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Review

Nutritional Composition of Black Soldier Fly Larvae (Hermetia illucens L.) and Its Potential Uses as Alternative Protein Sources in Animal Diets: A Review

by
Shengyong Lu
1,
Nittaya Taethaisong
1,
Weerada Meethip
1,
Jariya Surakhunthod
1,
Boontum Sinpru
1,
Thakun Sroichak
1,
Pawinee Archa
1,
Sorasak Thongpea
1,
Siwaporn Paengkoum
2,
Rayudika Aprilia Patindra Purba
1 and
Pramote Paengkoum
1,*
1
School of Animal Technology and Innovation, Institute of Agricultural Technology, Suranaree University of Technology, Muang, Nakhon Ratchasima 30000, Thailand
2
Program in Agriculture, Faculty of Science and Technology, Nakhon Ratchasima Rajabhat University, Muang, Nakhon Ratchasima 30000, Thailand
*
Author to whom correspondence should be addressed.
Insects 2022, 13(9), 831; https://doi.org/10.3390/insects13090831
Submission received: 5 August 2022 / Revised: 6 September 2022 / Accepted: 7 September 2022 / Published: 13 September 2022
Review Reports Versions Notes

Abstract

:

Simple Summary

With the increasing global population, the shortage of protein feed resources is becoming more and more serious, and human beings urgently need to find new protein sources to replace traditional soybean meal and fish meal. Black soldier fly larvae are rich in fatty acids, proteins and minerals. Numerous studies have shown that adding black soldier fly larvae powder to monogastric animals has no negative effects on animal growth performance, meat quality and immunity. However, black soldier flies are still subject to legal constraints and consumer acceptance when they are used as feed.

Abstract

The rapidly growing population has increased demand for protein quantities and, following a shortage of plant-based feed protein sources and the prohibition of animal-based feed protein, has forced the search for new sources of protein. Therefore, humans have turned their attention to edible insects. Black soldier fly larvae (BSFL) (Hermetia illucens L.) are rich in nutrients such as fat, protein and high-quality amino acids and minerals, making them a good source of protein. Furthermore, BSFL are easily reared and propagated on any nutrient substrate such as plant residues, animal manure and waste, food scraps, agricultural byproducts, or straw. Although BSFL cannot completely replace soybean meal in poultry diets, supplementation of less than 20% has no negative impact on chicken growth performance, biochemical indicators and meat quality. In pig studies, although BSFL supplementation did not have any negative effect on growth performance and meat quality, the feed conversion ratio (FCR) was reduced. There is obviously less research on the feeding of BSFL in pigs than in poultry, particularly in relation to weaning piglets and fattening pigs; further research is needed on the supplementation level of sows. Moreover, it has not been found that BSFL are used in ruminants, and the next phase of research could therefore study them. The use of BSFL in animal feed presents some challenges in terms of cost, availability and legal and consumer acceptance. However, this should be considered in the context of the current shortage of protein feed and the nutritional value of BSFL, which has important research significance in animal production.

1. Introduction

The International Feed Industry Federation (IFIF) reports that the world population will exceed 10 billion by 2050 [1]. By then, the increased population will consume twice as much animal protein as it does today; between 2010 and 2050, consumption of pork and poultry is expected to grow by 105% and 173%, respectively [2,3], which will create enormous challenges in the production of protein feed ingredients, estimated as being more than 1.3 billion tons of dry matter [4]. Soy grains and some oilseed cakes (e.g., soybean meal, rapeseed meal, and cottonseed meal), and some algal biomass are currently the main sources of protein for ruminants and monogastric animals [5]. Global livestock feed production was estimated to be 1.104 billion tons in 2018 alone, with a total value of more than USD 400 billion [6]. Protein is the most costly and restrictive ingredient in feed formulations, and the price of traditional sources of protein has risen significantly due to yield factors and competition between humans and animals [6,7,8]. In order to meet the demand for highly nutritious animal food, the future will drive animal production systems to find new sources of high-quality and sustainable protein feed raw materials. Economic and environmental concerns must be considered in this context, while competition with plant-based human and animal food chains is reduced [9,10,11,12]. Therefore, urea can be added as a protein source in ruminant diets to improve their growth performance and milk production performance [13,14,15,16]. However, in monogastric species, ammonia concentrations in the gastrointestinal tract and the environment can cause damage to the gastrointestinal mucosa, resulting in impaired nutrient absorption, energy inefficiency, and reduced growth performance [17]. Thence, people have turned their attention to insects with high protein content.
As protein raw materials, insects such as BSFL, mealworm larvae (Tenebrio molitor L.), and crickets (Orthoptera: Gryllidae) are the focus of emerging research fronts and are already used as alternative nutrient sources for poultry and swine feed because they contain nearly 100 percent of the edible portion of protein. [18,19,20]. The feed conversion rate of BSFL is better than that of mealworms and crickets, and its survival rate and nitrogen and phosphorus composition do not change greatly with a change in diet [21]. BSFL are characterized by a high food conversion rate, short reproductive cycle, and high content of fat, protein, minerals, and vitamins [22,23]. They are also highly sustainable as they can be raised on a large scale in organic streams, and at a much lower environmental cost than traditional protein sources [24,25]. Multiple studies have shown that BSFL can be used as a food or feed source, ultimately helping to solve the global food problem. However, consumers prefer to use BSFL in animal feed rather than directly for human consumption, because people have a certain degree of psychological aversion to eating insects [26,27,28]. Diets supplemented with BSFL appear to improve growth performance and digestibility in pigs and poultry compared to other protein feeds [29,30]. Schiavone et al. [31] used whole-fat BSFL to replace 50% or 100% soybean oil, and the results showed that the growth performance, blood biochemical immune parameters, and intestinal health of broilers were not impaired. BSFL can also reduce the quality and nutrient content of pig manure with an efficiency similar to that of poultry manure, which is beneficial for improving farm hygiene [32,33], reducing pest numbers, and reducing nutrient pollution in runoff [34]. Therefore, BSFL can replace traditional protein feed ingredients such as soybean meal and fish meal. This study reviews the nutritional value of BSFL, their effects on animal performance, digestion, and immunity, and the challenges they may face when fed to animals.

