Optimizing Waste Management: The Impact of Pre-treatment on Black Soldier Fly Larvae for Sustainable Protein Sourcing

doi:10.21203/rs.3.rs-5324297/v1

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Optimizing Waste Management: The Impact of Pre-treatment on Black Soldier Fly Larvae for Sustainable Protein Sourcing

https://doi.org/10.21203/rs.3.rs-5324297/v1

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Amidst escalating global urbanization and population growth, the necessity to revolutionize food systems and redefine waste management strategies has become paramount. This study aimed to contribute to the evolution of protein resource diversification within animal feed and offer a sustainable solution for organic waste management using black soldier fly larvae (BSFL) in Bafia, Cameroon. A survey characterized waste production in both restaurants and households to assess their quantity and quality. Subsequently, collected organic wastes were subjected to two pre-treatments: heating (60°C) and fermentation (4 days), while another batch was used fresh as feeding substrates for BSFL in comparison to a broiler starter diet in a 17 days larval feeding experimental period. Throughout the study period, various parameters were evaluated, including physicochemical properties of substrates, bioconversion and growth parameters, life cycle traits of adult BSF, and the nutritional composition of the larvae. The survey revealed a significant disparity in food waste disposal practices: while 98% of restaurants disposed of waste indiscriminately, 95% of households reported using food waste as fertilizer.In the experimental phase, heat treatment exhibited the highest substrate temperature and pH levels throughout the experimental period. Larvae reared on heated substrates showed superior daily weight gain (0.05g/larva/day) and bioconversion rate (41.76%) compared to other substrates. Additionally, larvae from heat-treated substrates had highest lipid (35%) and protein (29.89%) contents compared to all other organic waste treatments, although his protein content remained lower than that of the chick’s starter diet, which had a higher value (37.53%). Notably, flies from larvae reared on heated substrates emerged two days earlier than those from other treatments. These early-emerging adults lived longer and produced more eggs than their counterparts. This study has revealed a stark contrast in the disposal practices of food waste between restaurants and households in Bafia. The findings underscore the potential of utilizing waste, especially after heat pre-treatment, to produce high-quality black soldier fly larvae, offering a promising avenue for sustainable protein sourcing in animal feed while addressing organic waste management challenges.

Entomology

Environmental Engineering

Household Waste

Protein Resource Diversification

Insect Larvae

Organic Waste Recycling

Sustainable Animal Feed

The persistent increase in organic wastes generated worldwide and the sustainable production of animal feed are regarded as two burning issues for human health but also for biodiversity and ecosystem preservation. Environmental concerns associated with waste treatment and animal feed in the actual production system generate high levels of waste which led to contamination of water, air, and soil (Pastor et al., 2015), and can also be a route of spreading pathogens (Pastor et al., 2015; Kawasaki et al., 2020; Tanga et al., 2021). Nowadays, organic wastes are commonly treated using landfilling, composting, or incineration (Kinasih et al., 2020 ; Kim et al., 2021). In tropical regions, landfill is the main method for organic waste management (FAO, 2013). However, there are several negative effects linked with landfills, such as the occupation of valuable space taken up by wastes, the spread of pathogenic organisms, and the production of undesirable odors as well as contribution to greenhouse gas emissions (FAO, 2013). On the other hand, inaccessibility and poor quality of feed ingredients are two of the explicative causes of high meat prices in developing countries. It is therefore necessary to look for more sustainable methods to solve waste problems efficiently while reducing feed prices. Numerous studies have underlined the use of black soldier fly (Hermetia illucens) larva as the best candidate for processing organic wastes (Kinasih et al., 2018; Lalander et al., 2019; Shumo et al., 2019; Mahmood et al., 2023) in one hand and it is also present as one of the most sustainable proteins resources for animal production in another hand. The use of BSF is well known for playing a vital role in solving issues linked with high volumes of organic waste distributed all over the world. It has progressively been employed in treating biological waste as it is seen as being an environmentally friendly and inexpensive process (Kim et al., 2021; Singh and Kumari, 2019). Ibadurrohman et al. (2020) have reported that BSFL can produce 800 g of larval biomass (protein resources) from 4 kg of waste. For higher bioconversion performance, BSFL needs to feed on organic wastes rich in digestible nutritive substances (Kinasih et al., 2020; Leong and Kutty, 2020). Bortolini et al. (2020) highlighted that the black soldier fly (BSF) system aligns with a circular economy by efficiently converting decaying organic matter into larval biomass. Additionally, the frass produced can be reused as a compost-like soil enhancer, leaving no waste at the end of the process.Moreover, the larval biomass generated through the bioconversion of organic wastes is discovered to be a high-quality source of fat/oil (Kim et al., 2021; Leong et al., 2015; Lu et al., 2021; Tanga et al., 2021) as well as proteins (Kinasih et al., 2020; Nyakeri et al., 2017; Shumo et al., 2019), and is increasingly applied in multiple industries for animal feeding, biodiesel production, biopolymers (chitin), and fertilizer (Purkayastha and Sarkar, 2021). It is noteworthy that whole or processed BSF larvae or pupae can be incorporated into the diets of poultry, fish, and pigs thereby serving as prospective alternatives to common feed ingredients such as soybean and fish-based meal (Surendra et al., 2020). Consequently, the usual feed ingredients can be reserved for other uses including human consumption thus contributing to food security (Mangindaan et al., 2022). The use of black soldier fly (BSF) larvae as bio-converters of organic waste significantly reduces waste by up to 95%, produces high-quality protein for animal feed, recycles nutrients through nutrient-rich frass, creates economic opportunities, and mitigates environmental impacts, making it a sustainable solution as waste generation increases (Rehman et al., 2022; Georgescu et al., 2020). This innovative approach sustainably address the challenges of organic waste management and enhances food security (Nguyen et al., 2021; Eggink and Dalsgaard, 2023).. As waste generation increases, the production of BSF larvae will also rise, enhancing their role in sustainable waste management and resource recovery (Eggink and Dalsgaard, 2023). Even though the potential role of black soldier fly in organic waste treatment was previously reviewed by various researchers (Pastor et al., 2015; Da Silva and Hesselberg, 2020; Kim et al., 2021; Purkayastha and Sarkar, 2021; Raksasat et al., 2020; Singh and Kumari, 2019; Surendra et al., 2020), there is still a lack of systemized knowledge about the potential of H. illucens for the waste treatment. Specific question has to be solved to optimize the mass production of BSFL. Among them the availability of waste is the sine qua non conditions for BSFL sustainability. For urban settle if has been demonstrate that the organic waste (kichen waste, market, municipal…) are available and can ensure yearly production of the larvae but in middle town and rural area it can be challenging (Nurandi et al., 2023). Additionally, the variation in waste composition reinforces the need of their pretreatment in order to optimise bioconversion parameters, nutrient content and standardise production process (Daniela et al., 2024). This study therefore aimed to characterise waste production in medium size town and the assessed the best pretreatment for maximum valorisation.

