientifica UDO Agricola 9
(3), 666–671.
AOAC, 1990. Official Method of Analysis of the Association of Official Analytical
Chemists, 15th ed. Association of Official Analytical Chemists, Inc., Arlington.
Barroso, F.G., De Haro, C., Sánchez-Muros, M.J., Venegas, E., Sánchez, A.M., Bañón, C.P.,
2014. The potential of various insect species for use as food for fish. Aquaculture
422–423, 193–201. https://doi.org/10.1016/j.aquaculture.2013.12.024.
Bondari, K., Sheppard, D.C., 1981. Soldier fly larvae as feed in commercial fish
production. Aquaculture 24, 103–109. https://doi.org/10.1016/0044-8486(81)
90047-8.
Bruni, L., Belghit, I., Lock, E.J., Secci, G., Taiti, C., Parisi, G., 2020. Total replacement of
dietary fishmeal with black soldier fly (Hermetia illucens) larvae does not impair
physical, chemical or volatile composition of farmed Atlantic salmon (Salmo salar
L.). J. Sci. Food Agric. 100 (3), 1038–1047. https://doi.org/10.1002/jsfa.10108.
Cowey, C.B., 1994. Amino acid requirement of fish: a critical appraisal of present values.
Aquaculture 124 (1-4), 1–11. https://doi.org/10.1016/0044-8486(94)90349-2.
Cummins, V.C.Jr., Rawles, S.D., Thompson, K.R., Velasquez, A., Kobayashi, Y., Hager, J.,
Webster, C.D., 2017. Evaluation of black soldierfly (Hermetia illucens) larvae meal as
partial or total replacement of marine fishmeal in practical diets for Pacific
whiteshrimp (Litopenaeus vannamei). Aquaculture 473, 337–344. https://doi.org/
10.1016/j.aquaculture.2017.02.022.
De Silva, S.S., Gunasekera, R.M., Collins, R.A., Ingram, B.A., 2002. Performance of
juvenile Murray cod, Maccullochella peelii peelii (Mitchell), fed with diets of different
protein to energy ratio. Aquac. Nutr. 8 (2), 79–85. https://doi.org/10.1046/j.1365-
2095.2002.00191.x.
Devic, E., David, C.L., Leschen, W., Jauncey, K., 2013. A model for substitution of
fishmeal with maggot-meal in tilapia feeds - a commercial production farm in West
Africa. In: Paper Presented at the 10th International Symposium on Tilapia in
Aquaculture - ISTA10. Jerusalem, Israel. http://www.siamb.org.il.
Devic, E., Leschen, W., Murray, F., Little, D.C., 2017. Growth performance, feed
utilization and body composition of advanced nursing Nile tilapia (Oreochromis
niloticus) fed diets containing Black Soldier Fly (Hermetia illucens) larvae meal.
Aquac. Nutr. 24 (1), 416–423. https://doi.org/10.1111/anu.12573.
Diener, S., Zurbrugg, C., Tockner, K., 2009. Conversion of organic material by black
soldier fly larvae: establishing optimal feeding rates. Waste Manage. Resour. 27 (6),
603–610. https://doi.org/10.1177/0734242X09103838.
DOF, 2019. Perangkaan Perikanan Tahunan 2019. Department of Fisheries, Malaysia,
Wilayah Persekutuan,Putrajaya.
Dong, G.F., Yang, Y.O., Song, X.M., Yu, L., 2013. Comparative effect of dietary
supplementation with maggot meal and soybean meal in gibel carp (Carrasius
auratus gibelio) and darkbarbel catfish (Pelteobagrus vachelli): growth performances
and antioxidant response. Aquac. Nutr. 19 (4), 543–554. https://doi.org/10.1111/
anu.12006.
FAO, 2012. The State of World Fisheries and Aquaculture 2012. Food and Agriculture
Organization of the United Nations, Rome.
FAO, 2013. Edible Insects: Future Prospects for Food and Feed Security. Food and
Agriculture Organization of the United Nations, Rome.
Fasakin, E.A., Balogun, A.M., Ajayi, O.O., 2003. Evaluation of full-fat and defatted
maggot meals in the feeding of clariid catfish Clarias gariepinus fingerlings. Aquac.
Res. 34 (9), 733–738. https://doi.org/10.1046/j.1365-2109.2003.00876.x.