2. BSFL (Hermetia illucens L.)

BSFL (Hermetia illucens L.; Diptera: Stratiomyidae) are a saprophytic insect that primarily feeds on organic wastes such as plant residues, animal manure, and waste, food waste, agricultural byproducts, or straw [32,35,36,37]. BSFL are an excellent candidate for human and animal protein sources, and the utilization of organic waste can help to reduce pollution [38,39,40,41]. In the process of degrading waste, BSFL converts organic waste into amino acids, peptides, proteins, oils, chitin, and vitamins, thereby controlling certain harmful bacteria (such as Salmonella and Escherichia coli) and pests, and are also used in medicine and chemical and various animal feeds (mainly pets, pigs and poultry) [38,42].
BSFL originated in the South American savannah and are widely distributed in temperate, subtropical, and tropical regions, with an optimum temperature range of 25°C to 30 °C [43,44]. Due to their lack of resistance to cold, they cannot survive in northwestern Europe and regions with temperatures below 5 °C [45]. BSFL are one of five genera in the subfamily Hermetiinae of the order Diptera [46]. The other four genera are Patagiomyia, Chaetosargus, Notohermetia, and Chaetohermetia; Hermetia illucens is the most widespread of all species [47]. It is a large, slender black species with three segments—head, thorax, and belly—with brownish wings and tentacles projecting from the head [48]. There are five segments on the abdomen with white spots. Males are longer than females but have smaller end genitals and wings. Females have body lengths between 12 and 20 mm and wings between 8 and 14.8 mm [48]. Their life cycle has five stages: egg, larva, pupa, pre- and adult. The larval and pupal stages are the most nutrient-rich and largely depend on the quality of food, with about 18–33% fat and 32–53% protein [49,50,51]. BSFL have a lifespan of approximately 20–22 days, with a pupa for the first 6–8 days and an adult metamorphosis for the last 14 days [47,52,53]. Adult worms have no mouth, digestive system, or stinger, pose no threat to other organisms [54] and have no affinity for the human body and fresh food. Therefore, they also do not serve as vectors for disease transmission [55].
Bioconversion rate is one of the important indicators of waste efficiency used to treat BSFL [56,57], and the biotransformation rate depends on many factors, such as the concentration of digestible nutrients, protein, fat, fiber, pH, feeding rate [37], density and water content of substrates, etc. [37,58]. The ideal moisture content is between 60% and 80%, with a lower limit of about 40% [59]. The management requirements of livestock manure around the world are getting higher and higher [60,61,62]. Supplementing BSFL in livestock feed can reduce the excretion of manure by 60% [63]. Moreover, the larvae can also decompose more than 50% of chicken manure, and convert it into high-quality amino acids, protein, and fat for animal feed, reducing the cost of breeding [64]. At the same time, BSFL nutrients are also rich in minerals and chitin and have antioxidant and immune-boosting properties (discussed in the results below).