2.1 Study area

This study took place in the FASA Annex campus of the Bafia, Mbam and Inoubo division. This city has about 55 700 inhabitants. Bafia is located 473 meters above sea level, with geographic coordinates 4 ° 45'0 '' North latitude and 11 ° 13'60 '' longitude. This area is subject to an equatorial climate characterized by 4 seasons that alternate with the rainfall season (bimodal rainfall). Precipitation varies between 1 000 and 1 500 mm/year throughout the year. Temperatures are relatively constant with an average of 25° C which is optimal for BSFL production.

2.2 Animal material

The experiments utilized fertilized eggs obtained from breeding black soldier flies at the school animal farm. These flies were sourced from pupae provided by the Bilone application farm at Obala Center. Over a two-day period, eggs were collected from ruler-shaped wooden cells placed above egg-laying substrates in basins. The eggs were gathered by scraping them with a flat knife and then transferred to a jar for incubation. In this jar, we had previously added 100 grams of broiler chick starter feed (the reference feed), which was moistened to 70% with water. To prevent contamination from houseflies, the jar was covered with a canvas and sling. During the four-day incubation period, the substrate was sprinkled with water to keep it moist. By day four, we observed intense larval activity, indicating that it was time for harvest. Two days prior to harvest, we ceased watering the substrate to allow it to dry out, facilitating the separation of larvae from the substrate. On day four, we used a sieve that allowed only the larvae to pass through, enabling us to collect them for weighing.

2.3 Substrate treatments

To effectively map the waste stream in Bafia, a comprehensive survey was conducted in various restaurants throughout the city. For this study, a sample of four restaurants and 100 households was randomly selected based on their willingness to participate, family size (with a minimum of four members), and the adequacy of their waste management facilities. Surveys was conducted to target various organic waste generators, including restaurants, households, agricultural operations, and food processing facilities. This survey also captures information on the types and volumes of organic waste produced.

All collected waste was combined prior to further processing to ensure a uniform sample.Three distinct treatment methods were employed to process the organic waste before conducting bioconversion assays, informed by relevant literature and operational capabilities:

1. Heating Treatment (T1): The organic waste was heated to approximately 60°C for 10 minutes. This step aimed to eliminate all microbial activity, thereby reducing the microbial load and enhancing nutrient availability in the waste for subsequent use.

2. Fresh Waste Utilization (T2): The organic waste was utilized immediately after collection, minimizing the time for microbial action to increase and preserving its initial quality.

3. Fermentation Process (T3): The organic waste underwent fermentation for five days, allowing natural microbial action to decompose the material before it was used. This method aimed to enhance nutrient breakdown and improve the overall quality of the substrate.

Additionally, broiler chick starter feed was used as a reference feed (T4) for comparison purposes. Prior to the experimentation phase, bromatological analyses were performed to determine the composition of these treated substrates, with results summarized in Table 1. This detailed approach ensures that the study accurately captures the dynamics of waste management and bioconversion in Bafia, contributing valuable insights into sustainable practices in urban environments.

