Effects of the Incorporation Rate of Black Soldier Fly (Hermetia illucens) Larvae Meals on Zoo-Economic Performance and Carcass Quality of Broiler Chickens

ABSTRACT

The main protein sources used in broiler chicken diets, such as soybean meal and fishmeal, are costly, and one potential alternative is black soldier fly larvae meal (BSFLM).This study aimed to determine the incorporation rate of full-fat BSFLM in broiler chicken diets for optimum zoo-economic performance. The experiment involved 250 day-old unsexed broiler chickens randomly allocated into 25 batches. Five different levels of full-fat BSFLM incorporation (0%, 4%, 8%, 12%, and 16%) were tested during a 49-day experiment. Zootechnical data, economics indexes, and carcass quality were determined. Results indicated a significant decrease in feed intake with the increase of full-fat BSFLM. At the end of the experiment, the broiler chickens fed BSFLM4 demonstrated the highest live weight and the best FCR, with no statistical difference. In terms of economic parameters, the control diet showed the highest feed cost and the lowest economic feed efficiency, without a significant difference. Full-fat BSFLM incorporation did not significantly affect carcass yield. However, chickens receiving BSFLM 16% indicated having a lower zootechnical performance. A full-fat BSFLM incorporation rate of 12% into broiler chicken feed could improve zoo-economic performance in the current study. Moreover, BSFLM could serve as a cost-effective protein source.

Keywords:
Black soldier fly; Broiler chicken; Incorporation rate; Zoo-economic performance

INTRODUCTION

Global meat production tripled between the 1960s and the 2000s (Speedy, 2003). Production is expected to further double by 2050, with a significant increase in livestock production in southern countries (Coulan et al., 2011). The greatest increase has been observed in poultry meat production (Speedy, 2003), accompanied by an increase in the use of feed resources (Makkar et al., 2014). In a Sahelian country such as Niger, animal protein sources have always been imported at high costs (Brah et al., 2017; 2018). However, the trajectory of increasing food demand is facing a decrease in resources available for production, rendering the current linear food system unsustainable and highlighting the need to seek alternative sources. Insects are an important alternative and sustainable resource for animal feed, which is naturally consumed by poultry and has a bromatological composition corresponding to their nutritional needs (Sogari et al., 2019). Of all the feed produced from insects worldwide, 44.8 % is used as poultry feed, comprising grasshoppers, mealworm larvae, silkworm larvae, housefly maggots, and black soldier fly larvae (Makkar et al., 2014; Van Huis, 2022). Among insects, black soldier fly (Hermetia illucens) and house fly (Musca domestica) have been proposed as multifunctional insects. They can convert low-quality organic waste into valuable materials (Dörper et al., 2020), efficiently converting several tons of household waste into utilizable products, such as animal feed, plant fertilizers, and other secondary industrial compounds (Ojiha et al., 2020). Houseflies and black soldier fly larvae may be used as alternative animal protein sources in broiler chicken diets (Dzepe et al., 2021). The advantage of the black soldier fly is that it can be reared over a wide range of organic matter fluxes, and is less likely to transmit pathogens (Van Huis et al., 2020). The various uses of black soldier fly larvae meal (BSFLM) in broiler chicken feed do not reduce the zootechnical performance, cause mortality (Abd El-Hack et al., 2020), or induce metabolic disorders (Moula et al., 2017). Its fat improves the gut health and morphology of broiler chickens (Kim et al., 2021). Whole larvae (Seyedalmoosavi et al., 2022), whole meals (El-Kaiaty et al., 2022) or defatted (Schiavone et al., 2017), and fat (Dabbou et al., 2021) have all been used in chicken diets. These have been incorporated directly (Mat et al., 2022) or as substitutes for fish meal (Onsongo et al., 2018), soybean meal (Murawska et al., 2021), or soybean oil, the latter using larval fat (Kim et al., 2021). Black soldier fly larvae’s crude protein and amino acid profile were comparable to those of several protein-rich feeds, such as fishmeal and soybean meal (Abd El-Hack et al., 2020). BSFLM contains between 40-44 % crude protein based on dry matter 1.7-2.4 % methionine, and 6-8 % lysine based on crude protein (Makkar et al., 2014). Although several studies have focused on the nutritional value of BSFLM, few studies have focused on its economic performance.This study aimed to determine the optimal zoo-economic incorporation of BSFLM in broiler chicken diets.