3. Nutritional Value of BSFL (Hermetia illucens L.)

3.1. Regular Nutrition Facts

In animal feed, there are currently two types of BSFL: defatted and full fat, with the primary difference being in fat and saturated fatty acid content. Table 1 shows its nutritional value. The average crude protein content of BSFL was 414.7 g/kg, ranging from 216 g/kg [65] to 655 g/kg [66], which was lower than a conventional soybean meal (CSBM) (494.4 g/kg) and fish meal (675.3 g/kg) [67]. The protein content of full-fat BSFL is relatively similar, but the protein content after defatting is very different (from 216 g/kg to 655 g/kg), which may be related to the method of defatting, such as the irreversible damage to the protein caused by high temperatures. In full-fat BSFL, the fat content ranged from 294 g/kg [68] to 515.3 g/kg [69], with an average of 353.2 g/kg; these were both higher than CSBM (14 g/kg) and fish meal (103.6 g/kg) [67]. The average fat level after defatting (69.2 g/kg) was also higher than CSBM. BSFL contained ash at an average of 82.4 g/kg, ranging from 27 g/kg [45] to 132 g/kg [68], higher than CSBM (71.9 g/kg) and lower than fish meal (171.5 g/kg) [67]. The average level of crude fiber was 95.4 g/kg, ranging from 41 g/kg [45] to 213 g/kg [68], which was lower than CSBM (74.3 g/kg), but higher than fish meal (2.6 g/kg) [67]. The average content of chitin was 61.7 g/kg, ranging from 38.7 to 72.1 g/kg. The active ingredient of chitin is chitosan, which is another important polysaccharide in addition to cellulose. Chitin (linear polymer of -(1-4)N-acetyl-d-glucosamine units) and cellulose (linear polymer of -(1-4)d-glucopyranose units) have similar molecular structures [70]. Chitin is considered an indigestible fiber, but it can improve the immune function of animals [71,72]. The variation of crude fiber content in BSFL may be related to developmental stages, and the closer to metamorphic adults, the higher the fiber content [73]. Therefore, different research results produced different levels of chitin content.

3.2. Amino Acid Profile

Both defatted and full-fat BSFL have a rich amino acid profile and are thus considered a more sustainable protein source than CSBM or fish meal [77]. The amino acid profile of BSFL is shown in Table 2. The most abundant essential amino acids were leucine (average 44.6 g/kg, from 27.8 g/kg to 78.3 g/kg), lysine (average 38.8 g/kg, from 23.0 g/kg to 68.2 g/kg) and valine (average 40.1 g/kg, ranging from 28.2 g/kg to 67.9 g/kg). These three amino acid contents are higher than those of soybean meal, and even the valine content is higher than that of fish meal [67]. The least abundant essential amino acids are methionine and tryptophan, which are comparable to soybean meal and are much lower than fish meal [67]. The content of histidine ranged from 9.8 g/kg to 48 g/kg, and the content of isoleucine ranged from 17.7 g/kg to 48 g/kg, which was slightly higher than soybean meal and fish meal [67]. The content of phenylalanine ranged from 16.4 g/kg to 77.6 g/kg, and the content of threonine ranged from 16.2 g/kg to 45 g/kg, which are basically the same as soybean meal and fish meal. Arginine and histidine are lower than soybean meal and fish meal [67].

3.3. Fatty Acid Profile

The fatty acid content of BSFL is shown in Table 3. The most abundant saturated fatty acids (SFA) are lauric acid (C12:0), which ranges from 75 to 575. An amount of 6 g/kg, myristic acid (C14:0), which ranges from 23 to 98.7 g/kg, palmitic acid (C16:0), which ranges from 10.3 to 192.0 g/kg, and stearic acid (C18:0), which ranges from 9.8 to 69.0 g/kg. The highest content of monounsaturated fatty acids is oleic acid (c9C18:1), which ranges from 79.7 to 266.0 g/kg, palmitoleic acid (C16:1), which ranges from 10.3 to 192.0 g/kg, linoleic acid (C18:2n6), which ranges from 38.0 to 314.0 g/kg, and linolenic acid (C18:3n3), which ranges from 9.8 to 36.0 g/kg. SFA content ranges from 362.0 to 782.9 g/kg, MUFA ranges from 85.5 to 287.0 g/kg, n-6 PUFA ranges from 80.0 to 314.0 g/kg and n-3 PUFA ranges from 9.8 to 36.0 g/kg. The MUFA/SFA ratio ranges from 15.3% to 79.3% and the n-3 PUFA/n-6 PUFA ratio ranges from 8.5% to 17.9%.

3.4. Minerals Composition

Table 4 shows the mineral content of BSFL. BSFL are rich in minerals; calcium (Ca) is the most abundant and ranges from 1.2 g/kg to 35.7 g/kg. Copper (Cu) ranges from 0.1 g/kg to 15.0 g/kg. Iron (Fe) ranges from 0.1 g/kg to 191.0 g/kg. Magnesium (Mg) ranges from 1.0 g/kg to 3.5 g/kg. Manganese (Mn) ranges from 0.2 g/kg to 166.0 g/kg. Phosphorus (P) ranges from 1.0 g/kg to 10.3 g/kg. Potassium (K) ranges from 1.7 g/kg to 15.4 g/kg. Sodium (Na) ranges from 0.7 g/kg to 15.6 g/kg. Zinc (Zn) ranges from 0.7 g/kg to 103.0 g/kg. However, in addition to the accumulation of the above minerals, some toxic and harmful elements (such as Ba, Hg and Mo) will also bioaccumulate in BSFL [85], which will pose a challenge to the safety of feed and food production [86].

