Biomass Conversion and Biorefinery

[Link]

ORIGINAL ARTICLE

Bioconversion approach for the valorization of Jatropha curcas seed

cake into biodiesel using black soldier fly (Hermetia illucens) larvae
Leonel Brice Wandji Nono1,5 · Julius Kewir Tangka1 · Serges Bruno Lemoupi Ngomade2,3 ·
Boris Merlain Kanouo Djousse1 · Dolvine Nguemfo Dongmo2 · Neeraj Atray3,4

Received: 1 October 2023 / Revised: 14 December 2023 / Accepted: 15 December 2023

© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2024

Abstract
The aim of this study was to assess the biodiesel potential of black soldier fly larvae (BSFL)-fed Jatropha curcas seed cake
(JCSC). The larvae were fed with JCSC that had undergone three different treatments (biological, thermal, and thermobio-
logical) and an untreated control group. Every 4 days for 15 days, the larvae were fed treated and untreated JCSC at a rate of
90 g of JCSC per 550 larvae. The highest survival rate (98.42 ± 1.21%) was obtained with untreated JCSC. The oil content
of larvae from each treatment was 32.86 ± 0.42% for untreated JCSC and 31.84 ± 0.67%, 32.16 ± 0.17%, and 31.43 ± 0.19%
for biologically, thermally, and thermobiologically treated JCSC, respectively. The oil extracted from larvae from untreated
JCSC (with the highest fat content) was converted to biodiesel by a two-step transesterification process. Fatty acid methyl
esters were identified using gas chromatography/mass spectrometry (GC/MS) analyses. Furthermore, the nuclear magnetic
resonance (NMR) and Fourier-transform infrared spectroscopy (FT-IR) analyses of BSBL oil showed the presence of car-
boxylic acids and ester carbonyl functional groups. In addition, the physicochemical properties of biodiesel from BSFLO
were analyzed, and properties such as density (875.5 kg/m3), flash point (154 °C), iodine value (94.48 g­ I2/100 g oil), calorific
value (39.87 MJ/kg), cetane number (52.53), and induction time (14.57 h) were all within the standards set by ASTMD6751.

Keywords Jatropha cake · Black soldier fly larvae · Bioconversion · Transesterification

Abbreviations BSFLO-B Black soldier fly larvae oil biodiesel

FT-IR Fourier-transform infrared GC/MS Gas chromatography/mass spectrometry
ANOVA Analysis of variance FAME Fatty acid methyl esters
AOAC Association of Official Agricultural Chemists
NMR Nuclear magnetic resonance
ASTM American Society for Testing and Materials 1 Introduction
BSFL Black soldier fly larvae
BSFLO Black soldier fly larvae oil Energy demand is a challenge of great importance nowadays.
According to the statistics of British Petroleum [1], the share
of emerging economies in global oil demand will increase
* Leonel Brice Wandji Nono
bricewandji83@[Link] from 55% in 2021 to around 70% in 2050. This ever-increas-
ing demand is influenced by population growth and develop-
1
Renewable Energy Laboratory, Agricultural Engineering ment [2]. As stated in the 2015 United Nations report, the
Department, Faculty of Agronomy and Agricultural human population is estimated to grow from 7.3 billion to
Sciences, University of Dschang, Dschang, Cameroon
9.7 billion by the year 2050 [3]. This constantly increasing
2
Department of Chemistry, Noxious Chemistry demand is covered at 80% by fossil energy sources [4], and
and Environmental Engineering Research Unit, Faculty
of Science, University of Dschang, Dschang, Cameroon according to British Petroleum [5], the demand for fossil
3 fuel represents more than 96% of the current primary energy
Biofuel Division, CSIR-Indian Institute of Petroleum,
Dehradun 248005, India demand. This source of energy is present in all sectors of
4 activity and is the cause of some geopolitical conflicts in the
Academy of Scientific and Innovative Research (AcSIR),
Ghaziabad 201002, India world [6]. In addition, the use of this fossil energy source
5 largely contributes to the increasing level of ­CO2 in the
Dschang, Cameroun

