BIOTROPIA Vol. 28 No. 2, 2021: 92 - 101 DOI: 10.11598/btb.2021.28.2.1078
92
GROWTH OF BLACK SOLDIER FLY LARVAE
(Hermetia illucens) FED WITH PAK CHOI (Brassica chinensis)
AND CARP (Cyprinus carpio) RESIDUES
AGUS DANA PERMANA1, RAMADHANI EKA PUTRA1,2*, AULIYA NURULFAH2, MIA ROSMIATI1,
IDA KINASIH3, AND DIAN ANGGRIA SARI2
1School of Life Sciences and Technology, Institut Teknologi Bandung, Bandung 40132, Indonesia
2Department of Biology, Institut Teknologi Sumatera, Lampung, Indonesia
3Departement of Biology, Universitas Islam Negeri Sunan Gunung Djati Bandung, Bandung 40614, Indonesia
Received 8 June 2018/Accepted 12 February 2020
ABSTRACT
One main drawback of the local animal industry is the inavailability of affordable and sustainable protein
supply for the livestock. Insect larvae, such as the Black Soldier Fly (Hermetia illucens) larvae (BSFL), have been
considered as a protein source which can be produced at a large scale using low cost organic wastes as feeding
material. This study was designed to determine the response of BSFL to various waste combinations of vegetable
and animal remains, Pak Choi (Brassica chinensis) residues (S) and carp (Cyprinus caprio) fish offal (I)). A total of 540
BSFL were fed with 100 mg/larvae/day combination of vegetable wastes: animal waste 70%: 30% (S > I), 50%:
50% (S = I), and 30%: 70% (S < I). Among the feed combinations, the S < I group showed the best results as it
produced the significantly highest weight of BSFL at 122.8 mg/larvae and approximate digestibility of 62.01%,
with the least pupae mortality rate at 4.29%.
Keywords: bioconversion, biomass, Brassica chinensis, Cyprinus carpio, Hermetia illucens
INTRODUCTION
As the communities develop and increase in
size, the amount of waste generated by the
human population also increases. In the year
2000, about 49% of the total world population
lived in cities and generated more than three
million metric tons of daily waste (e.g.,
household items, food waste, packaging, ash)
and this number is predicted to double in 2025
(Hoornweg et al. 2013). In 2007, the amount of
food waste generated worldwide as the result of
economic activities, from production to
consumption, was estimated at 1.6 Gtonnes
(FAO 2013). These wastes are taking up space in
landfills, as the most common waste
management practice, thereby contributing to
the spread of pathogens, production of noxious
odors, and a significant amount of CO2 (Zhang
et al. 2019).
For several decades, researchers worldwide
have developed a method to process organic
matter away from landfills using biotic
decomposer such as black soldier fly larvae
(BSFL), earthworm, house fly, and mealworm
(Beard & Sands 1973; El Boushy 1991; Ndegwa
& Thompson 2001; Ramos-Elorduy et al. 2002;
Elissen et al. 2006; Diener et al. 2009), in which
BSFL is considered as the best candidate.
The black soldier fly is of Neotropic origin
and now spread in all warmer regions through
natural and human-mediated dispersal (Callan
1974; Marshall et al. 2015). This species can
colonize a wide range of organic wastes,
including agricultural wastes (Manurung et al.
2016; Supriyatna et al. 2016), animal and human
remains (Tomberin et al. 2005; Pujol-Liz et al.
2008), fish offal (St-Hilaire et al. 2007a), food
waste (Diener et al. 2011; Nguyen et al. 2013; *Corresponding author: ramadhani@sith.itb.ac.id
Growth of black soldier fly larvae fed with pakchoi (Hermetia illucens) and carp (Cyprinus carpio) remains – Permana et al.
93
Oonincx et al. 2015a), as well as human and
livestock feces (Myers et al. 2008; Banks et al.
2014; Oonincx et al. 2015b). Due to its biological
characteristic and being easily mass-produced
(Sheppard et al. 2002), this species has been
studied to recycle the nutrients found in organic
wastes to be converted into protein-rich and fat-
rich biomass (Sheppard et al. 1994; Diener et al.