3.5. Different Factors of Nutritional Value of BSFL (Hermetia illucens L.)

The content of minerals and other nutrients in BSFL significantly varies across different studies, and the reasons may be as follows:
First, it may be that the growth stages of BSFL are different. On the 4–14th days, the crude fat content of larvae increased rapidly, and the highest level could reach 28.4%, while crude protein showed a continuous downward trend at the same developmental stage. With the development of pupa, crude fat dropped sharply to 24.2%. The maximum crude protein in adulthood is 57.6% and the fat level is 21.6% [88].
Second, in relation to the nutritional structure ingested by BSFL, the content of fat and ash fed from vegetable waste, chicken feed and kitchen waste varies greatly [23,89]. In addition, BSFL on cow dung grow at a much slower rate of individual size than on poultry feed [90,91].
Third, it may be related to the processing method. Different killing methods (such as blanching, drying, freezing, high hydrostatic pressure grinding, and asphyxiation) also had an effect on pH, ash, fat content and oxidative capacity [92,93]. The temperature and method during storage also affect the nutritional quality of BSFL [94]. Different extraction methods also have a different nutrient content; for example, the best separation of protein is through alkali extraction [95]. When the processing temperature is 25 °C, the shelf life of BSFL can reach seven months [96].
Fourth, it is related to various factors such as temperature, humidity, sunlight, moisture content, pH, etc. Humidity and temperature will obviously affect the incubation, development and lifespan of BSFL [97,98]. Temperatures between 26 and 40 °C and relative humidity between 40–70% are the ideal living conditions for BSFL [55,99]. Sunlight also affects the nutrient composition of BSFL, with black soldier flies developing best in the wavelength range between 450 and 700 nm [54,100]. When the water content in the feed matrix is 60–80%, the survival rate and growth rate of BSFL are the highest [37,101]. The growth of black soldier flies is better under alkaline conditions than under acidic conditions, and a suitable pH value is between 6–9 [102,103].

4. Nutrition of BSFL (Hermetia illucens L.) in Poultry

4.1. Growth Performance

The effects of BSFL on the growth performance of poultry are shown in Table 5. Replacing 50% or 100% of soybean meal in layer diets with defatted BSFL had no effect on feed intake, egg production, yolk, shell weight, and the occurrence of mortality [104]. However, Murawska et al. [105] used full-fat BSFL instead of soybean meal. When 100% was replaced, the LW of the whole stage and average daily gain (ADG) (days 1–14 and days 14–35) were reduced. The higher the replacement level, the lower the daily feed intake (DFI), FCR, carcass weight, and muscle weight. In addition, abdominal fat deposits were also increased. This may be due to the fact that BSFL are not defatted, and the 100% replacement of soybean meal results in a high proportion of saturated fatty acids in the diet. Dabbou et al. [106] found that the dietary supplementation of 10% BSFL significantly increased LW, ADG, DFI, and FCR on days 10–35, whereas it did not affect FCR on days 1–10. Similar results were obtained by Onsogo et al. [68], who indicated that supplementation of 10% BSFL in the diet increased the final weight of broilers. However, Kawaseki et al. [107] indicated that supplementation of 10% BSFL had no effect on feed intake, BW, liver weight, egg-laying rate, and egg shell weight, but increased the richness of cecal microbiota. Schiavone et al. [31] reported that supplementation of 10% BSFL had no effect on daily weight gain (DWG), DFI and FCR, live weight (LW), chilled carcass, breast, thighs, abdominal fat, liver, heart, and spleen. Studies by others have produced similar results; supplementation of BSFL in the diet of chickens did not affect the LW, ADG, DFI, FCR, chilled carcass, breast, thighs, abdominal fat, liver, heart, and spleen [68,105,108,109]. Gariglio et al. [110] found that dietary supplementation of BSFL did not affect the LW, ADG, DFI, and FCR of ducks, but reduced SW and corresponding hot carcass (HC) and chilled carcass (CC). The abdominal fat weight showed a quadratic response, the lowest corresponding to the 6% group. To sum up, the analysis of the above results, adding 10% BSFL to the diet can improve the growth performance of chickens; 100% of soybean meal had a negative impact, and adding other levels had no effect.