MATERIALS AND METHODS

Ethical approval

The current study was conducted according to the guidelines of the National Institute for Agronomic Research of Niger.

Biological material

The biological material comprised 250 unsexed day-old Cobb 500 broiler chickens with an initial weight of 71±1.81 g, imported from the Federal Republic of Nigeria. The chickens were reared in two phases. The starter phase was from the 1^st to the 21^st day, and the growth-finishing phase was from the 22^nd to the 49^th day.

Experiment poultry house

The experiment was conducted with natural lighting and ventilation in a 105 m2 (15 m × 7 m) poultry house at the Regional Center for Agronomic Research in Maradi, Niger. The poultry house was subdivided into 25 lots/boxes (12 on one side and 13 on the other). Each lot/box had a dimension of 2.75 m² (2.75 m × 1 m). The poultry house was cleaned, disinfected with a product recommended in Niger, and was under quarantine for two weeks before the start of the experiment. The temperature of the experiment was 25 ± 2°C, and the humidity was 24%.

Sanitary conduct

The chickens were vaccinated against Newcastle disease with LOBIVAC NEW inactivated vaccine from LOBS/France at 8 days of age through subcutaneous injection, followed by a booster intramuscular injection at 22 days of age. They were then treated by orally through drinking water according to the product manufacturer’s instructions. They were also vaccined against coccidiosis with Amprolium 20% (0.5g/l/d) produced by LAPROVET/France, treated for post-vaccination reactions and heat stress with AMIN’TOTAL (0.5 g/l/d) and (1g/l/d), respectively, made by LAPROVET/France, and calcium deficiency was prevented with Calciplus (1ml/l/d), manufactured in India by Vetindia.

Feed formulation

The raw materials used for feed formulation through trial and error method comprised millet, wheat bran, peanut meal, fish meal, full-fat BSFLM (provided by the National Institute for Agronomic Research of Niger), lysine, methionine, bone meal, salt, peanut oil, and the premix. To prepare the feed mixture, all the raw materials were ground separately and weighed according to the formulas shown in Table 1. The samples of fish meal and full-fat black soldier fly larvae meal were subjected to a chemical analysis by the NIRS method to determine their, metabolizable energy concentration, dry matter, crude protein, crude fiber and amino acids content. The full-fat BSFLM was incorporated into the chicken feed at the rates of 0 % (BSFLM0), 4 % (BSFLM4), 8 % (BSFLM8), 12 % (BSFLM12), and 16 % (BSFLM016). BSFLM was considered a new raw material. Once incorporated, the levels of the different raw materials were adjusted to develop an isonitrogenous and isoenergetic feed formula that met the nutritional requirements of broiler chickens, following the National Research Council (NRC, 1994) recommendations. Therefore, during the starter phase of the chicks, regardless of the BSFLM incorporation rate, 22 % of the crude protein recommended for the feed was maintained. The energy varied between 2950 and 3000 kcal/kg of dry feed matter. For the finishing phase, 2950 kcal of energy per kg of dry matter of feed and 20 % crude protein were used in the feed. Broiler chickens received food and water ad libitum.

Table 1
Ingredient and nutrient composition of broiler chicken feeds containing different levels of full-fat black soldier fly larvae meal (BSFLM).