Vol.:(0123456789)
 Biomass Conversion and Biorefinery

atmosphere, which is directly linked to global warming [7]. 0.012 ­m2/year. This assertion is confirmed by Mohan et al.
Another disadvantage of this fossil energy source is that the [20], who maintain that, compared with soybean, rapeseed,
places where they are used are very far from the production palm, and microalgae, which occupy a land area of 636,
sites. As a result, due to the poor state of road networks in 974, 536.6, 741, and 97,800 L of oil/ha/year, respectively,
poor countries, the distribution of these energy sources is bioconversion by BSFL produces 162,000 L of oil/ha/year,
almost impossible in certain regions. Faced with this situa- although numerous studies have been carried out on bio-
tion, renewable energies present themselves as a promising diesel production from manure, organic waste [21], food
alternative to the use of fossil energy resources. waste, catering waste [22], pre-treated sewage sludge [23],
In 2011, approximately 95% of global biodiesel produc- and many other substrates [21, 24].
tion was produced using edible oilseeds [8]. This first gen- This work aims to contribute to the energetic valorization
eration of biofuels competes with human food. Faced with of biomass, in particular of Jatropha curcas seed cake by
this limit, a second generation of biofuels is produced based BSFL for biodiesel production. The effects of different pre-
on inedible oil seeds such as castor seeds, microalgae, and treatments on the proximate characteristics of Jatropha cakes
Jatropha curcas seeds [9–11]. Using non-edible oilseeds for were studied. The ability of BSFL larvae to decompose Jat-
biodiesel production induces increasingly large quantities of ropha curcas seed cakes despite their toxicity was evaluated
cake which are not sufficiently valued despite their richness as well as the effect of the treated cake on the proximate
in mineral elements and proteins [12, 13]. properties of the larvae. The novelty of this work is, on the
As for Jatropha curcas, the seed cake represents about one hand, the use of toxic biomass for larval nutrition and,
71.6% of the total mass of the seed [11]. Due to their toxic- on the other, the use of the oil extracted from the larvae
ity, Jatropha curcas seed cakes are not sufficiently valued for biodiesel production. This had not yet been investigated.
and are unsuitable for animals feeding without prior treat- The physicochemical properties of the biodiesel produced
ment [10]. According to Nesseim [10], fungal used in bio- were determined and compared with the ASTM standard.
logical treatment (Aspergillus niger, Penicillium) allows to The biodiesel was then tested using gas chromatography/
decrease phorbol esters content to 77%, curcine content to mass spectrometry (GC/MS), nuclear magnetic resonance
92.4%, trypsine inhibitor to 68.3%, and saponine to 95%. spectroscopy (1HNMR), and Fourier-transform infrared
Turcine and trypsin inhibitors are inactive more than 98% at spectroscopy (FT-IR).
121 °C during 25 min of heating. Despite the treatments, the
incorporation of these cakes in animal feed remains limited:
6.5% cockerel feed [12] and 2.5% and 5 to 10% soybean seed 2 Materials and methods
cake for rabbit feed and chicken feed, respectively [10]. The
literature presents a few techniques for the energy recovery 2.1 Origin of the materials used
of these seed cakes, like combustion, which produces up to
18 MJ of heat per kilogram [13]. By so doing, this technique The larvae used in this study came from the larvae breeding
under-exploits the richness of nutrients present in this cake. farm of the renewable energy laboratory of the Faculty of
According to Grimsby et al. [14], biomethanation, which pro- Agronomy and Agricultural Sciences of the University of
duces between 200 to 289 L of biogas per kilogram of meals, Dschang, Cameroon. Jatropha seeds were obtained from a
makes it a costly technology for people in poor countries. producer in the locality of Kumbo, in the North West region
Biradar et al. [15]. evaluated pyrolysis for biochar and syn- of Cameroon. The seeds were seeded using a mechanical,
gas production and concluded that this technique, although hydraulic cylinder press. Methanol (99.8%), ethanol (99%),
interesting for the production of agricultural amendments, is potassium hydroxide, sodium hydroxide (85% purity), sul-
not well mastered, and the cost of installing pyrolysis equip- furic acid (98%), phenolphthalein, and diethyl ether were
ment strongly limits their uses. Faced with the limits of these all purchased from Thermo-Fisher Scientific PVT Limited
processes on energy recovery of Jatropha seed cakes, biocon- in Mumbai, India.
version by black soldier fly larvae (BSFL) presents itself as
an up-and-coming alternative because of their triple applica- 2.2 Experimental methods
tions: it does not only enable the production of inexpensive
larval biomass and very rich in proteins that can replace fish 2.2.1 Treatment applied Jatropha curcas seed cake
and soybean cake [16] but can also serve as a raw material
for the production of biodiesel: 15.5 to 34.8% oil [17, 18]. Jatropha curcas seed cake has undergone three treatments:
Another important advantage of BSFL biodiesel is that it biological treatment, thermal treatment, and thermobiologi-
occupies very little agricultural land. Liew et al. [19] stated cal treatment. These treatments aim to reduce the toxic load
that 1 MJ of BSFL biodiesel requires around 0.0011 m ­ 2/year, (phorbol ester and anti-nutrients) in Jatropha curcas seed
whereas tobacco biodiesel requires 10 times more land, i.e., cake in accordance with Brand et al. [25] and Eroarome et al.
Biomass Conversion and Biorefinery

[26]. Untreated cake was used as a control. The biological larvae were harvested, washed, and weighed using a 0.01 g
treatment consisted of solid-state fermentation of Jatropha precision electronic scale. The ability of black soldier
curcas seed cakes with a 65% water content between 28 fly larvae to bio-convert Jatropha seed cakes was stud-
and 30 °C for 7 days in the dark. Aspergillus niger hav- ied by determining from each treatment the survival rate
ing a concentration of 1.7 × ­108 spores/mL was used as (SR) using Eq. (1), the waste reduction rate (WRR) using
a biological agent. It was done according to the protocol Eq. (2), and the bioconversion rate (BR) of Jatropha seed
described by Brand et al. [25]. Fermentation was stopped cake in larval biomass using Eq. (3):
after 7 days by drying at 70 °C for 12 h [27]. To keep the
number of larvae harvested
fermentation temperature between 28 and 30 °C, we used a SR = × 100 (1)
number introduced 4 day old larvae
100 W heating resistor as a heat source in a wooden crate
measuring 150 × 70 × 50 cm. This resistance was powered
by a photovoltaic solar system. The temperature was auto-
( )
weight of substrate residue
WRR = 1− × 100 (2)
matically controlled using an Arduino Uno module equipped weight of substrate added
with a temperature sensor (DHT22). The heat treatment was
carried out in accordance with the protocol described by wet weight of harvested larvae
Eroarome et al. [26] and adopted by Treboux [13]. The fol- BR = × 100 (3)
initial dry weight of substrate added
lowing parameters were used: the cake with 66% water con-
tent was heated to 121 °C for 30 min. The thermobiological The study of the proximate composition of the different
treatment was a combination of both biological and thermal treated cakes, having undergone the various treatments as
treatments. In this treatment, the cakes went through thermal well as those of the larvae resulting from the bioconver-
treatment followed (after cooling) by biological treatment. sion of these cakes, was carried out. Dry matter, organic
The experimental period was determined according to the matter, crude protein, and fat were evaluated as described
required time for BSF larvae to reach maturity, which was by the AOAC standard [28] methods. Fibers in the seed
approximately 15 days. During the experiment, four rep- cake were carried out using the Van Soest method [29] to
licates were carried out for each treatment, and four other determine neutral detergent fiber, acid detergent fiber, acid
treatments were carried out for the untreated seed cake for detergent lignin, cellulose, and hemicellulose. Following
the control. this analysis, the treatment selected to produce the larvae
required for biodiesel synthesis will be the one that pro-
duces the larvae with the highest oil content.
2.2.2 Bioconversion of Jatropha cake by black soldier fly
larvae