Table 1

Substrates bromatological composition
Treatments	Dry matter (%)	Ash (%)	Organic matter (%)	Crude proteins (%)
T1	91.54	5.65	94.04	20.89
T2	95.46	4.62	95.25	16.97
T3	84.74	5.76	94.24	14.65
T4	89.41	4.7	84.66	25.08
(T1), heating the organic waste at a temperature of around 50°c for 10 minutes; (T2) Serving the organic waste fresh as soon as it is collected, (T3) Fermented organic waste for 5 days; (T4) Broiler chick starter feed.

2.4 Data collection and experimental design

For the bioconversion of organic waste into larvae, plastic containers were utilized and covered with cloth to prevent contamination from domestic flies. A total of 0.6g of four-day-old larvae were introduced into 12 dishes, each containing approximately 320 larvae at a ratio of 0.05g per dish, with each treatment replicated three times. A continuous feeding strategy was implemented, wherein 100g of feed was added every two days, consisting primarily of common food waste such as cooked rice, beans, fish, vegetables, fufu corn, cassava fufu, spaghetti, and fruit peelings, all stored in sealed buckets to mitigate external contamination. The bioconversion process lasted for 13 days, during which the larvae progressed to the pupae stage; samples of 100 larvae per treatment were counted and weighed throughout the experiment to monitor weight changes. Harvesting was initiated based on the observed color change in the larvae from white to dark. At the conclusion of the experiment, larvae and substrate were separated and weighed, with larvae subsequently killed using heat and dehydrated under sunlight for preservation. A 30g sample from each treatment was collected for biochemical analysis. Approximately 100 pupae were then collected for emergence and placed in nets in a sunlit area equipped with dishes for egg-laying and water to facilitate the emergence of adult flies. This systematic approach enables the assessment of various parameters, including growth rates and bioconversion durations.

2.5 Studies parameters

2.5.1 Waste characteristics

2.5.2 Physicochemical parameters

2.5.3 Growth performance of larvae

2.5.4 Bioconversion of substrate

• Larval Survival Rate (SR): The survival rate of BSF larvae during composting was calculated using the formula:

$$\:SR\:\left(\%\right)=\left(\frac{{n}_{lv.end}}{{n}_{lv.start}}\right)\times\:100$$

Where n_lv.end is the number of BSF larvae at the end of composting and and n_lv.start is the number of BSF larvae at the start.

• Waste Reduction Rate (RR): The percentage of waste reduced on a total solids (TS) basis at the end of composting was determined as follows:

$$\:RR\:\left(\%\right)\:=\left(\frac{{m}_{in}-\:{m}_{res}}{{m}_{in}}\right)\times\:100$$

Where m_in and m_res are the masses of the inflow waste and treatment residue, respectively

- Waste Bioconversion Efficiency (BCE): The conversion efficiency of waste to larval biomass on a TS basis was calculated as follows:

$$\:BCE\:\left(\%\right)=\left(\frac{{m}_{lv}}{{m}_{in}}\right)\times\:100$$

Where m_in and m_lv are the masses of the inflow waste (in) and larval biomass (lv), respectively.

These parameters provide a comprehensive assessment of the composting process, allowing for an evaluation of the effectiveness of BSF larvae in converting pretreated waste into valuable biomass.

→ Length of larval stage: number of days between hatching and pupae formation

→ Length of adult stage: number of days between emergence and death of flies

→ Length of pupal stage: number of days from pupae formation to start of emergence

2.5.5 Nutritional composition of larvae and frass

At the end of the rearing period, a sample of 100 larvae per treatment repetition was collected, these larvae underwent manual sorting and washing with tap-water until the waste was eliminated. Subsequently, to sacrifice the larvae without considerably degrading their physicochemical and nutritional properties, they were boiled using the method described by Deschamps et al. (2019). This method consists of soaking the larvae for 5 minutes in hot water (100°C). Finally, the larvae obtained were drained and dried in an oven at a temperature of 50°C for 48 hours. After drying, the larvae were crushed using a “Silvercrest” brand blender, and the flours obtained were kept in a dry container for further analysis. A sample of 30g per repetition was collected for bromatological analysis (dry matter, organic matter, crude protein and crude ash) following the AOAC, (2000) procedure. In another hand, samples of rearing residues (frass) was collected, oven-dried at 60°C overnight, finely minced, and then analyses to determine the chemical composition. These analyses were conducted at the University of Dschang Laboratory of Animal Nutrition and production.

2.5.6 Life cycle and egg laying traits of adult flies

2.5.7 Microbiological load

From harvested larvae, 100 g of BSFL (at 91% dry matter) was used to determine the microbial composition using tenfold serial dilutions as described by Gorrens et al. (2021). The samples were immediately transported to the laboratory of animal health and physiology of the University of Dschang for bacterial culture and analysis in triplicate. The determination of the number of colonies involved a dilution with distilled water of 1 g of larval meal in 9 ml of distilled water, then 1 ml of the mixture was diluted 6 times consecutively in the test tubes also containing 9 ml of distilled water to reduce the rate of bacteria and to facilitate counting. One ml of the mixture from tubes 2, 4, and 6 was brought into contact with culture media previously heated to 60°C in a tide bath or an autoclave and cooled to 50°C. After the mixture had solidified, each jar was stored anaerobically (lactobacillus) or aerobically (salmonella, enterobacteria, and E. coli) in an incubator at 37°C. The colony count was performed twice in duplicate. The first count was 24 hours after incubation and the second 48 hours after incubation. The determination of the number of colonies was obtained by the jar which had the lowest number of spots, and then this number was multiplied by the power indicated by the number on the jar (10², 10⁴, or 10⁶).