Fashina-Bombata, H.A., Balogun, O., 1997. The effect of partial or total replacement of
fishmeal with maggot meal in the diet of tilapia (Oreochromis niloticus) fry.
J. Prospects Sci. 1, 178–181.
Gasco, L., Gai, F., Maricchiolo, G., Genovese, L., Ragonese, S., Bottari, T., Caruso, G.,
2018. Fishmeal Alternative Protein Sources for Aquaculture Feeds. Springer, Cham.
Gatlin, D.M., 2010. Principle of Fish Nutrition. United States of Agriculture: SRAC
Publication.
Halloran, A., Roos, N., Eilenberg, J., Cerutti, A., Bruun, S., 2016. Life cycle assessment of
edible insects for food protein: a review. Agron. Sustain. Dev. 36 (57) https://doi.
org/10.1007/s13593-016-0392-8.
Halver, J.E., Hardy, R.W., 2002. Fish Nutrition, 3 ed. Academic Press, California.
Hamackova, J., Kouril, J., Kozak, P., Stupka, Z., 2006. Clove oil as an anaesthetic for
different freshwater fish species. Bulgarian J. Agric. Sci. 12, 185–194.
Hilton, J.W., Atkinson, J.L., 1982. Response of rainbow trout (Salmo gairdneri) to
increased levels of available carbohydrate in practical trout diets. Br. J. Nutr. 47 (3),
597. https://doi.org/10.1079/bjn19820071.
Idowu, E.O., Afolayan, E.B., 2013. The effects of supplementing of fishmeal with maggots
at varying levels in the diet of Clarias gariepinus. Int. Arch. Appl. Sci. Technol. 4 (4),
41–47.
Index mundi, 2016a. Fishmeal Domestic Consumption by Country in 1000 MT. Retrieved
10 August 2016.
Index mundi, 2016b. Malaysia Palm Oil Feed Waste Domestic Consumption by Year.
Retrieved 12 September 2016 from: http://www.indexmundi.com.
M.S. Kamarudin et al.
Ingram, B., Sungan, S., Gooley, G., Sim, S.Y., Tinggi, D., De Silva, S.S., 2005. Induced
spawning, larval development and rearing of two indigenous Malaysian mahseer,
Tor tambroides and T. douronensis. Aquac. Res. 36 (10), 983–995. https://doi.org/
10.1111/j.1365-2109.2005.01309.x.
Ismail, S., Kamarudin, M.S., Saad, C.R., 2016. Dietary lipid requirement of lemon fin
barb hybrid. J. Environ. Biol. 37 (Special issue), 744–765.
Kamaruddin, M.S., Ramezani-Fard, E., Saad, C.R., Harmin, S.A., 2012. Effects of dietary
fish oil replacement by various vegetable oils on growth performance, body
composition and fatty acid profile of juvenile Malaysian mahseer, Tor tambroides.
Aquac. Nutr. 18 (5), 532–543. https://doi.org/10.1111/j.1365-2095.2011.00907.x.
Kamarudin, M.S., Otoi, S., Saad, C.R., 2011. Changes in growth, survival and digestive
enzyme activities of Asian redtail catfish, Mytus nemurus, larvae fed on different
diets. Afr. J. Biotechnol. 10 (21), 4484–4493. https://doi.org/10.5897/AJB09.1895.
Kamarudin, M.S., Ismail, S., Saad, C.R., 2015. Performance of Palm Oil As Fish Oil
Replacement in the Diet of Lemon Fin Barb Hybrid Fingerlings Middle East and
Central Asia Aquaculture. World Aquaculture Society, Tehran.
Katya, K., Borsra, M.Z.S., Ganesan, D., Kuppusamy, G., Herriman, M., Salter, A., Ali, S.A.,
2017. Efficacy of insect larval meal to replace fishmeal in juvenile barramundi, Lates
calcarifer reared in freshwater. Int. Aquat. Res. 9, 303–312. https://doi.org/
10.1007/s40071-017-0178-x.
Kaushik, S.J., 1998. Whole body amino acid composition of European seabass
(Dicentrarchus labrax), gilthead seabream (Sparus aurata) and turbot (Psetta maxima)
with an estimation of their IAA requirement profiles. Aquac. Living Resour. 11 (5),
355–358. https://doi.org/10.1016/S0990-7440(98)80007-7.