Four groups of 4-day-old larvae (0.0018 g of average weight)

2.3 Oil extraction
were fed with Jatropha seed cakes from these four different
The larvae extracted from the treatment of Jatropha cakes
treatments. Ninety grams of treated seed cake was served
showing the best fat yield were washed in fresh water
to 550 individuals every 4 days per treatment. Feeding was
and then sacrificed in boiling water (100 °C) for 40 s,
stopped when 40% of larvae of each treatment reached the
as indicated by Caligiani et al. [30]. Deactivated larvae
pre-pupal stage, as reported by Gao et al. [24]. The feed-
were dried in an electric dehydrator (oven) at 45 °C for
ing process took place in circular plastic containers (with a
2 days. Afterward, oil extraction from the larval biomass
diameter of 30 cm and height of 12 cm) covered with mos-
was carried out at 40 °C using a mechanical screw press.
quito nets to avoid predators and house fly larvae in the con-
This extraction method was chosen for its speed, low cost,
tainers. The process was carried out in a greenhouse whose
and environmental friendliness, compared with chemical
internal temperature was between 25 and 30 °C with a rela-
extraction, which is more costly, takes longer to extract,
tive humidity between 65 and 75%. To ensure the reliability
and is less environmentally friendly. Black soldier fly
and reproducibility of the results, this process was replicated
larvae oil (BSFLO) was filtered using a coffee filter at a
four times.
30 °C temperature. Extraction efficiency was evaluated
using Eq. (4).
2.2.3 Bioconversion parameters and bromatological mOE
property
ηoil =
mdry
× 100 (4)

Upon completing the feeding process with the Jatropha

cakes from the different treatments, the fully developed
 Biomass Conversion and Biorefinery

where 𝜂oil was the oil yield, msec was the dried larvae sample, 2.5.2 Transesterification in a basic homogeneous catalysis
and mOE was the extracted oil mass from the dried larva
sample. The catalytic reaction between BSFLO (%FFA < 1) and
methanol was carried out in a round-bottomed two-neck
2.4 Statistical analysis flask coupled to a magnetic stirrer and a condenser. For this
experiment, the temperature was controlled by soaking the
Data from each treatment were submitted to the analysis of flask in a silicone oil bath. The catalyst (KOH) was first
variance (ANOVA) test after prior confirmation of homoge- mixed with methanol, and the resulting mixture was stirred
neity of variance and normality. This is to check whether or for 30 min to release the methylate ions. The mixture catalyst
not there is a significant difference between treatments. The methanol was added to 100 g of preheated BSFLO, and the
means separation and classification were performed using reaction started immediately. The reaction temperature was
Duncan’s multiple range test. The software used for all these set at 65 °C. After 2 h of response, the resulting product
analyses was IBM SPSS Statistics 20, at a threshold level of (biodiesel and glycerol) was poured into a decantation fun-
5%. All data are presented as means ± standard deviation. nel, cooled, and decanted for 24 h. The upper phase contain-
ing the black soldier fly larvae oil biodiesel (BSFLO-B) was
recovered and subjected to multiple rinses with hot water to
2.5 Production of biodiesel eliminate any impurities. Following the washing process, the
biodiesel was dried in an oven at a temperature of 105 °C
Due to the high acid index (6.34 mgKOH/g) of the fat from for 4 h, enabling the evaporation of any remaining water and
BSFL fed with Jatropha cakes, a two-step transesterification methanol. The yield from the transesterification reaction was
was carried out in agreement with Q. Li et al. [9, 31]. and determined using Eq. (5).
W. Li et al. [32]. and then taken up by Tangka et al. [6]. This
method consists of using an acid-catalyzed esterification fol- Mb
Yield = × 100 (5)
lowed by a base-catalyzed transesterification. The protocol Mh
used is described as follows:
where Mb is the produced biodiesel mass and Mh is the
BSFLO mass used for biodiesel synthesis. Figure 1 presents
2.5.1 Esterification in acid catalysis the diagram summarizing this study.

Four hundred grams of filtered BSFLO was measured and 2.6 Characterization of oil and biodiesel
transferred to the two-necked flask and mixed with sulfuric
acid (1 wt% oil) and methanol in a methanol/BSFLO molar 2.6.1 Physical and fuel properties
ratio of 8:1 at a 65 °C temperature. After 1 h of reaction, the
product obtained was allowed to separate into lower organic The physical and fuel characteristics of BSFLO-B synthe-
and upper aqueous catalytic phases. After separation, sized from BSFLO were determined using the American
BSFLO (FFA < 1%) was collected for transesterification. Society for Testing and Materials (ASTM) procedures.