2.6.3.6 laying rate at peak laying

The laying rate at peak laying was considered as the highest rate of laying eggs by the females. This parameter was recorded by observations and counting of eggs laying.

2.6.3.7 Peak laying production and age

The peak laying period for black soldier flies is defined as the highest rate of egg-laying observed among females on a daily basis. In order to quantify egg production, the number of individual eggs within each bundle was counted under a light microscope, whereby a sample of egg bundle was collected, weigh and eggs contained in the bundle were counted and extrapolated to the total mass of eggs bundles collected.

This method allows the accurate identification of the highest peak in egg production, which correlates with the greatest number of bundles and eggs. It is important to note that not all bundles contain the same number of individual eggs. The total number of females that laid eggs was inferred from the count of egg bundles found on the wooden trays, with the assumption that each bundle corresponds to a single female (Hoc et al., 2019).

2.6.7 Adults life duration

The duration from emergence to death of adult flies was recorded in days and represented the lifespan of the adults.

2.6.8 Daily death rate of adults

The daily death rate of the flies was calculated by dividing the daily number of deceased individuals by the total initial population size.

2.6 Statistical data analysis

Data recorded from restaurants were introduced in Microsoft Excel and expressed in the form of frequencies, whereas data recorded after experimentations (pH, temperature, growth rate, etc.) were subjected to a one-way analysis of variance (substrate type). Microsoft Excel was used for graphical representations and the software statistics SPSS (Statistical Package for Social Sciences) 20.0 was used for analysis with Duncan’s test at 5% significance.

- Quantitative and qualitative characterization of organic waste collected

Data collected from restaurants and households revealed minimal variation in the types of food waste generated, but significant differences in the quantities of this organic waste (Fig. 1). The most commonly observed food waste items included cooked rice, spaghetti, beans, fish, vegetables, fufu (made from corn and cassava), and fruit peels.The quantity of waste varied among restaurants and was influenced by location and day of the week. The highest daily amount recorded in restaurants was 17,424 g, while the lowest was 4,798 g. For households, the quantities ranged from 230 g to 102 g. Overall, approximately 329.356 kg of waste was collected throughout the survey period. Notably, restaurant waste was not treated and was simply discharged into the surrounding environment. In contrast, household waste was utilized as an amendment for agricultural purposes.- Effects of substrate type on physicochemical parameters

Temperature, pH, and relative humidity in the larval environment were significantly influenced (p < 0.05) by the substrate treatment method. The heated treatment exhibited the highest temperature range at the beginning of the experiment, while the fresh, fermented, and standard diets maintained similar temperatures throughout. The lowest humidity was observed in the fermented treatment, with its curve consistently below those of the other treatments during the experimental period. In contrast, the humidity curve for T1 (boiled diet) recorded the highest levels. Regarding pH, all treatments displayed a linear trend throughout the trial, except for the fermented diet, which exhibited a tooth-like pattern. Additionally, the standard diet recorded the highest pH value, while the lowest was found in the fermented diet.- Effects of substrate treatment type on growth performance of larvae

Then, effect of substrate treatment mode on the growth parameters BSFL is summarized in Table 2. Overall, the treatment modes significantly influenced (p < 0.05) growth parameters, with the exception of feed intake. Then, larvae reared on heated substrates achieved a greater weight (0.384 g) than those fed fresh or fermented diets, indicating a significant impact of substrate treatment mode on larval weight (p < 0.05). In terms of consumption index, significant differences were observed (p < 0.05), with the fermented diet yielding the highest index and the standard diet recording the lowest value.

Table 2

Growth performance of BSFL according to substrate treatment mode
Characteristics	Standard diet	Heated	Fresh	Fermented	p
IBW(g)	0.001	0.001	0.001	0.001	0.00
FBW(g)	0.34 ± 0.03^c	0.38 ± 0.05^b	0.315 ± 0.00^ab	0.29 ± 0.03^a	0.008
ILN	321.00	321.00	321.00	321.00	0.00
FLN	241.00 ± 5.66^a	295.50 ± 6.36^b	311.00 ± 5.66^b	308.50 ± 7.78^b	0.001
Mortality (%)	24.92 ± 1.76^c	7.94 ± 1.98^b	3.12 ± 1.76^a	3.89 ± 2.42^a	0.001
DGR (g/larva/day)	0.04 ± 0.07^b	0.05 ± 0.00^c	0.03 ± 0.00^ab	0.03 ± 0.00^a	0.008
MW (g/larva)	0.349 ± 0.21^bc	0.384 ± 0.14^c	0.317 ± 0.009^ab	0.295 ± 0.009^a	0.014
TWG (g)	0.347 ± 0.21^bc	0.382 ± 0.141^c	0.315 ± 0.009^ab	0.293 ± 0.009^a	0.014
FT (g)	1.255 ± 0.00	1.108 ± 0.00	1.154 ± 0.00	1.074 ± 0.00	0.008
CI	2.063 ± 0.088^a	2.218 ± 0.207^ab	2.669 ± 0.021^bc	2.816 ± 0.257^c	0.031
IBW: initial body weight; FBW: final body weight; ILN: initial larvae number; FLN: final larvae number; DGR: daily growth rate; p: probability; MW: mean weight; TWG: total weight gain; FT: feed taken; CI: consumption index; a, b and c: means with the same superscript in the same line are not significantly different at 0.05 significant level.