Ingredients (%)	Starter feed						Finisher feed
	BSFLM 0%	BSFLM 4%	BSFLM 8%	BSFLM 12%	BSFLM 16%		BSFLM 0%	BSFLM 4%	BSFLM 8%	BSFLM 12%	BSFLM 16%
Millet Wheat bran Peanut meal	60.5	60.2	60.75	60.5	58.5		64	64	64	64	64
	6.5	6.1	3.45	3	2		5.5	5.22	5	3.92	3.3
	13.35	11.1	13.5	7.15	17.25		15.5	15	14.14	15.63	12.66
Fishmeal Full-fat BSFLM	13	12.3	8	11	0		8	5.75	3.8	0	0
	0	4	8	12	16		0	4	8	12	16
Lysine Methionine Bone meal Salt	0.3	0.3	0.3	0.3	0.3		0.1	0.1	0.1	0.1	0.1
	0.3	0.3	0.3	0.3	0.3		0.1	0.1	0.1	0.1	0.1
	4	3.5	3.3	3.3	3		5	4	3.21	2.54	2.09
	0.3	0.3	0.3	0.3	0.2		0.3	0.3	0.3	0.2	0.2
Peanut oil Premix1	1.5	1.65	1.85	1.9	2.25		1.1	1.13	1.15	1.31	1.35
	0.25	0.25	0.25	0.25	0.2		0.4	0.4	0.2	0.2	0.2
TOTAL	100	100	100	100	100		100	100	100	100	100
Calculated nutritional composition
ME(Kca/KgDM)2	3000.02	3000.21	3000.43	3000.93	2950.23		2959.09	2958.95	2959.04	2958.48	2958.37
Protein (%)	22.05	22.01	22.01	22.03	22.00		20.26	20.26	20.26	20.26	20.26
Crude Fiber (%)	3.06	3.14	3.13	3.10	3.43		3.00	3.15	3.29	3.41	3.46
Crude fat (%)	4.46	4.61	4.72	4.88	4.92		4.47	4.64	4.80	4.94	5.10
Lysine (%)	1.38	1.48	1.49	1.7	1.51		1.04	1.10	1.17	1.19	1.32
Methionine (%)	1.18	1.45	1.69	2.00	2.15		1.04	1.21	1.47	1.71	1.99
Calcium (Ca) (%)	1.83	1.79	1.68	1.94	1.52		1.91	1.65	1.47	1.24	1.24
NPP (%)3	0.97	0.98	0.95	1.10	0.92		0.97	0.89	0.84	0.77	0.80
Ca/NPP	1.88	1.21	1.76	1.76	1.65		1.96	1.85	1.75	1.61	1.55

• (¹) Premix content per kg : 220 mg of Mg, 220 mg of Zn, 110 mg of Fe,248 mg of Cu, 33 mg of I, 77,105 IU of Vit A, 27,538 IU of Vit D, 165 IU of Vit E, 0,11 mg of Vit. B12, 8 mg of menadion, 66 mg of riboflavin, 11 mg of thiamine, 66 mg of pantothenic acid, 275 mg of niacin, 14 mg of Vit B6, 7 mg of folic acid, 3,855 mg of choline and 0.33 mg of biotin,
• (²) Metabolizable Energy in kilocalories per kilogram of dry matter; (³) Non-phytic phosphorus

Experimental design

The 250 unsexed Cobb 500 broiler chicks were raised on peanut hull litter for 7 weeks, including 3 weeks (1 to 21 days of life) of starter period and 4 weeks (22 to 49 days of life) of finishing period. The chickens were then randomly distributed among 25 batches, each with 10 chicks at the beginning of the experiment (five replications). Five feeds were randomly distributed into 25 batches, with five repetitions per feed. The parameters monitored were as follows: zootechnical performance including mortality, feed intake, growth, and feed conversion ratio (FCR), economic indexes including feed cost and economic feed efficiency (EFE), and quality performance including carcass and organ yields.

Data collection

The mortality was recorded daily during the rearing period. The mortality rate was defined as the ratio of the number of dead chickens recorded during the rearing period to the total number at the beginning of the rearing period, and it was expressed as a percentage.

During the experiment, water and feed were distributed ad libitum. The feed was weighed daily and distributed to the chickens in the morning. The refusal was collected the day before the new distribution. The ingested feed quantities were evaluated as the difference between the quantities distributed and refused. In each batch, the average feed intake per chicken was obtained by dividing the total quantity consumed by the number of chickens. It was expressed in grams per day.

The initial weights of the chicks were determined at the beginning of the experiment. Then, three subjects per batch were weighed weekly to establish a growth trend curve. Finally, all the chickens in each batch were weighed individually at the end of the starter phase (21 d) and the end of the experiment (49 d). The average live weight was determined in grams (g) at the start of the experiment, at 21 days, and at 49 days by calculating the ratio of the total weight of the subjects of the same batch in g to the total birds of the batch.

Using the live weight measurements per period, the average daily gain (ADG) of the chickens was calculated between the two weighing periods as the ratio of the average weight gain of the chicken over days, which expresses the growth rate of chickens in grams per day.

The FCR was calculated as the ratio of the average quantity of feed consumed by chickens over a given period to the average weight gain of the chickens corresponding to this period (Brah et al., 2018).

The market prices of the raw materials used for feed formulation and the selling price per kilogram of live chicken weight were used to calculate the economic parameters, as per Houndonougbo et al. (2009). Feed cost expresses the amount (in FCFA) of feed used to produce 1 kg of a live chicken, and EFE is the ratio between the cost of production per kilogram of live weight of chickens over a period and the cost per kilogram of feed used for production over the same period. The cost of production per kg of live weight of chicken was calculated by taking the product of weight gain and the selling price per kg of live weight. EFE expresses the gross profitability of feed use.