2009; Li et al. 2011; Surendra et al. 2016).
Through the bioconversion process, the species
is applied as a feed ingredient for aquaculture,
livestock, and poultry industries (Newton et al.
1977; St-Hilaire et al. 2007b; Li et al. 2016;
Magalhaes et al. 2017; Renna et al. 2017;
Schiavone et al. 2017).
However, the heterogeneity of available
organic material created a challenge to the
optimization and implementation of this system,
especially in the municipal areas. Restaurant
waste, for example, containing animal and plant
matters which are rich in carbohydrate and a
similar amount of protein and fat, while mixed
fruits and vegetables are rich in carbohydrate
with significantly low-fat content. In Indonesia,
most organic wastes are produced through
economic activities in the traditional and
modern markets which are dominated by
vegetables and animal remains. Applying these
heterogeneous resources as diet for black soldier
fly would affect the development, productivity,
some life-history traits, and chemical
composition of the biomass (Tomberlin et al.
2002; Oonincx et al. 2015a; Tschirner & Simon
2015; Cammack & Tomberlin 2017).
This study was designed to imitate the real
condition in Indonesia as a model for other
similarly developed tropical countries in which
different organic wastes are produced. The
objectives of this experiment were 1) to
compare the consumption efficiency of BSFL to
diet combination of vegetable waste and animal
residues, and 2) to determine the effects of diet
composition on its growth, development time,
pupae survival, and on the adult sex ratio. The
results of this study could be used as the basis
for diet manipulation in optimizing waste
reduction, converting organic materials to insect
biomass, and sustainability of the bioconversion
system using municipal organic wastes.
MATERIALS AND METHODS
Animal Specimen
This study used the seven-day old larvae of
the black soldier fly that were obtained from
eggs purchased from a BSF farm in Sumedang,
West Java. All the eggs were kept on the
substance made of commercial chicken feed
(60% moisture) and kept at constant
temperature (28 oC, 70% RH) in a container
(50 x 25 x 10 cm) at the Laboratory of
Environmental Toxicology, School of Life
Sciences and Technology, Bandung, Indonesia.
Treatment
Each treatment (with nine replicates)
contained 60 larvae fed with 100 mg/day/larvae
(wet weight, 60% moisture content) of a diet
combination of vegetable wastes (Brassica
chinensis) and carp (Cyprinus caprio) fish offal. The
treatments were composed of diet combination
ratios of fish offal: vegetable wastes, namely;
30 : 70 ( S > I), 50 : 50 (S = I), and 70 : 30 (S < I),
and replicated 3 times. The seven-day old larvae
were initially placed into a plastic cup (with a
height of 12 cm, upper diameter 7 cm, lower
diameter 5 cm) filled with feeding material, and
covered with a black sheet. The lid of the cup
contained holes to allow air circulation. To
prevent oviposition of other flies and
parasitoids, a round dark cloth with diameter
0.01 mm was clamped between box and lid. The
diet for larvae was prepared, weighed, and kept
frozen 24 hours before the treatment to prevent
the decomposition process. All cups were kept
in a shady area. Sampling and feeding were
conducted every three days (Diener et al. 2009;
Lalander et al. 2019) during which period the
remaining larvae were transferred into another
glass already filled with the next feed. The
residual material of the previous glass was dried
at 60 oC for dry mass determination.
Feeding was conducted until more than 40%
of all larvae metamorphosed into prepupae
(Tomberlin et al. 2002; Lalander et al. 2019) while
weighing was conducted until all larva
metamorphosed into prepupae. All prepupae
were removed daily from each container and
weighed, then placed in a plastic container for
BIOTROPIA Vol. 28 No. 2, 2021
94
further rearing process into an adult. Prepupae
and pupae were held in the same incubator in
which the larvae were reared and monitored for
adult emergence daily (Cammack & Tomberlin
2017).