As illustrated in Fig. 4, the standard diet exhibited the highest mortality rate (p < 0.005), while the fresh substrate recorded the lowest, comparable to the fermented diet. Additionally,

- Effects of substrate type on bioconversion of substrate

The bioconversion parameters of black soldier fly larvae (BSFL) are summarized in Table 3. These parameters were significantly influenced (p < 0.05) by the treatment mode.Food waste from restaurants demonstrated a greater substrate reduction compared to the standard feed, resulting in the standard diet recording the lowest substrate reduction rate (p > 0.05). In contrast, the fresh diet derived from restaurant waste exhibited the highest substrate reduction value. A similar trend was observed in feed conversion, where the standard diet again recorded the lowest value (p > 0.05). The highest bioconversion rate was associated with the heated diet, while the lowest was observed in the fermented diet.Additionally, the table indicates that the highest reduction index was found in treatments utilizing food waste, with the fresh diet achieving the greatest value (p < 0.05) compared to the standard diet.- Effects of substrate type on the nutritional composition of larvae

Table 3

Waste bioconversion parameters and reduction of substrate according to treatment mode
Characteristics	Standard diet	Heated	Fresh	Fermented	P
SR (%)	33.004 ± 0.42^a	41.754 ± 0.60^b	44.174 ± 3.355^b	40.833 ± 2.27^b	0.021
FC	2.063 ± 0.088^a	2.218 ± 0.20^b	2.669 ± 0.021^bc	2.816 ± 0.257^c	0.031
BCR (%)	36.49 ± 0.70^ab	41.76 ± 0.98^b	36.43 ± 0.38^ab	34.366 ± 2.25^a	0.047
RI (%)	2.539 ± 0.033^a	3.21 ± 0.046^b	3.398 ± 0.258^b	3.141 ± 0.175^b	0.021
SR: substrate reduction; FC: feed conversion; BCR: bioconversion conversion rate; RI: reduction index; p: probability; a, b, and c: means with the same superscript in the same line are not significantly different at 0.005 significant level.

Table 4 summarizes the nutritional composition of the larvae, which was significantly influenced by the substrate treatment (p < 0.05). Larvae fed with heated food waste exhibited the highest values for dry matter, ash, and lipid content (p < 0.05) compared to other substrates. The dry matter content of the standard diet was comparable to that of the boiled diet. In terms of protein, the standard diet recorded the highest crude protein level (37.53 g) (p < 0.05). Meanwhile, both the fermented and fresh diets demonstrated elevated organic matter content relative to the other treatments, as detailed in Table 4.- Effects of substrate type on the nutritional composition of frass

Table 4

Nutritional composition of larvae according to treatment mode
Characteristics	Standard diet	Heated	Fresh	fermented	P
Dry matter (g/100g)	92.78 ± 0.12^bc	93.16 ± 0.113^c	91.44 ± 0.11^a	92.39 ± 0.18^b	0.001
Ash (% dry matter)	10.45 ± 0.04^c	12.49 ± 0.19^d	9.45 ± 0.08^b	9.01 ± 0.09^a	0.000
Organic matter (% dry matter)	89.55 ± 0.04^b	87.72 ± 0.19^a	90.55 ± 0.08^c	90.99 ± 0.09^d	0.000
Crude proteins (% dry matter)	37.53 ± 0.04^d	27.49 ± 0.03^a	29.88 ± 0.035^c	28.38 ± 0.05^b	0.000
Lipids (% dry matter)	27.07 ± 0.03^a	35.20 ± 0.04^d	33.46 ± 0.04^b	34.24 ± 0.06^c	0.000
a, b, c, d: means with the same superscript in the same line are not significantly different at 0.05 significant level. p: probability;

The composition of frass was significantly influenced by the treatment mode of the feeding substrates (p < 0.05), as summarized in Table 5. According to the table, the crude protein content of frass derived from fresh substrates was higher (p < 0.05) than that from other treatments. Conversely, the ash and dry matter content of frass from the standard diet was greater (p < 0.05) than that from restaurant organic waste, regardless of the treatment mode. In contrast, the organic matter content of frass from the standard diet was the lowest among all treatments studied.