BSFLM is, however, not marketed in Niger. It is produced by the National Institute for Agronomic Research of Niger. Therefore, the price per kilogram of dried larvae meal was estimated at 1500 FCFA (2.73 USD), which was used to evaluate the investment in kilograms of larva meal. In the same period, the kg of fish meal used was priced at 3350 FCFA or 6.09 USD.

Carcass quality

The carcass characteristics were studied by slaughtering 10 chickens per feed to determine the carcass weight, carcass yield, viscera, feathers, head and feet, empty gizzard, and liver. Carcass and organ yields were expressed as a percentage of live weight at slaughter.

Statistical analysis

The data was entered on an “EXCEL® 2013” spreadsheet. The calculation of means, standard deviations, one-factor variance analysis (feed), and comparison of means (ANOVA) was performed using the R 4.2.1 software (USA). The differences between the arithmetic means were compared using the Student-Newman-Keuls (SNK) test to detect the effects of treatments at 5%, probability levels.

RESULTS AND DISCUSSION

Zootechnical Performances

Chemical composition

Fish meal had a higher concentration of metabolizable energy and crude protein content compared to the full-fat larvae meal. As for crude fiber, it is more concentrated in the full-fat larvae meal than in fish meal. The lysine and methionine contents of the fish meal were similar to those found in the full-fat larvae meal (Table 2). The chemical composition of BSFLM varies depending on the author. That could be due to the differences in breeding substrates (Makkar et al., 2014), but the drying methods of non-defatted BSFLM have also been shown to significantly influence moisture, ash, crude protein, crude fiber, ether extract, nitrogen-free extract, phosphorus, and gross energy content (Pornsuwan et al., 2023). The chemical composition of the full-fat black soldier fly larvae obtained in this analysis confirms the observations of certain authors, who argue that protein content as well as amino acid profile in BSF larvae is comparable to those in many protein-rich feedstuffs such as fish meal and soybean meal (Abd El-Hack et al., 2020).

Table 2
Chemical composition of the fish meal and full-fat BSFLM used.

Parameters	ME (Kcal/KgDM)	DM (%)	CP (%)	CF (%)	Lys (%)	Meth (%)
Fish Meal	1912	94.76	55.89	10.62	2.60	1.06
Full-fat BSFLM	1673	96.20	42.28	17.07	2.28	1.02

• ME: Metabolizable Energy in kilocalories per kilogram of dry matter, DM: Dry Matter, CP: Crude Protein, CF: Crude Fiber, Lys: Lysine and Meth: Methionine.

Mortality

A total of two mortalities were recorded in the control group during the 49 days of the experiment. The first mortality was recorded on day 1 of the experiment, and the second on day 21. However, no mortality was observed in the BSFLM-based treatments. The finding corroborates the results reported by Mat et al. (2022), who did not observe any mortality or visible physiological disorders while incorporating 12 % BSFLM in broiler chicken feed. The same trends were observed by De Souza Vilela et al. (2021), with an incorporation rate of 20 % BSFLM into broiler chicken diets. Kim et al. (2021) determined that replacing soybean oil with BSFLM improved the gut health and morphology of broiler chickens.

Feed intake

During the starter phase, the incorporation of BSFLM did not significantly influence broiler chicken feed intake (p>0.05, Table 3). However, broiler chickens in the control group (BSFLM0) demonstrated the highest feed intake during finishing. The difference in feed intake in the finishing phase between broiler chickens fed with the BSFLM0 diet and the other groups (BSFLM4, BSFLM8, BSFLM12, and BSFLM16) were 2.07, 7.66, 9.96, and 17.47 g/d, respectively. The difference for overall groups was statistically significant at the 5 % level (p<0.05). Considering the entire experimental period (49 d), the average broiler chicken feed intake of the control batch was higher than that of the BSFLM16 batch (Table 3). Additionally, there was a statistically significant difference in feed intake throughout the experiment (p<0.05). However, the daily quantities of feed ingested by chickens in the control and BSFLM4 batches were statistically similar (p>0.05). The same applies to the quantities ingested by broiler chickens in the BSFLM8 and BSFLM12 batches. The amount of feed ingested by the broiler chickens decreased linearly with an increase in the BSFLM incorporation rate in the feed. Murawaska et al. (2021) observed a similar trend. However, Mat et al. (2022) reported no significant differences in the feed ingestion of up to 12 % defatted BSFLM. Although the feed concentrations of metabolizable energy and crude protein were similar, the fat content increased with the increasing incorporation of BSFLM. The fat content increased the amount of saturated fatty acids in the diet and reduced feed intake (Lu et al., 2022). The amount of feed ingested by the broiler chickens was lower than that observed by Murawska et al. (2021) when replacing soybean meal with BSFLM in ROSS 308 broiler chickens. They were, however, similar to the amount of defatted BSFLM reported by Mat et al. (2022) in COBB 500 broiler chickens. This observation may be related to the chicken strains used in this study. Olusegun et al. (2020) observed significant differences in feed intake when comparing the performance of three broiler chicken strains.