4.2. Antioxidants and Immunity

The effects of BSFL on the antioxidants and immunity of poultry are shown in Table 6. Dabbou et al. [106] found that dietary supplementation of 5%, 10%, and 15% BSFL had no effect on erythrocyte, aspartate aminotransferase (AST), creatinine, triglycerides, cholesterol, heterophiles to lymphocytes ratio (H/L), leukocyte and urea acid, but increased levels of glutathione peroxidase (GPx) and total antioxidant status (TAS). Gariglio et al. [109] also obtained similar results, finding that supplementing 3%, 6%, and 9% BSFL had no effect on the erythrocyte, heterophils, lymphocytes, basophils AST, alanine aminotransferase (ALT) and gamma-glutamyl transferase (GGT) of chickens. However, the concentration of cholesterol dropped from 30.23% to 23.86% in the 9% group compared with the control, and also reduced malondialdehyde (MDA) and nitrotyrosine levels in plasma. These data indicate that BSFL have antioxidant capacity. Schiavone et al. [31] report that even substituting 100% of BSFL had no effect on the biochemical immune performance of broilers. These results are in agreement with the findings of Loponte et al. and Bellezza Oddon et al. [108,111], who showed that supplementation of 5% BSFL had no effect on the biochemical immune performance of chickens. However, the findings of Marono et al. [112] were slightly different from the above results. Supplementation of 100% BSFL increased concentrations of cholesterol, globulin, and triglycerides, but had no effect on other immune parameters. Gariglio et al. [109] showed that the supplementation of BSFL in a duck’s diet did not affect the levels of plasma AST, ALT, GGT, GPx, TAS, and methylglyoxal (MG), while MDA decreased linearly with the increase in BSFL. The above findings on the ratio of globulin to albumin provide an overall increase in circulating immunoglobulins, demonstrating that the supplementation of BSFL in poultry diets has a greater resistance to disease and better immune function, at least without adverse effects or influences [22].

4.3. Meat Quality and Nutritional Content

The effects of BSFL on the meat quality and nutritional content of poultry are shown in Table 7. The study by Cullere et al. [113] using BSFL to replace soybean oil found that it had no effect on moisture, protein, lipid and ash in meat, cholesterol and TBARs; pH, L*, a*, b*, thawing loss and cooking loss had no effect either. However, it did increase ratio levels of SFA and n-6/n-3, and reduce MUFA, PUFA and n-3 PUFA. Similar results were obtained by Moula et al. [114], who reported that the FA content of added BSFL was 36.7% higher than that of the control group, which was 33.8%. Murawska et al. [105] obtained different research results, finding that BSFL replacing 50% soybean meal can increase muscle b* and replacing more than 75% will increase muscle pH, but there is no effect on aroma intensity or desirability. The study by Schiavone et al. [115] showed that the dietary supplementation of 10% BSFL increased a* and the protein content of muscle; at 15% supplementation, b* and moisture in the muscle were reduced, and the ratio of FA/PUFA gradually increased with increasing levels of supplementation. The higher red color may be due to the accumulation of pigments in the insect meal in the meat, while the yellow color may be related to the corn gluten content of the insect meal’s diet. Muscle FA content is directly related to the type of fatty acid in BSFL. Cullere et al. [116] found that supplementation of 10% and 15% BSFL increased the content of aspartic acid, glutamic acid, alanine, serine, tyrosine, and threonine in muscle. This shows that the amino acids in BSFL can be absorbed and preserved by poultry. Gariglio et al. [110] found that black soldier flies did not affect pH 24 and the color of the chest and thigh muscles. BSFL did not affect the SFA content of breast meat, and the levels of lauric acid (C12:0) and myristic acid (C14:0) increased with the increase in BSFL; α-linolenic acid (C18:3 n-3) in breast meat also significantly increased. Linear quadratic decline and the ratio of ∑n-6/∑n-3 of breast and thigh meat decreased linearly, with the lowest in the 9% group.

5. Nutrition of BSFL (Hermetia illucens L.) in Swine

5.1. Growth Performance

Table 8 shows the effect of BSFL on pig growth performance. The use of BSFL to replace fish meal in part or entirely increased the average daily gain of finishing pigs. The final body weight, fasted weight, and carcass weight were significantly higher in the 50% and 100% supplemented groups than in the unsupplemented and 25% supplemented groups. The FCR of the BSFL-supplemented diet, however, was significantly lower than that of the unsupplemented group [117]. Driemeyer [118] supplemented 3.5% BSFL in piglet diets without affecting ADG, DMI, and digestibility, but reduced FCR. Crosbie et al. [77] found that on the seventh day, the weight of pigs fed the 25% BSFL diet was higher than that of the pigs fed the 50% diet, and the BSFL had no effect on body weight at other stages, decreased ADMI and G: F on days 14–21. Biasato et al. [119] found that BSFL did not affect the digestibility of BW, WG, ADG, ADFI, FCR, and nutrients of piglets. A similar result was obtained by Ipena et al. [120], who found that supplementation of BSFL did not affect average daily gain and the final body weight of piglets, nor did they affect their feed efficiency and energy efficiency, and had an effect on piglet diarrhea. Yu et al. [121] showed that supplementing 4% BSFL increased the abundance of lactobacillus, pseudo-butyric vibrio, rosella, and faecalibacterium in the swine intestinal tract, while the abundance of streptococcus decreased. Supplementation at a level of 8% increased the number of Clostridium cluster XIVa. The above results indicate that BSFL not only had no negative effects on the feed intake, digestion and growth performance of pigs, but also promoted the development of gut microbes while reducing FCR.