Data Analysis
Larvae Growth Rate and Productivity
Future production of insect larvae through
the bioconversion method highly depends on
the larvae growth rate. In this study, the growth
rate of each larva was determined by daily
biomass change (Waldbauer 1968), with the
following formula:
Growth rate = 𝐵/t (1)
where:
B = weight gain (mg)
t = development time (days)
On the other hand, the productivity of
determined by formula:
Productivity = [Dry weight of larvae/(t x V)] (2)
where:
t = larvae rearing period (day)
V = volume of rearing container (dm3)
In this study, the volume of reactor applied was
0.414 dm3.
Consumption ability
The ability of larvae to consume diet was
determined by AD (Approximate Digestibility),
ECD (Efficiency of Conversion of Digested-
feed), WRI (Waste Reduction Index), and
proportion of diet used for metabolism,
converted into biomass, and undigested.
AD parameter was used to determine the
effectiveness and larvae ability to digest the diet
which could be measured by the formula:
AD = (I-F)/I x 100% (3)
where:
AD = approximate digestibility
I = initial weight of diet (mg)
F = weight of residue (undigested food +
excretions) (mg)
The ability of larvae to digest each diet
composition was measured by ECD based on
the formulae of Scriber and Slansky (1982) and
modified by Dienar et al. (2009):
B = (I – F) – M0 (4)
ECD = B/(I – F) (5)
where:
B = the total amount of food use for growth
I = total amount of food offered during the
experiment
F = total amount of residue (undigested food
+ excretory food)
M = amount of food metabolized by larvae
(calculated by mass balance)
Dry weight was used in all calculations.
To measure overall material reduction, the
time of larvae development was required to
reduce the amount of food included in
calculation along with overall degradation (D) of
waste. All of those variables were defined as
Waste Reduction Index (WRI) which was
determined by the formula:
WRI = [(I-F)/I x 100]/t (6)
where:
I = initial weight of diet (mg)
F = total amount of residue (undigested food +
excretory), and larvae rearing period (day)
Mass Balance
Mass balance is one approach to design the
biomass production system and to predict the
digestibility of the diet. In this approach, the
total amount of feed consumed by larvae was
divided into three outputs: the mass of diet
material that is used to maintain homeostasis of
larvae, the mass of undigested diet material, and
the harvested biomass (Fig. 1).
Statistical Analysis
One way ANOVA (P ≤ 0.05) with
subsequent Tukey HSD tests were applied to
detect the difference of the means among all
treatments.
Growth of black soldier fly larvae fed with pakchoi (Hermetia illucens) and carp (Cyprinus carpio) remains – Permana et al.
95
Figure 1 Mass balance model of organic waste bioconversion into body biomass of the BSFL
RESULTS AND DISCUSSION
Black Soldier Fly Larvae Growth
The pattern of larval growth among
treatments was relatively similar as all prepupae
reached pupal stage on day 21 for all treatments.
Moreover, the larval weight of group S < I was
the highest, followed by S = I and S < I. On
average, the final weight of harvested prepupae
was 122.80 mg for group S < I which was
significantly higher than group S = I (113.88
mg) and S > I (106.89 mg) (Fig. 2).
Diet quality affects the growth and
development time of BSFL (Furmant et al. 1959;
Myers et al. 2008; Diener et al. 2009; Oonincx
et al. 2015a,b). The development time to reach
the prepupae stage could range from two weeks,
under optimal condition, to more than 3 months
if the food is limited (Table 1). In this study, the
development time of BSFL to reach the
prepupae stage was shorter than most of the
other studies (Tabel 1). Higher protein and fatty
acid content in the fish offal might have
provided the necessary nutrients for the larval
growth and metabolism (Cammack &
Tomberlin 2017). On the other hand, those
nutrients might have also encouraged the
diversity of bacterial species, some of which
might be associated with BSFL and promote
larval growth and development (Dong et al.