Table 3
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken feed intake (g/d) during 49 days of experiment.

Phase	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Starter	26.734	26.232	26.360	26.368	26.276	0.37	0.713
finisher	106.12a	104.05a	98.46b	96.16b	88.65c	6.21	<0.001
All phase	72.09a	70.70a	67.56b	66.25b	61.92c	2.45	<0.001

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) was incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b,c Vaues with the same letters on the same row are not statistically different (p>0.05).

Live weight

The live weights of broiler chickens were similar in all batches at the binding stage (p>0.05, Table 4).

Table 4
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken live weight (g) during 49 days of experiment.

Live weight	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Initial live weight	69.92	70.18	73.54	71.66	73.80	7.70	0.113
21 days live weight	421.43a	424.30a	412.88ab	445.80a	386.58b	21.43	0.003
49 days live weight	1917.19a	1959.76a	1667.66ab	1678.10ab	1473.64b	199.8	0.009

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b Values with the same letters on the same row are not statistically different (p>0.05).

At 21 d, the broiler chickens fed the BSFLM12 diet showed the highest live weight. However, these differences were not statistically significant when compared to those observed in the chickens that were fed BSFLM0 and BSFLM4 (Table 4).The chickens that were fed BSFLM16 demonstrated the lowest body weight at this phase, but that was not statistically different from those that were fed BSFLM8. At the end of the experiment (d 49), broiler chickens fed BSFLM4 weighed more, exceeded those that were fed BSFLM0, BSFLM8, BSFLM12, and BSFLM16 by 42.57, 292.10, 281.66, and 486.12 g, respectively. The difference in weight was statistically significant at a 5 % level (p<0.05) for overall. However, the live weights of broiler chickens that were fed the BSFLM0, BSFLM4, BSFLM8, and BSFLM12 diets were not significantly different at the 5 % significance level. These feeds contained similar levels of metabolizable energy (ME) and crude protein (CP) during both phases.The ME and CPs drop when incorporating 16 % BSFLM led to decreased live weight in the starter phase.The level and source of ME (Ghaffari et al., 2007; Akbari et al., 2017) and CP content (Folorunso et al., 2014) in feeds potentially affect broiler chicken performance. Broiler chickens that were fed BSFLM4 demonstrated a higher live weight than the control (BSFLM0) due to the amino acid content, particularly methionine, which increased with BSFLM in the feed. Ahmed and Abass (2011) reported that increasing the level of methionine in feed increases the live weight of chickens. Broiler chickens from the BSFLM8 and BSFLM12 batches had lower live weights than those from the BSFLM4 because of the fat content, which reduces feed intake (Lu et al., 2022). Broiler chicken weights at 49 days were lower than the live weights, as reported by Oddon et al. (2021) and Murawska et al., (2021) at 38 and 42 days, respectively, using only male ROSS 308 broiler chickens. However, Brah et al. (2018) observed the same live weights of broiler chicken after 49 days in Niger Republic with unsexed COBB 500 chicken by gradually replacing fish meal with grasshopper meal. The strain, sex, and environment affected the final live weight of the broiler chickens. Olusegun et al. (2020) reported that Ross chickens and males demonstrated a higher final live weight than chickens of other strains. The environment, particularly temperature, affects the live weight of broiler chickens (Baracho et al., 2019). Heat stress reduces the genetic potential of chickens in tropical climates (Kpomasse et al., 2021).