5.2. Antioxidants, Immunity, and Meat Quality

Since there is not as much research on BSFL in swine as there is in poultry, we counted blood indicators and meat quality indicators together. The effects of BSFL on the antioxidants, immunity, and meat quality of pigs are shown in Table 9. Research by Biasato et al. [119] showed that dietary BSFL supplementation had no significant effect on the animals’ blood chemistry profile or serum protein, except that monocytes and neutrophils exhibited linear and quadratic responses, respectively, to increases in the dietary levels of BSFL. Research by Chia et al. [117] showed that replacing 50% of fish meal with BSFL increases the muscle protein content, while BSFL at any level increases muscle total fat and organic matter (OM) content, but has no effect on muscle water content. Altmann et al. [122] found that the dietary supplementation of BSFL had very little effect on pork quality parameters and sensory attributes. All physicochemical parameters, except backfat (L*), were not affected by diet. In addition, BSFL increased the content of polyunsaturated fatty acids (PUFA), GLA and linoleic acid (C18:2), and lauric acid (C12:0) was five times higher. This may be related to the content of saturated fatty acids in BSFL.

6. Challenges of Using BSFL (Hermetia illucens L.)

6.1. Security and Legal Issues

At present, the main obstacles to the large-scale use of BSFL in animal feed are the legal regulations related to food safety [123]. Despite the existence of substantial funding for research on BSFL, restrictive European laws regarding the use of insects in animal feed remain a major challenge for the development of insect production units [124]. The Food and Agriculture Organization of the United Nations’ global food regulations establishes safe conditions for BSFL to meet the production of insects for breeding and pet animal feed [125]. That is: “These should not be pathogenic or have other adverse effects on plant, animal or human health; they should not be considered carriers of plant, animal or human pathogens and should not be protected or defined as invasive alien species”. They also place restrictions on the substrates of BSFL’s nutritional source: the substrate must contain “products of non-animal origin” or a limited set of animal products, including fish meal, refined fats, blood and gelatin from non-ruminant animals, milk, eggs, honey, etc. Meat, manure, “catering waste” and “other waste” are explicitly excluded [126]. Although the U.S. Food and Drug Administration (FDA) has an official Memorandum of Understanding with the American Association of Feed Control Officials (AAFCO) for all regulations governing animal feed, it is also only sold as a human novelty food and is not expressly identified as food [126,127].

6.2. Consumer Acceptance

Consumer acceptance of BSFL-fed animal meat products should also be considered. There is general support for the idea of using insects in animal feed, especially in fish and poultry feed. A questionnaire found that two-thirds of study participants were willing to accept the use of insects in animal feed [128]. Sogari et al. [129] also obtained similar findings, with the most accepted being the use of insects in fish feed. This shows that consumers still have certain doubts about insect-fed animals, and efforts need to be made to improve consumers’ perceptions of insect-fed animal meat products. In addition, there are also findings of direct human consumption of BSFL. In the Malaysian province of Sabah on the island of Borneo, more than 60 species of insects are eaten, primarily by certain groups of the indigenous Kadazan Dusun people. BSFL are one of them and are eaten raw with a locally brewed fermented beverage called tapai [130]. In addition, the strong relationship between dietary SFA and coronary heart disease (CHD) risk may also be one of the reasons why consumers do not want to consume BSFL directly [131].

6.3. Production and Price

At present, there is no unified standard for the production and subsequent processing of BSFL. Due to the small scale of production equipment, low yield, and low efficiency, there is only enough BSFL for consumers who are early adopters and will use them in small amounts for scientific research feed [132]. Mass production is still a long way off. In this case, the availability and price of BSFL are not competitive with soybean meal and fish meal, resulting in BSFL not being widely used in poultry or swine diets [124].

7. Conclusions

In conclusion, the high protein content of BSFL has great potential as a protein source in poultry and swine diets, although there is no information on its application in ruminant diets. According to the results of its application in monogastric animals and ruminants with a special rumen function, BSFL has a lot of room for future development in ruminant feed. Although studies on the effects of BSFL on growth performance, antioxidants, immunity, and meat quality in pigs and poultry have been inconsistent (as to whether they have caused improvement or not), there have been no reports of the negative effects of BSFL on pigs or poultry. This shows that BSFL can replace soybean meal or fish meal as a feed protein source. Due to the relatively short application time of BSFL in animal feed, the development of related laws is relatively backward. It is necessary to formulate standard production and processing procedures and improve relevant laws to promote the production of BSFL and reduce prices. Furthermore, consumer acceptance of meat products from insect-fed animals is a challenge to overcome.

Author Contributions

Conceptualization, S.L., N.T., W.M., J.S., B.S., T.S., P.A., S.T., S.P., R.A.P.P. and P.P.; methodology, S.L., S.P., R.A.P.P. and P.P.; investigation, S.L.; resources, S.L., N.T., W.M., J.S., B.S., T.S., P.A., S.T., S.P., R.A.P.P. and P.P.; data curation, S.L., writing—original draft preparation, S.L. and R.A.P.P.; writing—review and editing, S.L., S.P., R.A.P.P. and P.P.; visualization, S.L.; supervision, S.P., R.A.P.P. and P.P.; project administration, N.T., S.T., S.P., R.A.P.P. and P.P.; funding acquisition, S.P., R.A.P.P. and P.P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Suranaree University of Technology (SUT; contract no. Fulltime 61/02/2021), Thailand Science Research and Innovation (TSRI), National Science Research and Innovation Fund (NSRF; project codes: 90464; 160368; FF3-303-65-36-17), National Research Council of Thailand (NRCT; project code: 900105), and Nakhon Ratchasima Rajabhat University (NRRU).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All other material is from published literature referenced in the reference list.