Koprucu, K., Ozdemir, Y., 2005. Apparent digestibility of selected feed ingredients for
Nile tilapia (Oreochromis niloticus). Aquaculture 250 (1-2), 308–316. https://doi.org/
10.1016/j.aquaculture.2004.12.003.
Kroeckel, S., Harjesb, A.G.E., Rothc, I., Katzc, H., Wuertzb, S., Susenbetha, A.,
Schulzb, C., 2012. When a turbot catches a fly: evaluation of a pre-pupae meal of the
black soldier fly (Hermetia illucens) as fishmeal substitute — growth performance and
chitin degradation in juvenile turbot (Psetta maxima. Aquaculture 364-365,
345–352. https://doi.org/10.1016/j.aquaculture.2012.08.041.
Lall, S.P., McCrea, L.M., 2007. Role of nutrients in skeletal metabolism and pathology in
fish-an overview. Aquaculture 267 (1–4), 3–19. https://doi.org/10.1016/j.
aquaculture.2007.02.053.
Li, S., Zhang, B., Zhou, J., Ji, H., 2017. Defatted black soldier fly (Hermetia illucens) larvae
meal in diets for juvenile Jian carp (Cyprinus carpio var. Jian): growth performance,
antioxidant enzyme activities, digestive enzyme activities, intestine and
hepatopancreas histological structure. Aquaculture 477, 62–70. https://doi.org/
10.1016/j.aquaculture.2017.04.015.
Li, H., Xu, W., Jin, J., Zhu, X., Yang, Y., Han, D., Liu, H., Xie, S., 2019. Effects of dietary
carbohydrate and lipid concentrations on growth performance, feed utilization,
glucose, and lipid metabolism in two strains of Gibel carp. Front. Vet. Sci. 6, 165.
https://doi.org/10.3389/fvets.2019.00165.
Li, Y., Kortnera, T.M., Chikwatia, E.M., Belghit, I., Lock, E.J., Krogdahl, A., 2020. Total
replacement of fishmeal with black soldier fly (Hermetia illucens) larvae meal does
not compromise the gut health of Atlantic salmon (Salmo salar). Aquaculture 520.
https://doi.org/10.1016/j.aquaculture.2020.734967.
Lock, E.J., Arsiwalla, T., Waagbo, R., 2016. Insect larvae meal as an alternative source of
nutrients in the diet of Atlantic salmon (Salmo salar) postsmolt. Aquac. Nutr. 22 (6),
1202–1213. https://doi.org/10.1111/anu.12343.
Lovell, T., 1998. Nutrition and Feeding of Fish. Kluwer Academic Publishers, Norwell.
Luna, L.G., 1968. Manual of Histology Staining Methods of the Armed Forces Institute of
Phatology, third ed. McGraw-Hill Book Company, New York.
Magalhães, R., Sánchez-López, A., Silva Leal, R., Martínez-Llorens, S., Oliva-Teles, A.,
Peres, H., 2017. Black soldier fly (Hermetia illucens) pre-pupae meal as a fishmeal
replacement in diets for European seabass (Dicentrarchus labrax). Aquaculture 476,
79–85. https://doi.org/10.1016/j.aquaculture.2017.04.021.
Magnus, J.B., 2007. Thermodynamic Analysis. Forschungszentrum Jülich, Jülich.
Mhurchu, C.N., Dunshea-Mooij, C., Bennett, D., Rodgers, A., 2005. Effect of chitosan on
weight loss in overweight and obese individuals: a systematic review of randomized
controlled trials. Obes. Rev. 6 (1), 35–42. https://doi.org/10.1111/j.1467-
789X.2005.00158.x.
Mohanta, K.N., Mohanty, S.N., Jena, J., Sahu, N.P., 2009. A dietary energy level of 14.6
MJ kg− 1 and protein-to-energy ratio of 20.2 g MJ− 1 results in best growth
performance and nutrient accretion in silver barb Puntius gonionotus fingerlings.
Aquac. Nutr. 15 (6), 627–637. https://doi.org/10.1111/j.1365-2095.2008.00632.x.