Average daily gain

During the broiler chicken starter phase, the BSFLM12 diet induced higher ADG, whereas the BSFLM16 diet resulted in low ADG (Table 5). The ADGs in this phase were observed to be different (p<0.05). The BSFLM4 diet induced higher ADG in the broiler chicken finisher phase. However, this rate was not statistically different from that induced by the BSFLM0 diet. BSFLM8 and BSFLM12 induced similar ADGs (Table 5). The broiler chickens that were fed BSFLM16 had a low ADG during this phase.

Table 5
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken average daily gain (g/d) during 49 days of experiment.

Phase	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Starter	16.74a	16.86a	16.16ab	17.82a	14.89b	0.94	0.002
finisher	53.42a	54.84a	44.81ab	44.01ab	38.82b	6.76	0.022
All phase	37.69a	38.56a	32.53ab	32.78ab	28.57b	4.11	0.009

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b Values with the same letters on the same row are not statistically different (p>0.05).

Over the entire duration of the experiment, the broiler chickens that were fed BSFLM4 demonstrated a higher ADG than those fed BSFLM0, BSFLM8, BSFLM12, and BSFLM16 by 0.87, 6.03, 5.78, and 9.99 g/d, respectively. The difference in ADG between broiler chickens fed with BSFLM0 and BSFLM4 was not statistically significant (Table 5). The broiler chickens fed with BSFLM16 demonstrated low ADG. Mat et al. (2012) reported that the incorporation of BSFLM at 4 % showed a higher ADG than the control and decreased performance after incorporation at 8 %. Kareem et al. (2018) also observed that the crude protein digestibility of 4 % was higher than that of the control. The broiler chickens fed with BSFLM16 had inferior ADG because of their high fat and crude fiber content, particularly chitin, which reduced feed intake and protein digestibility. Although chitin has positive effects on immune defenses and an antimicrobial role, the presence of chitin in feed reduces protein digestibility (Abd El-Hack et al., 2020, Duper et al., 2021). Mohammad et al. (2017) reported similar ADGs when studying the effect of BSFLM on the growth performance of broiler chickens from 21-49 days.

Feed conversion ratio

The amount of feed required to produce one kg of live-weight broiler chickens was statistically different (p<0.05) in the starter phase. Broiler chickens in the BSFLM16 group required more feed for weight gain (Table 6). In the finishing phase, although broiler chickens fed the BSFLM16 diet required more feed, their FCR was not significantly different (p>0.05) from the FRCs of the other broiler chickens (Table 6). Mat et al. (2021) and Murawska et al. (2021) reported no significant differences between FCRs after 42 d of study using non-defatted BSFLM. However, Dabbou et al. (2018) observed an increase in FCR with an increase in the rate of BSFLM defatting. Schiavone et al. (2017) reported that BSFLM defatting reduced the concentration of metabolizable energy and increased feed intake. The FCR was within the range observed by Moula et al. (2017) when 2 % BSFLM was incorporated into broiler chicken diets. However, they were higher than the FCR reported by Oddon et al. (2021) in male chickens only; which may be sex-related. Benyi et al. (2015) reported that females had a higher FCR than males in COBB 500 chickens.

Table 6
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken feed conversion ration during 49 days of experiments.

Phase	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Starter	1.61b	1.56b	1.63b	1.48b	1.77a	0.01	0.003
finisher	1.992	2.000	2.208	2.196	2.288	0.06	0.210
All phase	1.912	1.896	2.082	2.026	2.172	0.03	0.102

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b Values with the same letters on the same row are not statistically different (p>0.05).

Economic performance

Feed cost

In the broiler chicken starter phase, the feed cost (FC) was, on average, 1181.04 FCFA. The FC of broiler chickens fed with BSFLM0 in this phase was higher (Table 7), with a statistically significant difference (p<0.05). During the finishing period, the FC was higher in broiler chickens fed with BSFLM16 (Table 7). However, this FC was not significantly different (p>0.05) from the other FCs. On average, the FC was 1140.14 FCFA to produce one kg of live weight throughout the experiment. The FC decreased significantly (p<0.05) with increasing BSFLM incorporation into broiler chicken feeds. The control feed (FLMSN0) FC exceeded that of the BSFLM4, BSFLM8, BSFLM12, and BSFLM16 feeds by 23.10; 118.67; 48.94, and 75.25 FCFA, respectively. Onsongo et al. (2018) reported that substituting soybean meal and fishmeal with BSFLM reduced feed prices; however, it did not significantly reduce feed costs. However, Affedzi-Obresi et al. (2020) reported that FC differences were not statistically significant when substituting soybean meal with BSFLM; however, substituting fishmeal with BSFLM significantly improved the FC.The use of BSFLM as a substitute for fish meal allows for a considerable reduction in feed prices, and makes it possible to gain more weight at certain substitution rates. Brah et al. (2018) reported lower feed costs than those observed in this study when FM was substituted with locust meals in Niger Republic, which has been linked to the soaring prices of raw materials used in feed formulation.