Acknowledgments

The authors would like to thank the staff of the Centre of Scientific and Technological Equipment and the Suranaree University of Technology goat and sheep farm, Siriwan Phetsombat, and Thara Wongdee for helpful discussions during preparation of the manuscript.

Conflicts of Interest

The authors declare no competing interests.

Nomenclature

a* = red/green value, ADFI = average daily feed intake, ADG = average daily gain, ALP = alkaline phosphatase, ALT = alanine aminotransferase, AST = aspartate amino transferase, b* = blue/yellow value, BUN = blood urea nitrogen, BW = body weight, BSFL = black soldier fly larvae, CSBM = conventional soybeans meal, D = days, DF = defatted, DFI = daily feed intake, DMI = dry matter intake, DWG = daily weight gain, FA = fatty acid, FBW = final body weight, FCR = feed conversion ratio, FF = full-fat, FM = fish meal, G: F = gain: feed, WG = weight gain, GGT = gamma-glutamyl transferase, GLA = gamma linolenic acid, GOT = glutamic oxaloacetic transaminase, GPT = glutamate-pyruvate transaminase, GPx = glutathione peroxidase, H/ L = heterophiles to lymphocytes ratio, HDL = high-density lipoproteins, L * = lightness, LDL = low-density lipoproteins, LW = live weight, MCH = mean corpuscular hemoglobin, MCV = mean corpuscular volume, MDA = malondialdehyde, MG = methylglyoxal, MUFA = monounsaturated fatty acid, OM = organic matter, PUFA = polyunsaturated fatty acids, SFA = saturated fatty acid, TAS = total antioxidant status, TBARs = thiobarbituric acid reactant.