Fig. 1  Sketch of the study process

Biomass Conversion and Biorefinery

These characteristics are density, specific gravity, kinematic 2.6.4 Gas chromatography/mass spectrometry (GC/MS)
viscosity, cloud point, pour point, flash point, calorific value, analysis
acid value, iodine value, peroxide value, and water and sul-
fur content. The analysis to measure the concentration of the content
of fatty acid methyl esters (FAME) of BSFLO was carried
out on a 6890 series GC associated with a mass spectrom-
2.6.2 Fourier‑transform infrared (FT‑IR) analysis eter, model MS-5973 MSD. The separation was done on a
DB-5MS capillary column (30 m × 0.32 mm, 0.25 µm film
Using a Fourier-transform infrared spectrometer (Thermo thickness). The carrier gas used was helium at a 1.5 mL/min
Scientific Nicolet iS5 FT-IR), the IR spectra of BSFLO and flow rate. The injection was carried out at a temperature of
BSFLO-B produced were obtained to determine the func- 250 °C. Programming of the GC oven was thus the tempera-
tional groups. KBr was combined with the sample (0.2 to ture increased by 60 °[Link]−1 at 150 °C, by 4 °[Link]−1 at
0.4 mg) for each test to get a consistent mixture. The IR 190 °C, and by 7 °[Link]−1 at 250 °C. A volume of 0.1 μL
spectrum scan was performed in the wave number range of of BSFLO in ­CHCl3 was injected in split mode, with a split
500 to 4000 ­cm−1 using OMNIC Specta software. ratio of 1:10. The mass spectrometer was tuned to scan in the
50–550 m/z range with electrons in impact ionization mode.
2.6.3 Nuclear magnetic resonance (NMR) analysis

An NMR spectrometer (Bruke, 600 MHz) and a 5-mm- 3 Results and discussions
diameter NMR tube were used to obtain the 1H NMR spec-
tra of BSFLO and its biodiesel. The sample (10–20 mg) 3.1 Effects of different pre‑treatments
was placed into an NMR tube and diluted with 500–600 on the proximate characteristics of Jatropha
µL of deuterated chloroform (­ CDC13). Tetramethylsilane cakes
(TMS) was applied as an internal standard. As an inter-
nal benchmark, the chemical shift of the ­CDCl3 peak was The study of the proximate composition and the determina-
noticed at 7.26 ppm. Scan number (NS), 16; spectrum width, tion of the fibers of Jatropha curcas cakes treated differently
12,019 Hz; line broadening for exponential window func- are illustrated in Fig. 2.
tion, 0.3 Hz; relaxation time, 5 s; and temperature, 299.6 K From these results, it appears that the untreated cakes
have been set as standard parameters for the scan. have the highest dry matter (94.74 ± 0.28%), organic

Fig. 2  Comparative study of the proximate composition and the analysis of the fibers of treated Jatropha seed cake (TO untreated seed cake, TT
thermal treatment, TB biological treatment, TTB thermobiological treatment)
 Biomass Conversion and Biorefinery

matter (93.61 ± 0.56%), fat (24.64 ± 0.08%), crude fiber 3.2 Effect of treatment on growth parameters
(59.35 ± 0.23%), and hemicellulose (19.93 ± 0.11%) per- of black soldier fly larvae on Jatropha curcas
centage. In addition, all the treatments contributed to cakes
reducing the residual fat content contained in the meals.
It went from 24.64 ± 0.08% in the untreated cakes to Larvae reared on Jatropha seed cake appear to develop simi-
20.62 ± 0.07%, 16.91 ± 0.03%, and 17.48 ± 0.04% in the larly to the pre-pupal stage compared with previous stud-
cakes that had undergone heat treatment, biological treat- ies conducted with the solid residual fraction of restaurant
ment, and thermobiological treatment, respectively. For waste. In this study, 40% of 4-day-old larvae reached the
these treatments, that is a reduction of 4.02%, 7.73%, and pre-pupal stage within 10 days. This is in line with the work
7.16%, respectively. This can be explained by the fact that of Gao et al. [24]. The faster development indicates that
the fungi that developed in the meal during the biological Jatropha seed cake may be a good diet for black soldier fly
treatment operation consumed the fat for their growth. The larvae compared with other substrate types, such as restau-
biological treatment has the highest crude protein content rant waste, as reported by Zheng et al. [8].
(24.64 ± 0.08%), which is an increase of 1.96% compared The growth parameters of the larvae from the different
to the untreated meal, which is 22.06 ± 0.27%, very close treatments were studied, and the results are presented in
to 24, 54% obtained by Staubmann et al. [33], and 24.3% Table 1. Initial observations reveal that the organic treat-
obtained by Kongkasawan et al. [34]. On the other hand, ment has the highest dry prepupa mass and the highest sur-
this protein content is higher than the 12.55% reported by vival and bioconversion rates compared with the control
Guedes et al. [35]. for cakes from whole seeds. The aug- and other treatments. On the other hand, untreated Jatropha
mented protein content can be attributed to the growth of seed cake has a higher waste reduction rate (37.16 ± 0.68%)
fungi, in particular Aspergillus niger, with was used for followed by thermal treatment (35.80 ± 1.74%), biological
biological treatment. This increase in protein content is treatment (34.69 ± 0.12%), and thermobiological treatment
less than that obtained by Nesseim [10], which was 7.5%. (30.49 ± 0.80%). Although there was no significant differ-
This difference is mainly due to the type of seed cake used ence (p > 0.05) between treatments according to the two-way
in the experiment. In this study, the Jatropha seed cake ANOVA, the biological treatment showed the best growth
of the whole seed (kernel + hull) was used, while Nes- parameters. This may be explained by the prior activity of
seim [10] used an almond cake (without shells). Jatropha the biological agent (Aspergillus niger), which weakened
sheaths used in this study consisted of 61.25% almond the macrostructure of the oilcake, making nutrients more
very rich in protein and 38.75% shell rich in lignin, similar accessible to the larvae. Against all expectations, the ther-
to those obtained by Becker, which was 65% almond [36] mobiological treatment showed the poorest results, followed
and 35% hull versus 58% almond and 42% hull obtained by by the thermal treatment. The post hoc Tukey test indicates
Temesgen [37]. This also explains the low crude protein that there was no difference between untreated seed cake
content of close to 24.3% obtained by Kongkasawan et al. undergoing biological and thermal treatment for larvae dry
[34]. and partly the high residual fat content of the seed weight, waste reduction rate, and bioconversion rate. Moreo-
cake used in this study in comparison with those obtained ver, there was a difference between the thermobiological
by Sogang et al. [38], which was 22.47% for press cakes treatment and the other three treatments for the above param-
at 25 °C and pressure of 422.06 bars. The presence of the eters. This suggests that heat, while reducing the levels of
shells, which are essentially made up of lignin, contributes anti-nutritional factors (turcine and trypsin inhibitor), does
to lowering the crude protein content, and during tritura- not promote better bioconversion than biological treatment.
tion, it fixes the oil particles and contributes to increasing The one-way ANOVA analysis shows that the survival
the residual oil content in the cake. rate of the larvae in this investigation was not influenced by