Mohanty, B., Mahanty, A., Ganguly, S., Sankar, T.V., Chakraborty, K., Rangasamy, A.,
Paul, B., Sarma, D., Mathew, S., Asha, K.K., Behera, B., Aftabuddin, M.D.,
Debnath, D., Vijayagopal, P., Sridhar, N., Akhtar, M.S., Sahi, N., Mitra, T.,
Banerjee, S., Paria, P., Das, D., Das, P., Vijayan, K.K., Laxmanan, P.T., Sharma, A.P.,
2014. Amino acid compositions of 27 food fishes and their importance in clinical
nutrition. J. Amino Acids 2014, 7. https://doi.org/10.1155/2014/269797. Article
ID 26979.
Ng, W.K., Liew, F.L., Ang, L.P., Wong, L.X., 2001. Potential of mealworm (Tenebrio
molitor) as an alternative protein source in practical diets for African catfish, Clarias
gariepinus. Agric. Resour. 32 (1), 273–280. https://doi.org/10.1046/j.1355-
557x.2001.00024.x.
Ogunji, J.O., Kloas, W., Wirth, M., Schulz, C., Rennert, B., 2006. Housefly Maggot Meal
(Magmeal): An Emerging Substitute of Fishmeal in Tilapia Diets. University of Bonn:
The Centre for Development Research, Bonn, Germany.
10
Aquaculture Reports 21 (2021) 100775
Ogunji, Toor, R., Schulz, C., Kloas, W., 2008. Growth performance, nutrient utilization of
Nile tilapia Oreochromis niloticus fed housefly maggot meal (magmeal) diets. Turk. J.
Fish. Aquat. Sci. 8, 141–147.
Ogunji, J.O., Nimptsch, J., Wiegand, C., Schulz, C., Rennert, B., 2011. Effect of housefly
maggot meal (magmeal) diets on catalase, and glutathione S-transferase in the liver
and gills of carp Cyprinus carpio fingerling. Int. Aquat. Res. 3, 11–20.
Olaniyi, C.O., Salau, B.R., 2013. Utilization of maggot meal in the nutrition of African
catfish. Afr. J. Agric. Res. 8 (37), 4604–4607. https://doi.org/10.5897/
AJAR12013.7154.
Olsen, R.L., Hasan, M.R., 2012. A limited supply of fishmeal: impact on future increases
in global aquaculture production. Trend Food Sci. Technol. 27 (2), 120–128. https://
doi.org/10.1016/j.tifs.2012.06.003.
Peres, H., Oliva-Teles, A., 2005. The effect of dietary protein replacement by crystalline
amino acid on growth and nitrogen utilization of turbot Scophthalmus maximus
juveniles. Aquacultue 250 (3–4), 755–764. https://doi.org/10.1016/j.
aquaculture.2005.04.046.
Rahman, M.L., Salam, M.A., Ahsan, M.D., Hossain, M.S., Hossain, M.A., 2017. Protein
sparing ability of carbohydrates from different sources in diets for fry of stinging
catfish Heteropneustes fossilis. Sains Malays. 46 (2), 239–244. https://doi.org/
10.17576/jsm-2017-4602-08.
Ramos-Elorduy, J., Moreno, J.M.P., Prado, E.E., Perez, M.A., Otero, J.L., de Guevara, O.
L., 1997. Nutritional value of edible insects from the State of Oaxaca, Mexico.
J. Food Compos. Anal. 10 (2), 142–157. https://doi.org/10.1006/jfca.1997.0530.
Ramsden, M., 2016. Insects: A New Ingredient for Poultry Feed? Retrieved 12 January
2016, From RSK ADAS Ltd. http://www.adas.uk.
Rawski, M., Mazurkiewicz, J., Kierończyk, B., Józefiak, D., 2020. Black soldier fly full-fat
larvae meal as an alternative to fishmeal and fish oil in Siberian sturgeon nutrition:
the effects on physical properties of the feed, animal growth performance, and feed
acceptance and utilization. Animals (Basel) 10 (11), 2119. https://doi.org/10.3390/
ani10112119.
Sheppard, D.C., Tomberlin, J.K., Joyce, J.A., Barbara, C., 2002. Rearing methods for the
black soldier fly (Diptera: Stratiomyidae). J. Med. Entomol. 39 (4), 695–698.
https://doi.org/10.1603/0022-2585-39.4.695.