Table 5

Nutritional composition of frass according to treatment mode
Parameters (g/100g)	Standard diet	Heated	Fresh	fermented	P
Crude protein	17.61 ± 0.021^b	15.96 ± 0.02^a	20.56 ± 0.09^d	17.99 ± 0.02^c	0.000
Organic matter	83.44 ± 0.57^a	92.08 ± 0.06^d	89.60 ± 0.30^b	90.83 ± 0.14^c	0.000
Ash	16.56 ± 0.57^d	7.77 ± 0.14^a	10.39 ± 0.30^c	9.16 ± 0.14^b	0.000
Dry matter	89.17 ± 0.12^d	88.21 ± 0.15^b	86.50 ± 0.40^a	87.86 ± 0.01^b	0.001
a, b, c, d: means with the same superscript in the same line are not significantly different at 0.05 significant level. p: probability;

- Effect of substrate type on the life cycle and egg laying of adult flies

The life history of the flies was significantly influenced by the treatment mode (p < 0.05). Emergence began 12 days after the flies were placed in emergence dishes. Notably, larvae fed on heated waste exhibited the highest emergence rate, starting two days earlier than those from other treatments. The shortest emergence period was observed in pupae fed heated, fermented, and fresh diets, which emerged over eleven days. In contrast, pupae from the standard diet took fifteen days to emerge, marking the longest duration. Egg production was assessed based on bundles (packages). Copulation commenced one day after adult flies emerged, with egg laying beginning the following day for all treatments except the standard diet, which started two days later. Flies fed on the heated diet produced the highest number of bundles, while those on the fermented diet produced the fewest. The longest duration of egg laying was recorded for flies on the heated diet, averaging 15 days, compared to an average of 13 days for all other treatments. Mortality began six days after emergence for flies fed on fresh and fermented diets and eight days after emergence for those on heated and standard diets. The duration of mortality was consistent across all treatments.

Effect of Substrate Type on the Life Cycle and Egg Laying of Adult Flies

The adult life history was significantly influenced by the treatment mode, with the heated diet demonstrating the highest performance. This may be attributed to the elevated energy levels accumulated during the larval stage, which also resulted in the highest egg-laying rates for adults from this treatment.

Effect of Substrate on Emergence Rate

Emergence began 12 days after the flies were placed in emergence dishes. Pupae from the boiled sample exhibited the highest emergence rate, starting two days earlier than those from other treatments. Pupae fed on heated, fermented, and fresh diets had an emergence period of eleven days, while pupae from the standard diet took fifteen days to emerge (Fig. 2).

Effect of Substrate on Egg Laying Rate

Egg production was assessed in terms of bundles (packages). Copulation commenced one day after adult flies emerged, with egg laying beginning the following day for all treatments except for the standard diet, which started two days later. Flies fed on the heated diet produced the highest number of bundles, whereas those fed on the fermented diet produced the fewest. The longest duration of egg laying was recorded for flies on the heated diet, lasting 15 days, while all other treatments averaged 13 days (Fig. 3).

Effect of Substrate Type on Death Rate

Mortality began six days after emergence for flies fed on fresh and fermented diets and eight days after emergence for those on heated and standard diets. The duration of mortality was similar across all treatments (Fig. 4).

Effect of Substrate Type on Microbiological Composition of Larvae

Table 6 summarizes the effect of substrate treatment mode on the microbiological load of black soldier fly larvae (BSFL). Larvae from the fresh diet recorded the highest levels of Enterobacteria spp., while those from the fermented diet had the lowest. For Salmonella spp., larvae from the heated sample exhibited the highest colony count compared to other treatments, while larvae from the fermented diet showed no colonies at all. Regarding Clostridium spp., larvae from the fresh diet had the highest number of colonies, whereas those from the fermented diet had the fewest; larvae from the heated diet showed no colonies.Discussion

Table 6

Microbiological load of larvae in CFU
Treatment
Heated	15×10²	80×10²	00×10²
Fresh	86×10²	06×10²	200×10²
Fermented	04×10²	00×10²	01×10²
Standard	10×10²	08×10²	30×10²

The biotechnology process using black soldier fly larvae to recycle biowaste into useful products has been widely studied (Wang and Shelomi, 2017; Nana et al., 2018, Dzepe et al., 2023); it is a sustainable way to improve waste management generating valuable products (animal protein and biofertilizer). In this study, selected life-history traits of BSF were analysed using three food waste treatment methods; (Heated, Fermented, and Fresh), and a standard feed composed of chicken broiler starter. The BSFL was successfully developed on all substrates. Surveys in restaurants and households are permitted to evaluate the situation of food waste, how it is being used or discarded, and how it can be used to produce black soldier fly larvae in the studied environment. For areas where food waste being generated is not used either for farm work or directly as animal feed (especially in households), it is discarded in nearby streams, gutters, landfills, or placed a sight for asses to local service in charge of dirt (municipal council), which still end up in dumping grounds. The area has no food waste management and these dirt’s end up polluting the environment. The quantity of dirt recorded from the chosen areas in the trial period was about 320kg.