2009; Yu et al. 2010, 2011; Jeon et al. 2011;
Zheng et al. 2013). Furthermore, other bacteria
unassociated with BSFL, such as Escherichia coli,
Salmonella enterica, and Pseudomonas marginalis,
could have been killed by the antimicrobial
substance produced by BSFL and then used as a
source of nutrition (Erickson et al. 2004; Liu et
al. 2008; Park et al. 2015).
Figure 2 Growth pattern of BSFL
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Table 1 Comparative data on development time and efficiency of conversion of digested-feed (ECD) for black soldier
fly larvae on various substrates
Reference Substrate Development time (days) ECD (%)
May (1961) Housefly medium 18 -
Myers et al. (2008) Dairy manure 28-30 -
Diener et al. (2009) Chicken feed 16-42 24.4 - 38.0
Sealey et al. (2009) Dairy manure 120
Li et al. (2011) Dairy manure < 31
Gobbi et al. (2013) Meat meal 33
Gobbi et al. (2013) Hen feed 15
Manurung et al. (2016) Rice straw 38-52 5.69 - 10.85
Supriyatna et al. (2016) Cassava peel 20-54 12 - 21
Abduh et al. (2017a) Rubber seed - 12.5 - 25.9
Abduh et al. (2017b) Pandanus tectorius - 6.3 - 27.4
This study Combination of vegetables and fish offal 21 17.33 - 22.53
Productivity
Among all treatments, larvae of group S < I
had the significantly highest productivity (11.15
mg/larvae/day/dm3) compared to group S > I
(9.69 mg/larvae/day/dm3) and group S = I
(9.42 mg/larvae/day/dm3) (Fig. 3).
The larva of group S < I which contained
more protein has produced significantly larger
prepupae (ANOVA, P < 0.05). This conformed
with earlier studies of Diener et al. (2009),
Cammack & Tomberlin (2017). Furthermore,
the higher moisture content might have also
contributed to the higher prepupae biomass of
group S < I.
Consumption Ability
The consumption-ability of the larva was
determined by waste reduction index (WRI),
efficiency of conversion of digested-feed (ECD),
and approximate digestibility (AD). Among
treatments, the group S < I produced the
significantly highest WRI (3.13) which indicated
a higher preference of larvae to richer protein-
and-lipid- containing diet (Fig. 4). The level of
waste reduction was similar to chicken feed
(Diener et al. 2009) however, it was higher than
rice straw feed (Manurung et al. 2016) and
rubber seed feed (Abduh et al. 2017a) which
indicated the effect of diet composition to the
level of consumption by BSFL.
The effectiveness of larvae to convert
digested diet into biomass was measured by
ECD. In this study, the ECD ranged between
17.33 to 22.53% with group S < I showing the
lowest ECD (17.33%) while also recording the
significantly highest AD at 62.01% (Table 2).
Figure 3 Productivity of BSFL
Note: * = significant at P < 0.05).
Growth of black soldier fly larvae fed with pakchoi (Hermetia illucens) and carp (Cyprinus carpio) remains – Permana et al.
97
Figure 4 Waste Reduction Index of diet
Note: * = significant at P < 0.05).
Table 2 ECD and AD among different diet regimes
Diet
(100 mg/larva/day)
ECD
(Efficiency of Conversion of Digested-Feed)
AD
(Approximate Digestibility)
S = I (50 : 50) 22.53% 49.46%
S > I (70 : 30) 21.56% 45.45%
S < I (30 : 70) 17.33% 62.01%
The ECD level recorded in this study was
relatively higher than most of the previous
studies (Table 1). ECD decreased when the
quality of diet decreased (higher proportion of
undigested material, such as cellulose and
hemicellulose). However, in this study, the larval
group that consumed the protein has showed
lower ECD than the group that consumed a
cellulose-rich diet. Higher ECD manifested by
BSFL receiving an inferior diet could be a
strategy to obtain more nutrients by increasing
the consumption rate (Couture et al. 2016).
On the other hand, as shown by AD, a diet
with higher protein content was more readily
digested by the larvae which compensated for its
lower ECD. This compensation allowed the S <
I group to produce heavier harvested prepupae.