Table 1  Growth parameters of larvae from various treatments

Parameters Untreated Biological treatment Thermal treatment Thermobio-
logical treat-
ment

Larvae dry weight (g) 34.33 ± 0.33a 35.00 ± 0.56a 33.67 ± 0.88a 29.00 ± 2.51b
Waste reduction rate ( WRR ) (%) 37.16 ± 0.68a 34.69 ± 0.12a 35.80 ± 1.74a 30.49 ± 0.80b
Larval survival rate (SR) (%) 92.12 ± 1.49a 98.42 ± 1.21a 93.81 ± 1.81a 90.66 ± 1.48a
Bioconversion rate (BR ) (%) 35.91 ± 1.30a 37.28 ± 0.84a 33.96 ± 0.71a 30.63 ± 2.70b
a,b
Means with the same letter in the row are not significantly different (p > 0.05)
Biomass Conversion and Biorefinery

the different treatments carried out. Nonetheless, the post the protein contents in the current work were included in
hoc Tukey test confirmed that there was no significant dif- intervals 44.94 ± 0.21% and 45.75 ± 0.31%. This difference
ference between all the treatments concerning the survival may be attributed to the different natures of the substrates
rate. This suggests that Jatropha seed cake, although toxic to fed. According to these observations, BSFL feeding with
monogastric animals, is not harmful to BSFL [11, 32]. These Jatropha seed cake, with its slightly higher crude protein
different larval survival rates from these treatments were content and high fat (32.08 ± 0.25%) contents, can be an
higher than that obtained by Nguyen et al. [39]. in house- alternative source of protein in animal nutrition [16, 42] and
hold waste (47%) and in fruit and vegetable waste (77%) but a very cheap raw material for biofuel production [34, 43].
comparable to those obtained by Lalander et al. [40]. with
chicken feed (93.0 ± 2.9%), chicken droppings (92.7 ± 33%), 3.4 Oil extraction
and human feces (91.8 ± 4.5%). According to Ojeda-Avila
et al. [41], larvae depend on the larvae’s accessibility to food BSFL oil yield from untreated cakes obtained by mechani-
sources and the type of food they eat. cal pressing was 20.74% of the dry larvae mass, which was
less than 32.86 ± 0.42% obtained by chemical extraction
3.3 Effect of the treated cake on the proximate (Soxhlet method). The drop in oil yield recorded during the
properties of the larvae mechanical extraction could be explained by the losses due
to the mechanical pressing system and the losses recorded
After various treatments, the results of the proximal prop- during the filtration operations. This value (32.86 ± 0.42%)
erties of the larvae from the different treatments are pre- is greater than the 30% yield obtained with BSFL fed with
sented in Table 2. For these results, it was observed that animal manure [32, 44, 45], Mechanical extraction has the
the untreated seed cakes showed the highest fat con- advantage that the extraction residues (cakes) do not con-
tent (32.86 ± 0.42%) followed by thermal treatment tain any chemical element, which can prevent their use as a
(32.16 ± 0.17%), biological treatment (31.84 ± 0.67%), and source of protein in animal feed [6].
thermobiological treatment (31.43 ± 0.19%). Regarding the
protein content, thermal treatment presented the highest 3.5 Biodiesel production
content (45.75 ± 0.31%), followed by biological treatment
(45.60 ± 0.25%), thermobiological treatment (45.46 ± 0.41), The two-step transesterification process resulted in a 97.02%
and untreated seed cakes (44.94 ± 0.21%). The one-way biodiesel yield. This yield is higher than 86.51% obtained
ANOVA analysis shows no significant difference in the fat with BSFL oil fed with food waste under a 70 °C reaction
and crude protein content of the larvae (prepupa) derived temperature in 6 h with 5% (0.25 g) H ­ 2SO4 as a catalyst and
from the cakes subjected to different treatments. Neverthe- an oil:methanol molar ratio of 1:8 [46]. This value is also
less, further post hoc Tukey’s tests showed no significant higher than the 93.1% obtained by Zheng et al. [8]. under the
difference between the treatments. This is why the untreated same conditions. According to previous results, based on the
cakes were used for the rest of the work because these treat- Jatropha seed cake used in this study, the overall biodiesel
ments did not affect the proximate composition of the larvae. yield (ratio between the weight of biodiesel produced and
This confirms that the toxic substances (ester of phorbol the weight of Jatropha seed cake initially used to obtain this
and anti-nutritional) contained in cakes have no influence biodiesel) was 4.12%, which could be higher if the cake
on the BSFL. used was almond. The average biodiesel yield obtained by
Earlier studies had reported that the protein contents of Zheng et al. [8] from the solid residual fraction of organic
BSFL were around 44.4–54.7% when feeding with low-tem- restaurant waste converted by BSFL was around 2.4%, half
perature thermal pre-treated sewage sludge [23]. Meanwhile, of that found in this study. This difference can be explained