Table 7
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken feed cost (FCFA/Kg of live weight) during 49 days of experiment.

Phase	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Starter	1198.79a	1194.06a	1142.80a	1200.20a	1018.47b	77.77	0.003
finisher	1187.88	1146.41	1006.50	1088.57	1217.69	84.04	0.118
All phase	1193.33a	1170.23a	1074.66b	1144.39ab	1118.08ab	46.17	0.013

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b Values with the same letters on the same row are not statistically different (p>0.05).

Economic feed efficiency

The EFE was statistically different (p<0.05) for all broiler chickens in the starter phase. The BSFLM16 diet was observed to be the most profitable during this phase. The BSFLM16 diet was observed to be less profitable, and the BSFLM8 diet, the most profitable in the finishing phase (Table 8). However, there was no significant difference at the 5 % level between all the EFEs in finishing. All feeds were profitable throughout the experimental period. There was no significant difference at the 5 % level. Onsongo et al. (2018) also reported that all feeds formulated with BSFLM were profitable. However, there was no difference in the gross financial margin when substituting BSFLM for soybean meal and fishmeal. Affedzi-Obresi et al. (2020) reported that the substitution of fishmeal by BSFLM resulted in a higher gross margin than the substitution of soybean meal by BSFLM. The low profitability of BSFLM has been linked to larval production costs. Until now, black soldier fly larvae have been produced experimentally and for scientific research (Abd El-Hack et al., 2020). The EFC reported by Brah et al. (2018) was higher than that observed in this study due to increased broiler chicken production costs.

Table 8
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken economic feed efficiency during 49 days of experiment.

Phase	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Starter	1.472b	1.474b	1.532b	1.460b	1.718a	0.01	<0.001
finisher	1.474	1.610	1.748	1.616	1.438	0.05	0.238
All phase	1.474	1.538	1.640	1.538	1.578	0.01	0.119

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b Values with the same letters on the same row are not statistically different (p>0.05).

Carcass and organ quality

Carcass yield

The live weight sampled for carcass characteristics was higher in the BSFLM0 group and lower in the BSFLM16 group at the end of experiment. The difference was significant (p<0.05) between live weights at slaughter (Table 9). After slaughter, plucking, heading, and evisceration, the carcass weight of broiler chickens fed with BSFLM0 was higher than those fed with BSFLM4, BSFLM8, BSFLM12, and the difference was statistically significant at the 5 % level. The average carcass yield was on 70.78 %. The carcass yields of BSFLM0 broiler chickens were 0.608 %, 4.154 %, 0.702 %, and 2.936 % higher than those of broiler chickens fed BSFLM4, BSFLM8, BSFLM12, and BSFLM16, respectively. Howeve there was no statistical difference at the 5 % level. Nayohan et al. (2022) concluded that incorporating BSFLM did not affect carcass yield. Kareem et al. (2018) observed that no difference in carcass yield was associated with abdominal fat deposition in chickens, which was within the ranges observed by Murawska et al. (2021); however, it was lower than those reported by Oddon et al. (2012) for ROSS 308 broiler chicken males.

Table 9
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken carcass characteristics.

Parameters	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Live weight (g)	1957.3a	1674.9b	1684.2b	1733.3b	1437.0c	185.29	<0.001
Carcass weight (g)	1416.1a	1202.8b	1145.7bc	1243.2b	1007.0c	148.94	<0.001
Carcass yield (%)	72.354	71.746	68.200	71.652	69.936	7.06	0.127

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b,c Values with the same letters on the same row are not statistically different (p>0.05).