Siddiqui, A.Q., Mohammad, S., Howlader, Ahmad, A.A., 1988. Effects of dietary protein
levels on growth, feed conversion and protein utilization in fry and young Nile
tilapia, Oreochromis niloticus. Aquaculture 70 (1-2), 63–73. https://doi.org/10.1016/
0044-8486(88)90007-5.
Sinansari, S., Fahmi, M.R., 2020. Black soldier fly larvae as nutrient-rich diets for
ornamental fish. Paper Presented at the International Conference on Sustainable
Aquatic Resources.
Sing, K.W., Kamarudin, M.S., Wilson, J.J., Azirun, M.S., 2014. Evaluation of blowfly
(Chrysomya megacephala) maggot meal as an effective, sustainable replacement for
fishmeal in the diet of farmed juvenile red tilapia (Oreochromis sp.). Pak. Vet. J. 34
(3), 288–292. https://doi.org/10.13140/2.1.3944.0007.
Stamer, A., Weselss, S., Neidigk, R., Hoerstgen-Schwark, G., 2014. Black soldier fly
(Hermetia illucens) larvae-meal as an example for a new feed ingredients’ class in
aquaculture diets. In: Rahmann, G., Aksoy, U. (Eds.), Building Organic Bridges:
Proceedings of the 4th ISOFAR Scientific Conference at the Organic World Congress
2014. International Society of Organic Agriculture Research (ISOFAR), Istanbul.
St-Hilaire, S., Cranfill, K., Mcguire, M.A., Mosley, E.E., Tomberlin, J.K., Newton, G.L.,
Sealey, W., Sheppard, C., Irving, S., 2007a. Fish offal recycling by the black soldier
fly produces a foodstuff high in omega-3 fatty acids. J. World Aquac. Soc. 38 (2),
309–313. https://doi.org/10.1111/j.1749-7345.2007.00101.x.
St-Hilaire, S., Cranfill, K., McGuire, M.A., Mosley, E.E., Tomberlin, J.K., Newton, L.,
Sealey, W., Sheppard, C., Irving, S., 2007b. Fish offal recycling by the black soldier
fly produces a foodstuff high in omega-3 fatty acids. J. World Aquac. Soc. 38 (2),
309–313. https://doi.org/10.1111/j.1749-7345.2007.00101.x.
Suhenda, N., Tahapari, E., 1997. Penentuan kebutuhan kadar protein pakan untuk
pertumbuhan dan sintasan benih ikan jelawat (Leptobarbus hoeveni). J. Penelit.
Perikan. Indones. 3 (2), 1–9.
Teotia, J.S., Miller, B.F., 1974. Nutritive content of house fly pupae and manure residue.
Br. Poult. Sci. 15 (2), 177–182. https://doi.org/10.1080/00071667408416093.
Thestar, 2013. Wasteful Ways of Malaysian Gluttons. Retrieved 31 October 2015, from
Star Media Group Berhad http://www.thestar.com.my.
van Huis, A., 2013. Potential of insects as food and feed in assuring food security. Annu.
Rev. Entomol. 58, 563–583. https://doi.org/10.1146/annurev-ento-120811-
153704.
van Huis, A., Itterbeeck, J.V., Klunder, H., Mertens, E., Halloran, A., Muir, G.,
Vantomme, P., 2013. Edible Insects: Future Prospects for Food and Feed Security.
Food and Agriculture Organization of the United Nations, Rome.
Zarantoniello, M., Randazzo, B., Truzzi, C., Giorgini, E., Marcellucci, C., Vargas-
Abúndez, J.A., Zimbelli, A., Annibaldi, A., Parisi, G., Tulli, F., Riolo, P., Olivotto, I.,
2019. A six-months study on Black Soldier Fly (Hermetia illucens) based diets in
zebrafish. Sci. Rep. Ist. Super. Sanita 9 (8589), 1–12. https://doi.org/10.1038/
s41598-019-45172-5.
Zhou, C., Ge, X., Niu, J., Lin, H., Huang, Z., Tan, X., 2015. Effect of dietary carbohydrate
levels on growth performance, body composition, intestinal and hepatic enzyme
activities, and growth hormone gene expression of juvenile golden pompano,
Trachinotus ovatus. Aquaculture 437 (12), 390–397. https://doi.org/10.1016/j.
aquaculture.2014.12.016.