Table 2  Proximate properties of Parameters Untreated Biological treatment Thermal treatment Thermobio-
larvae from various treatments logical treat-
ment

Dry matter (%) 95.33 ± 0.10a 95.76 ± 0.08a 95.03 ± 0.00b 95.43 ± 0.09b
Organic matter (%) 94.40 ± 0.17a 94.33 ± 0.90a 94.52 ± 0.10a 94.21 ± 0.13a
Ash (%) 5.60 ± 0.17a 5.57 ± 0.09a 5.47 ± 0.11a 5.79 ± 0.13a
Crude protein (%) 44.94 ± 0.21a 45.60 ± 0.25a 45.75 ± 0.31a 45.46 ± 0.41a
Fat (%) 32.86 ± 0.42a 31.84 ± 0.67a 32.16 ± 0.17a 31.43 ± 0.19a
a,b
Means with the same letter in the same row are not significantly different (p > 0.05)
 Biomass Conversion and Biorefinery

by the fact that the two base substrates were not the same obtained is identical to that found by Q. Li et al. [31],
and did not come from the same origin. close to 0.6 mg KOH/g obtained by Zheng et al. [8]. and
less than 1.1 mg KOH/g found by Q. Li et al. [9]. This
3.6 Characterization of biodiesel acid index equals the maximum limit recommended by
the ASMT D6751 standard (0.8 mg KOH/g) and is higher
3.6.1 Physicochemical properties of biodiesel than the maximum limit (0.5 mg KOH/g) recommended
by EN14214. The cetane number of BSFLO-B is lower
The physical and chemical characteristics of the biodiesel than the 53 reported by Q. Li et al. [9]. and 52.07 obtained
derived from BSFLO fed with Jatropha curcas cakes were by Ngomade et al. [48]. These values are between 48 and
evaluated following the American Society for Testing and 60, as recommended by ASTMD 6751–02. One of the
Materials (ASTM) guidelines. This characterization is rel- essential parameters that characterizes a biofuel is the
evant and makes it possible to limit the risks of corrosion, calorific value. The calorific value (Table 2) of BSFLO-B
filter clogging, and fuel injection problems [43]. Table 3 (39.87 MJ/kg) is lower than that of petrodiesel (42.54 MJ/
resumes the physical and chemical properties of BSFLO as kg). The presence of oxygen in the structure of biodiesel
well as those of the biodiesel obtained for this work and the compared to that of petrodiesel can account for this phe-
previous work. nomenon. Studies by Onukwuli et al. [50] show that the
Viscosity is an essential characteristic influencing fuel presence of oxygen in biodiesel certainly improves com-
lubrication, injection, and atomization [48]. An increase in bustion and reduces emissions, but it also reduces calo-
fuel viscosity is typically associated with a higher propen- rific value. In addition, the calorific values of BSFLO and
sity for engine deposits. However, the kinematic viscos- BSFLO-B, 39.56 MJ/kg and 40.13 MJ/kg, respectively, are
ity of BSFLO-B fell within the range specified by ASTM consistent with those of Ngomade et al. [48]. The ASTM
(1.9–6.0 ­mm2/s). Moreover, biodiesel with this standard D6751 and EN 14214 standards recommend an induction
can effectively lubricate engine components, which proves time for biodiesel greater than 3 and 6 h, respectively. The
advantageous for users [49]: BSFLO-B acid number of biofuel obtained from this study had an induction time of
0.83 mg KOH/g against 6.34 KOH/g for BSFLO. This 14.57 h, which was well above what the standards recom-
indicates the efficacy of the transesterification reaction in mend. Thus, from the point of view of oxidation stability,
neutralizing the free fatty acids present in the oil [48]. the biodiesel in this study complies with the ASTM D6751
This acid index value (0.83 mg KOH/g) of the biodiesel and EN 14214 standards.

Table 3  Physical and chemical characteristics of BSFLO and BSFLO-B compared to previous work and ASTMD 6751–02 and EN14214
Properties BSFLO BSFLO- BSFL ­biodiesela BSFL biodiesel BSFL BSFL Petrodiesel ASTMD 6751–02 EN14214
B bio- ­biodieselc ­biodieseld
diesel

Density (kg/m3) at 907.7 875.5 875 n.d 885 860 840 n.d 860–900
15 °C
Viscosity ­(mm2/s) 37.05 3.42 5.2 2.8 5.8 4.9 3.90 1.9–6 3.5–5
at 40 °C
Calorific value 38.59 39.87 n.d 37.9 n.d n.d n.d n.d n.d
(MJ/kg)
Cetane number 45.72 52.53 50 63.5 53 58 n.d 48–60 Min. 51
Acid value (mg 6.34 0.83 < 0.8 n.d 1.1 0.6 0.12 Max. 0.8 Max. 0.5
KOH/g)
Iodine index (g 110.89 94.48 n.d 17.4–18.3 n.d n.d n.d n.d Max. 120
I2/100 g)
Flashpoint (°C) n.d 154 121 114 123 128 97 Min.130 Min. 101
Pour point (°C) 9.0 − 12 n.d n.d n.d n.d − 13 n.d n.d
Induction time (h) 66.96 14.57 n.d n.d n.d n.d n.d Min. 3 Min. 6

n.d. not detected

a
Data obtained from Ref [47]
b
Data obtained from Ref. [23]
c
Data obtained from Ref. [9]
d
Data obtained from Ref. [8]
Biomass Conversion and Biorefinery