Temperature is a very important parameter because it determines directly the growth rate of larvae and conditions the state of larvae at each stage of development. Zheng et al. (2012) mention a temperature range of 26–29ºC to be good for the rearing process. The heated treatment had the highest temperature (26ºc) for our trial and this can be explained by the intense activity of larvae. This is consistent with the conclusions of Warburton and Hallman, (2002) who stipulate that there is heat release as BSFL consumes their food substrate, which is due to intense microbial activities which causes a gradual increase in the temperature of the substrate. After 8 days, the temperature curves had the same downward trend to the end, which is explained by the reduction of the food intake by larvae when entering the pupa stage (Cheng et al., 2017) and the accumulation of ammonia in the frass. The fermented diet had a lower pH this is probably related to intense microbial activity rendering the substrate more acidic. However, all the diets had their pH around 6-6.5 which was within the normal range (6–10) as stipulated by Ma et al. (2021). The acidic pH value obtained can be explained by the quality of our substrates mainly composed of starchy compounds (maize, cassava, banana…). According to Pramanik et al., (2019) and before Alidadi et al. (2016) the degradation of sugars and lipids in a food substrate by larvae leads to the production of organic acids and carbon dioxide acidifying the Middle.

In this study, the highest mortality rate was recorded in the standard diet (24.92%). This can be explained by the particle size of this diet. The newly hatched larva showed a high preference for powdered and soft material with high protein and carbohydrate content, and are relatively unable to create pores to breathe when the substrate is too compacted (Cheng et Chiu, 2017). Food waste treatments recorded low mortality because it was composed of restaurant waste with easily accessible nutrients. Moreover, it can also be suggested that all treatment diets provide adequate conditions for BSFL.

The larvae fed on a heated diet exhibited the highest growth characteristics as compared to the rest of the diets. It is known that proteins and carbohydrates play a vital role in the development of larvae (Banks et al., 2014), so we can suggest from this that the high growth rate of the heated diet larvae was due to the increased protein bioavailability after heating. Moreover, Liew et al. (2022) revealed that thermal treatment increases the solubility of organic matter, improves biodegradability of substrates, and therefore enhances the growth of larvae. Also, the fact of heating might have affected the feed bonds thereby softening the feed to ease digestion by larvae (Roma et al., 2013). The low growth performance observed in the fermented diet might be explained by the fact that; fermentation could induce a high proliferation of microorganisms’ thereby creating a competition for nutrients with BSFL leading to a reduction in growth.

All the larvae in different treatments had the same length of days before harvest reflecting the fact that the physiochemical conditions provided by the substrates were able to fit the requirement for BSFL development. It is well known that BSFLs have a high capacity to adapt to various growth media (Peguero et al., 2021). But never the less they had different weights and sizes.

The bioconversion rate was found to be significantly affected by the type of substrate (p < 0.05). The bioconversion rate of the trial exhibited a range of 34.37 to 41%, with the highest rate recorded with the heated substrate. These values are higher than those reported by Rehman et al. (2017) in a study involving dairy cattle manure. In contrast to the dietary substrates used in this study, which were pretreated food waste, Rehman's diet was administered without any prior pretreatment. This discrepancy may account for the comparatively low results observed. These findings align with the conclusions of Ateng et al. (2016), which suggest that the valorization of fibrous feedstuffs by BSFLM larvae necessitates prior pre-treatment of these fibers. In other hand, the higher bioconversion in food waste-treated samples can be attributed to feed texture (soft and high moisture content). This supports the hypothesis that BSFL can consume organic materials from various origine if their nutritional composition and physical characteristics are optimal (Banks et al., 2014; Nyakeri et al., 2017).

Feed conversion is the quantity of feed taken and changed into larval biomass. Our results obtained (2.063–2.816) were comparable to those of Rehman et al. (2017). The lower the value of the feed conversion index, the lower the larvae to convert organic materials into larval biomass (Banks et al., 2014, Nyakeri et al., 2017).

Substrate reduction is the amount of feed used up, and our result showed that food waste treatments had the highest rate, perhaps because of the low fiber content compared to the standard diet having the lowest substrate reduction rate (33.004%) since BSFL converts less substrate composed with high fibers content (Cheng et al., 2017).

The analysis of the chemical composition of larvae clearly showed that substrates pre-treatments have significantly affectedtheir bromatological composition. According to the work of Nguyen et al. (2013); OonIncx et al. (2015), the nutritional composition of larvae depends on the quality and quantity of ingested feeds. The treatments applied on the substrate significantly (p < 0.05) influence the dry matter content of different BSFL. The highest dry mater was recorded with heated substrates. The high dry matter values obtained in this treatment suggest that they can potentially extend the shelf-life of BSFL. In the same veins, the treatments applied on substrate significantly influenced (p˂0.05) the ash content of BSF larvae flour with the lower value obtained for the fermented waste (9.01%) and the high value with the heated waste treatment (12.49%.). These values are comparable to those previously reported on BSFL 9.03–13.18% (Holeh et al., 2022; Nugroho et al., 2022). According to Vanqa et al. (2022), the difference recorded in the proximate composition of insects could be caused by the differences feed type, level of individual development, climate, and geographical location.

Concerning the lipid content, the heated substrates recorded the highest content (p˃0.05) between all the treatment assessed in this study (35.20%). This can suggest that heated process have increase nutrient avaibility for BSFL. In fact, ssubstrates with high amounts of proteins, lipids and, in general, substrates complete and balanced in all nutrients, are the best for the development of the BSF and its bioconversion performances. The amount of lipids recorded in this study can be a good indicator that oil extracted from H. illucens can supply some oil-soluble vitamins, such as vitamins A, D, E, and K.