Mass Balance of Bioconversion Process
Around 4.45 to 6.66% of the substrate was
transformed into biomass, 40.99 to 55.35% was
used for metabolism, and 37.99 to 54.55% was
undigested. The highest transformation rate of
the substrate into biomass was recorded on the
group S < I (Fig. 5).
High transformation rate of the substrate to
biomass in group S < I indicated the importance
of food digestibility in the production of more
biomass.
Pupae Mortality and Adult Sex Ratio
The level of pupae mortality was low at all
groups, around 4.29 to 10.71%. The highest
mortality was recorded at group S > I (10.71%)
while the lowest in group S < I (4.29%) (Fig. 6).
The level of pupae mortality in this study was
lower than those of Tomberlin et al. (2002) and
Gobbi et al. (2013) and of Cammack and
Tomberlin (2017). Generally, the larvae of black
soldier fly are fed on a wide variety of substrates
on the larval stage and accumulate a large store
of fat to reduce and/or eliminate the need for
the adult to feed (Sheppard et al. 2002). For this
reason, the quality of diet plays a key role in the
development of adults during the pupae stage.
To produce high quality food, the larvae of
insects tend to consume a balanced diet that is
optimum for its growth and development
(Gobbi et al. 2013). This study showed that
larvae reared with the high protein diet
combined with complex carbohydrates (from
vegetable wastes) could significantly reduce the
level of pupae mortality. Furthermore, the juice
produced by the degradation of fish offal
maintained the diet moisture which highly
influenced pupae mortality, particularly for fly
species (Cickova et al. 2012; Cammack &
Tomberlin 2017).
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Figure 5 Proportion of digested feed used for metabolism, converted into biomass, and left undigested (residue)
Note: * = significant at P < 0.05).
Figure 6 Percentage of pupae mortality
Note: * = significant at P < 0.05).
Figure 7 Proportion of adult female and male
More female adults were produced than the
males for all groups although the proportion
was more balanced in S < I group with strong
differences manifested by the group receiving
the balanced feed (Fig. 7). The female-biased sex
ratio showed in this study confirmed some
earlier studies (Tomberlin et al. 2002; Zarkani &
Miswati 2012; Gobbi et al. 2013). However,
other studies reported a more male-biased adult
proportion when larva were fed with artificial
feeds (Ma et al. 2018; Meneguz et al. 2018).
Variables like pH of the substrate, nutritional
variability, and feeding regime were probably the
factors that govern the sex ratio of adult flies
Growth of black soldier fly larvae fed with pakchoi (Hermetia illucens) and carp (Cyprinus carpio) remains – Permana et al.
99
(Quezada-Garcia et al. 2014; Ma et al. 2018;
Meneguz et al. 2018). Strong differences on the
sex ratio related with substrate differences in
this study are against some previous studies
reporting the insignificant effect of diet quality
and content to the sex ratio of black soldier fly
(Tomberlin et al. 2002; Gobbi et al. 2013; Diener
et al. 2015). However, this result agrees with the
study of Zarkani & Miswati (2012) in the
tropical region which provides some evidences
of the effect of environmental factor to the final
stage of the developmental period of BSFL.
CONCLUSIONS
Diet combination consisting of a higher
proportion of protein and lipid has resulted in a
higher weight of harvested prepupae and the
lowest mortality of the black soldier fly which
was probably due to a higher consumption rate
and approximately higher digestibility. To
improve the sustainable production of the feed,
further studies are suggested on the rearing
environment of larvae particularly, on reducing
the mortality rate of pupae brought about by the
bioconverted waste that is high in protein and
lipid; on the effect of various waste materials to
biomass production and sustainability; and on
the composition of biomass.
ACKNOWLEDGMENTS
This study was partly and equally supported
by Riset ITB 2013 and Hibah Kompetensi 2018
granted to the corresponding author, P3MI
funding granted to the first author, and DIPA
BOPTAN UIN Sunan Gunung Djati Bandung
granted to the last author.
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