3.6.2 Fourier‑transform infrared (FT‑IR) analysis corresponding peak wave number characteristic of biodiesel
obtained by Tulashie et al. [53]. and Foroutan et al. [54]. is
Figure 3 shows the overlapping infrared spectra of BSFLO 1196 and 1161 ­cm−1, respectively. On the other hand, in
and BSFLO-B. In this figure, an absorption peak is observed this study, this peak was at 1010 ­cm−1 and identical to that
at a wave number of 720 ­cm−1. This peak characterizes the of Ngomade et al. [48]. This difference may be due to the
—CH2—bond deformation in oil, esters, and biodiesel. characteristics of the spectrometer used. The 2 ­cm−1 absorp-
This functional group comes from the glycerol residues of tion peak shift observed on the oil and biodiesel spectra is
the transesterification reaction. The absorption band in the identical to that observed in the literature [48].
1450 and 1165 ­cm−1 region confirms the vibration of the
­CH2 and ­CH3 aliphatic groups. Ester groups can be iden- 3.6.3 Nuclear magnetic resonance (NMR) analyses
tified at the 1743 ­cm−1 peak level with the oscillation of
1
the C = O bond (carbonyl group of the triglyceride struc- H NMR spectra of BSFLO and its biodiesel are shown
ture), while the CO group in the oil and the ester appears respectively in Fig. 4a, b. It is essential to remember that
at 1165 ­cm−1. It is essential to highlight that the presence these two samples are mixtures of esters and, therefore,
of the —O—CH3 group, indicated by the peak observed should have similar peaks. The only visible distinction is the
at 1010 ­cm−1, is evident in the spectrum of BSFLO-B but peak, which appears as a singlet at 3.65 ppm on the spectra
not in the spectra of BSFLO and ester. The absorption peak of BSFLO-B (Fig. 4b), attributed to the protons typical of
observed at 3472 ­cm−1 is assigned to the stretching vibration the methoxy group (—O—CH3). On the BSFLO spectrum
of the —OH bonds in water molecules. Given the presence (Fig. 4a), a type of proton is observed between 4.1–4.5 ppm,
of triglycerides and ester components in the composition of which appears as a doublet observed in the spectrum attrib-
the produced biodiesel, its FT-IR spectrum was compared uted to the protons of the (—O—CH2) group of triglycer-
to that of the base oil and the ester. The peak observed at ides. Note that the peak of the protons of the group (—O—
3472 ­cm−1 on the biodiesel IR curve is very weak. This peak CH2) is not observed on the biodiesel spectrum, showing the
corresponds to the elongation of the —OH group present in effectiveness of the transesterification reaction in converting
water molecules, which confirms the low water content of triglycerides into monoesters. The peaks common to the two
the produced biodiesel. We also observe a shift in the wave samples were observed at 0.86 ppm (F) for the protons of
number between oil and biodiesel IR peaks. This can be the terminating methyl group (—CH3), 1.2–1.7 ppm (E, D)
observed at wave number 722 for oil and 720 for biodiesel. for the aliphatic hydrogen (—CH2—), 2 ppm (C) for (—
This confirms the transformation of the oil into biodiesel. CH2—) close to the double bonds, 2.35 ppm (B) for (—
The distinctive absorption peaks of BSFLO have been CH2—) bonded to the carbon of the carbonyl group, and
depicted in Fig. 3, indicated by the black line. These find- 2.78 ppm (A) for —CH2— close to the unconjugated double
ings align with the results presented by Souza et al. [51]. bonds [55, 56].
and Kongkasawan et al. [34]. and show an agreement with
the findings reported by Ngomade et al. [48, 52]. in their 3.6.4 FAME profile analysis
work on Podocarpus falcatus seed oil and biodiesel. The
The chromatogram of biodiesel from BSFL revealed twelve
peaks corresponding to the different methyl esters. These
peaks were identified using Chemstation software and the
NIST database. The chromatogram in Fig. 5 shows the peaks
corresponding to the different fatty acid methyl esters in the
biodiesel. These fatty acids are shown in Table 4.
In this study, the three main fatty acids are oleic acid
(C18:1), lauric acid (C12:0), and palmitic acid (C16:0),
as reported by Ewald et al. [58]. The peak observed at a
retention time of 11.85 min is identified as being an oleic
acid methyl ester with a percentage of 42.17% resulting
from the esterification of oleic acid present in the oil of
larvae fed on Jatropha cakes. The significant abundance
of this fatty acid in the BSFLO suggests that the larvae
were provided exclusively on Jatropha cakes. The primary
fatty acid found in Jatropha oil is oleic acid [59]. This
could explain their strong presence in the cakes, which
Fig. 3  Infrared spectra of BSFLO and BSFLO-B served as food for the larvae. The fatty acid composition of
 Biomass Conversion and Biorefinery

Fig. 4  1H NMR spectrum of a

BSFLO, b BSFLO-B

the BSFLO corresponds with that of Nicholas et al. [57]. 3.7 Sustainability of biodiesel production
Table 4 presents the comparison of the fatty acid composi- by bioconversion approach
tion of the BSFLO and those of different authors. The fatty
acid composition of BSFLO varies greatly depending on In their investigation, Liew et al. [19] grouped environmen-
the diet they feed on [57]. In addition, lauric, oleic, and tal impact assessment into 3 main stages, which are the (i)
palmitic acids are highly present in BSFLO. sludge pre-treatment stage, where the waste-activated sludge
Biomass Conversion and Biorefinery