Organ yield

The feather yield of the BSFLM16 broiler chickens was significantly higher (Table 10). Broiler chickens from the BSFLM4, BSFLM8, and BSFLM batches had similar feather yields that were not statistically different. The BSFLM0 broiler chickens had the lowest feather yield. Broiler chickens fed the BSFLM16 diet developed more viscera and outperformed the BSFLM0, BSFLM4, BSFLM8, and BSFLM12 diets by 1.60 %, 1.72 %, 1.22 %, and 1.11 %, respectively, with no significant differences (p>0.05). The empty gizzard yield was not significantly affected (p>0.05) by the incorporation of BSFLM (Table 10). Feed metabolism had a statistical effect on broiler chicken liver yield (p<0.05). The broiler chickens fed the BSFLM8 diet demonstrated a higher liver yield, which was not statistically different from those fed with the BSFLM0, BSFLM4, and BSFLM16 diets. Broiler chicken chickens fed BSFLM12 had the lowest liver yield (Table 10). Onsongo et al., (2018) reported that BSFLM did not affect the broiler chicken giblet yield. Also, Kareem et al., (2018) reported that BSFLM incorporation did not significantly influence the gizzard and liver yields. Feeding broiler chickens with a diet containing BSFLM did not affect the health or blood parameters of broiler chickens (Dabbou et al., 2018). The significant liver difference observed in this study could be related to the effort required for the transformation of larval fat, considering that Dabbou et al. (2018) found no differences between livers using defatted meals. The gizzard yield was similar to that reported by Oddon et al. (2021), and higher than that observed by Murawska et al. (2021).

Table 10
Effects of different incorporation rates of full-fat black soldier fly larvae meal on broiler chicken organ characteristics.

Parameters	BSFLM0	BSFLM4	BSFLM8	BSFLM12	BSFLM16	SEM	p-value
Feather yield (%)	4.42	5.26	5.03	5.21	5.72	0.46	0.084
Viscera yield (%)	13.55	13.43	13.93	14.04	15.16	3.13	0.570
Empty gizzard yield (%)	1.45	1.65	1.64	1.59	1.74	0.03	0.137
Liver yield (%)	2.02ab	2.09ab	2.30a	1.92b	2.01ab	0.03	0.042
Feather yield (%)	4.42	5.26	5.03	5.21	5.72	0.46	0.084

• BSFLM0, BSFLM4, BSFLM8, BSFLM12, and BSFLM16: Feeds where full-fat black soldier fly larvae meal (BSFLM) were incorporated at 0%, 4%, 8%, 12%, and 16 %, respectively. ^a,b Values with the same letters on the same row are not statistically different (p>0.05).

CONCLUSIONS

The incorporation of ful-fat BSFLM did not cause broiler chicken mortality throughout the experiment. The zootechnical performance in terms of live weight and ADG was not significantly influenced until a 12 % of incorporation of full-fat BSFLM into broiler chicken diet. The incorporation rate did not influence the FCR, carcass yield, or certain organs. The control feed (BSFLM0) exhibited poor economic performance compared to other diets in terms of feed cost and efficiency. The BSFLM16 diet exhibited the lowest zootechnical performance. The optimum incorporation rate of full-fat BSFLM into the COBB 500 broiler chicken feed was 12 %. By incorporating full-fat BSFLM in broiler chicken diets, feed costs can be reduced. Additional studies on full-fat BSFLM digestibility and its incorporation into laying hen feeds will be necessary to further popularize larva use.

ACKNOWLEDGMENTS

The authors are grateful to all the contributors of this study, particularly the Norwegian Agency for Development Cooperation (NORAD), the National Institute for Agriculture Research of Niger (INRAN), the International Institute for Tropical Agriculture (IITA), and Dan Dicko Dankoulodo University of Maradi (UDDM), Niger

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• Funding

  This work was supported by the BBEST Project: Chicken and Fish Feed and Organic Fertilizer Value Chain Development Using BSF-Based Urban Biowaste Processing in DRC, Ghana, Mali, and Niger. Led by the International Institute of Tropical Agriculture (IITA), the prime sponsor is the Norwegian Agency for Development Cooperation (NORAD) [Grant QZA-21/0195].

• Data availability statement

  The original contributions presented in this study are included in the article/supplementary material. For inquiries, please contact the corresponding author/s.

• Disclaimer/Publisher’s Note

  The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.

Edited by

Section editor:

Rodrigo Garófallo Garcia

Data availability

The original contributions presented in this study are included in the article/supplementary material. For inquiries, please contact the corresponding author/s.

Publication Dates

• Publication in this collection
  01 Nov 2024
• Date of issue
  2024

History

• Received
  11 Apr 2024
• Accepted
  02 Aug 2024