For the protein content, the values obtained within the framework of this study vary from 32.02 to 39.11% (p˂0.05) with the greatest value obtained from the larvae fed with the no treated substrate (T0) and the lowest recorded with samples of larvae fed with the crushed substrate (T1). The drop in protein content observed in T1 and T2 could be associated with the denaturation of proteins under the effect of heat during the grinding and heat treatment of the substrates used for the production of larvae. These values are comparable to those reported by Bubler et al. (2016) on freeze-drying non-defatted H. illucens flour with a value of 34.7% on a dry basis. Furthermore, Lalander and Lopes (2024), revealed that lower temperature pre-treatments (around 50–60°C) may however be suitable before BSF larvae rearing. Recent studies on H. illucens have recorded that the rearing substrate can modulate both the crude protein content (with values ranging between 35 and 49%) (Barragan-Fonseca et al., 2021; Fuso et al., 2021). However, Kroeckel et al. (2012) recorded 54.1% crude protein content in H. illucens flour, and this value is significantly higher than that obtained in this study. It has been shown that many factors are known to affect the rearing of insects, including the number of animals placed in a designated area (also known as larval density), which correlates with their growth and development over time (Barragan Fonseca et al., 2018). Other parameters that are interconnected and impacted by larval density include nutrient availability per larva, larval feeding dose/rate, substrate depth, and moisture (Lopes et al., 2023). Barragan-Fonseca et al. (2018, 2019) showed that the higher the protein content in the larval diet, the higher the protein and fat accumulation in the larvae. Also, Lopes et al. (2020) reported that even small inclusions of fish to bread waste resulted in higher protein accumulation in the BSFL, while according to Ewald et al. (2020) the larvae accumulated more fat when fed diets with higher protein content.

Like larvae, the chemical composition of frass was significantly affected by the substrate’s pretreatment (p < 0.05). Globally, the heated substrates exhibited the highest chemical contain as compared to other treatment. This high contain offer a good compost quality for crops amendment or feed for ruminants.

The microbiological analysis of larvae revealed a low amount of microbial infection, indicating that they can efficiently be incorporated into animal feed. This low microbial colony count may be attributed to the treatment mode employed, specifically the heating of larvae prior to drying. This finding contrasts with the results reported by Jeon et al. (2011), which demonstrated a higher number of colony-forming units. This discrepancy is likely attributable to the larval treatment and conservation protocols employed in the latter study.Conclusion

In conclusion, this study highlights the significant potential of black soldier fly larvae (BSFL) for converting approximately 3.5 tons of organic food waste generated monthly in Bafia, Cameroon, into an estimated 1.98 tons of high-quality larval biomass. By employing heat and fermentation pre-treatments, we demonstrated that BSFL exhibited superior growth rates, bioconversion efficiency, and nutritional content when fed on heat-treated substrates compared to untreated or fermented waste. Notably, larvae from heat-treated diets showed enhanced daily weight gain and higher lipid and protein levels, while adult flies displayed improved life cycle traits. These findings underscore the importance of adopting BSFL as a sustainable solution for organic waste management and protein production, advocating for further research to optimize pre-treatment methods and assess the economic feasibility of large-scale BSFL systems in urban settings. However, integrating a thorough cost analysis will be vital for promoting sustainability in urban settings effectively.

Ethics approval and consent to participate

Authors strictly fellow up rule and regulation regarding animal as edited by the university of Dschang protocol.

Consent for publication

All authors read and approved the final manuscript.

Conflict of interests:

The authors declare that for this article they have no actual, potential, or perceived conflict of interests.

Funding:

This project has been funded by the Healthy Diet for Africa Programme under the Horizon Europe Research and Innovation Action Programme of the European Commission under Grant Agreement No. 101083388.

Author Contributions:

M.K.H., generated the research idea, designed the study, designed and conducted the data collection and analysis, interpreted the results, and wrote the manuscript. G.F.L., participated in the design of the study, data collection, analysis, and reading of the manuscript. D.D., S.C.H.N and S.Y.C participated in the design of the study and reading of the manuscript. K.J.R., and K.A participated in the overall design process. S.A.N. and D.F.R participated in the writing of the manuscript.

Availability of data and materials

The datasets during and/or analyzed during the current study available from the corresponding author on reasonable request.

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Optimizing Waste Management: The Impact of Pre-treatment on Black Soldier Fly Larvae for Sustainable Protein Sourcing

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Abstract

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INTRODUCTION

MATERIAL AND METHOD

2.1 Study area

2.2 Animal material

2.3 Substrate treatments

2.4 Data collection and experimental design

2.5 Studies parameters

2.5.1 Waste characteristics

2.5.2 Physicochemical parameters

2.5.3 Growth performance of larvae

2.5.5 Nutritional composition of larvae and frass

2.5.6 Life cycle and egg laying traits of adult flies

2.5.7 Microbiological load

2.6.3.6 laying rate at peak laying

2.6.3.7 Peak laying production and age

2.6.7 Adults life duration

2.6.8 Daily death rate of adults

2.6 Statistical data analysis

RESULTS

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