Fig. 5  Chromatogram of biodiesel from BSFL (RT retention time)

Table 4  Identification of the chemical composition of biodiesel from BSFL established by GC/MS and FAME composition of BSFL-B accord-
ing to their origin
RT (minutes) Fatty acid This study (%) Waste-activated Tobacco Bread dough [57]
sludge [23] sheaths [57]

6.05 Capric acid (C10:0) 1.22 n.d 1.1 n.d

7.78 Lauric acid (C12:0) 21.18 50.27–48.76 24.6 40.74 ± 1.25
9.13–9.23 Myristoleic acid (C14:0) 0.36 20.14–20.78 n.d n.d
9.32 Myristic acid (C14:0) 8.53 n.d 3.3 6.74 ± 0.59
10.56 7-Hexadecenoic acid, methyl ester, (Z)- 5.62 n.d n.d n.d
10.71 Palmitic acid (C16:0) 15.15 10.65–11.13 18.4 15.21 ± 0.99
10.85 12-Tridecynoic acid, methyl ester 0.21 n.d n.d n.d
11.35 Margaric acid (C17:0) 0.24 n.d n.d n.d
11.84 Oleic acid (C18:1) 42.17 11.65–11.90 24.5 9.70 ± 0.57
11.97 Stearic acid (C18:0) 4.29 n.d 8.0 1.88 ± 0.14
12.14 Linolenic acid (C18:2) 0.81 1.50–1.40 19.3 18.92 ± 1.12

n.d. not detected

was pre-treated at 90 °C for 16 h, (ii) BSFL rearing and depletion (13%), ozone depletion (13%), climate change
processing stage, and (iii) last stage inclusive of lipid extrac- (11%), and terrestrial ecotoxicity (11%). In this study, water
tion and biodiesel production. In this work, only untreated depletion was negligible because the water from a river was
Jatropha seed cake was used for biodiesel production. This filtered using a biological sand filter to remove all impuri-
means that (i) the environmental impact assessment stage ties (suspended particles) before use. Moreover, there is no
was not applicable in this case. Thus, according to Liew specific requirement on the water quality needed for washing
et al. [19], more than 50% of all ecological damages, like BSFL [19]. Regarding climate change, Liew et al. [19] report
lipid extraction and biodiesel production, were avoided, that out of the 11% of damage, 9% was caused by gaseous
representing only 1–2% of each environmental impact. This emission during BSFL rearing. For Liew et al. [19, 23] and
involves the BSFL rearing and processing stage, inflicting Mohan et al. [20], the release of ­CH4 and ­N2O contributed
the least damage to the environment. heavily to the global warming potentials of BSFL rearing.
For Liew et al. [19], under the BSFL rearing and process- On the other hand, Mohan et al. [20] indicated in their work
ing stage, the contributions of most impact categories were that BSFLs are not methane-emitting insects. This implies
well below 10%, except for water depletion (33%), fossil that the main greenhouse gas emitted during BSFL rearing
 Biomass Conversion and Biorefinery

was ­N2O, corresponding to 273 kg ­CO2 eq, as reported by CSIR-Indian Institute of Petroleum, India. The authors are very grateful
Forster et al. [60]. to Dr. Neeraj Atray for all his facilities

Author contribution Leonel Brice Wandji Nono: writing, review

and editing, writing original draft, software, project administration,
4 Conclusion methodology, investigation, funding acquisition, formal analysis, data
curation, and conceptualization. Julius Tangka Kewir: writing origi-
nal draft, validation, supervision, project administration, methodology,
This study focused on the energy recovery of biomass, in and data curation. Serges Bruno Lemoupi Ngomade: funding acquisi-
particular Jatropha curcas seed cake, by BSFL for the pro- tion, methodology, investigation, and editing. Boris Merlain Djousse
duction of biodiesel. At the end of this analysis, it emerged Kanaouo: project administration, resources, and supervision. Dolvine
that the different treatments applied to the Jatropha seed Nguemfo Dongmo: methodology, review, and editing. Neeraj Atray:
visualization and supervision.
cakes had very little effect on the proximal composition of
the cakes. The same is true for larval growth parameters, Funding This work was supported by the Third World Academy of Sci-
the highest of which (98.42 ± 1.22%) was obtained in bio- ences (TWAS) for the advancement of science in developing countries,
logically treated seed cake, followed by 93.81 ± 1.81%, under the Research Grant No. 3240321637.
92.12 ± 1.49%, and 90.66 ± 1.48% for thermal, biological, Data availability All data generated or analyzed during this study can
and thermobiological treatments, respectively. The same be available upon request. If needed, you may contact the correspond-
observations were made for the proximal composition of lar- ing author for a soft copy of the data.
vae from these different treatments. Larvae from untreated
seed cake had the highest oil content (32.86 ± 0.42%), com- Declarations
pared with 32.16 ± 0.17%, 31.84 ± 0.67%, and 31.43 ± 0.19 Ethical approval The Administration Committee of the Indian Institute
from heat, biological, and thermobiological treatments, of Petroleum, Dehradun, India, approved this study.
respectively. These results show that the phorbol esters and
the anti-nutrients contained in the Jatropha curcas cake do Conflict of interest The authors declare no competing interests.
not affect the growth parameters and the bromatological
composition of the larvae fed with these cakes. BSFL oil
yield from untreated cakes obtained by mechanical pressing
was 20.74% of the dry larvae mass. The yield of BSFL oil References
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