References

  1. Statistics, F.G.F. What Is the Global Feed Industry. International Feed Industry Federation Factsheet; International Feed Industry Federation (IFIF): Wiehl, Germany, 2019; Available online: https://ifif.org/wp-content/uploads/2019/06/IFIF-Fact-Sheet-October-11th-2019.pdf (accessed on 11 October 2019).
  2. McLeod, A. World Livestock 2011-Livestock in Food Security; Food and Agriculture Organization of the United Nations (FAO): Rome, Italy, 2011. [Google Scholar]
  3. Tiengtam, N.; Paengkoum, P.; Sirivoharn, S.; Phonsiri, K.; Boonanuntanasarn, S. The effects of dietary inulin and Jerusalem artichoke (Helianthus tuberosus) tuber on the growth performance, haematological, blood chemical and immune parameters of Nile tilapia (Oreochromis niloticus) fingerlings. Aquac. Res. 2017, 48, 5280–5288. [Google Scholar] [CrossRef]
  4. Paengkoum, P.; Thongpea, S.; Paengkoum, S. Utilization of concentrate supplements containing varying levels of cassava leaf pellet by growing goats fed a basal diet of pangola hay. Indian J. Anim. Res. 2017, 51, 1091–1096. [Google Scholar] [CrossRef]
  5. Kaewwongsa, W.; Traiyakun, S.; Yuangklang, C.; Wachirapakorn, C.; Paengkoum, P. Protein enrichment of cassava pulp fermentation by Saccharomyces cerevisiae. J. Anim. Vet. Adv. 2011, 10, 2434–2440. [Google Scholar]
  6. Parisi, G.; Tulli, F.; Fortina, R.; Marino, R.; Bani, P.; Dalle Zotte, A.; De Angelis, A.; Piccolo, G.; Pinotti, L.; Schiavone, A. Protein hunger of the feed sector: The alternatives offered by the plant world. Ital. J. Anim. Sci. 2020, 19, 1204–1225. [Google Scholar] [CrossRef]
  7. Van Huis, A.; Oonincx, D.G. The environmental sustainability of insects as food and feed. A review. Agron. Sustain. Dev. 2017, 37, 43. [Google Scholar] [CrossRef]
  8. Chen, S.; Paengkoum, P.; Xia, X.; Na-Lumpang, P. Effects of dietary protein on ruminal fermentation, nitrogen utilization and crude protein maintenance in growing Thai-indigenous beef cattle fed rice straw as roughage. J. Anim. Vet. Adv. 2010, 9, 2396–2400. [Google Scholar] [CrossRef]
  9. Allegretti, G.; Talamini, E.; Schmidt, V.; Bogorni, P.C.; Ortega, E. Insect as feed: An emergy assessment of insect meal as a sustainable protein source for the Brazilian poultry industry. J. Clean. Prod. 2018, 171, 403–412. [Google Scholar] [CrossRef]
  10. Dicke, M. Insects as feed and the Sustainable Development Goals. J. Insects Food Feed 2018, 4, 147–156. [Google Scholar] [CrossRef]
  11. Purba, R.A.P.; Paengkoum, S.; Yuangklang, C.; Paengkoum, P. Flavonoids and their aromatic derivatives in Piper betle powder promote in vitro methane mitigation in a variety of diets. Ciência Agrotecnologia 2020, 44, e012420. [Google Scholar] [CrossRef]
  12. Purba, R.; Yuangklang, C.; Paengkoum, S.; Paengkoum, P. Milk fatty acid composition, rumen microbial population and animal performance in response to diets rich in linoleic acid supplemented with Piper betle leaves in Saanen goats. Anim. Prod. Sci. 2020, 62, 1391–1401. [Google Scholar] [CrossRef]
  13. Paengkoum, P.; Liang, J.; Jelan, Z.; Basery, M. Utilization of steam-treated oil palm fronds in growing saanen goats: II. Supplementation with energy and urea. Asian-Australas. J. Anim. Sci. 2006, 19, 1623–1631. [Google Scholar] [CrossRef]
  14. Wanapat, M.; Chumpawadee, S.; Paengkoum, P. Utilization of urea-treated rice straw and whole sugar cane crop as roughage sources for dairy cattle during the dry season. Asian-Australas. J. Anim. Sci. 2000, 13, 474–477. [Google Scholar] [CrossRef]
  15. Vorlaphim, T.; Paengkoum, P.; Purba, R.A.P.; Yuangklang, C.; Paengkoum, S.; Schonewille, J.T. Treatment of rice stubble with Pleurotus ostreatus and urea improves the growth performance in slow-growing goats. Animals 2021, 11, 1053. [Google Scholar] [CrossRef]
  16. Paengkoum, P.; Liang, J.; Jelan, Z.; Basery, M. Utilization of steam-treated oil palm fronds in growing goats: 1. supplementation with dietary urea. Asian-Australas. J. Anim. Sci. 2006, 19, 1305–1313. [Google Scholar] [CrossRef]
  17. Patra, A.K.; Aschenbach, J.R. Ureases in the gastrointestinal tracts of ruminant and monogastric animals and their implication in urea-N/ammonia metabolism: A review. J. Adv. Res. 2018, 13, 39–50. [Google Scholar] [CrossRef]
  18. Schiavone, A.; De Marco, M.; Martínez, S.; Dabbou, S.; Renna, M.; Madrid, J.; Hernandez, F.; Rotolo, L.; Costa, P.; Gai, F. Nutritional value of a partially defatted and a highly defatted black soldier fly larvae (Hermetia illucens L.) meal for broiler chickens: Apparent nutrient digestibility, apparent metabolizable energy and apparent ileal amino acid digestibility. J. Anim. Sci. Biotechnol. 2017, 8, 51. [Google Scholar] [CrossRef]
  19. Gasco, L.; Dabbou, S.; Trocino, A.; Xiccato, G.; Capucchio, M.T.; Biasato, I.; Dezzutto, D.; Birolo, M.; Meneguz, M.; Schiavone, A. Effect of dietary supplementation with insect fats on growth performance, digestive efficiency and health of rabbits. J. Anim. Sci. Biotechnol. 2019, 10, 4. [Google Scholar] [CrossRef]
  20. Oonincx, D.G.; De Boer, I.J. Environmental impact of the production of mealworms as a protein source for humans–a life cycle assessment. PLoS ONE 2012, 7, e51145. [Google Scholar] [CrossRef]
  21. Oonincx, D.G.; Van Broekhoven, S.; Van Huis, A.; van Loon, J.J. Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. PLoS ONE 2015, 10, e0144601. [Google Scholar] [CrossRef]
  22. El-Hack, A.; Mohamed, E.; Shafi, M.E.; Alghamdi, W.Y.; Abdelnour, S.A.; Shehata, A.M.; Noreldin, A.E.; Ashour, E.A.; Swelum, A.A.; Al-Sagan, A.A. Black soldier fly (Hermetia illucens) meal as a promising feed ingredient for poultry: A comprehensive review. Agriculture 2020, 10, 339. [Google Scholar] [CrossRef]
  23. Spranghers, T.; Ottoboni, M.; Klootwijk, C.; Ovyn, A.; Deboosere, S.; De Meulenaer, B.; Michiels, J.; Eeckhout, M.; De Clercq, P.; De Smet, S. Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates. J. Sci. Food Agric. 2017, 97, 2594–2600. [Google Scholar] [CrossRef] [PubMed]
  24. Meneguz, M.; Schiavone, A.; Gai, F.; Dama, A.; Lussiana, C.; Renna, M.; Gasco, L. Effect of rearing substrate on growth performance, waste reduction efficiency and chemical composition of black soldier fly (Hermetia illucens) larvae. J. Sci. Food Agric. 2018, 98, 5776–5784. [Google Scholar] [CrossRef] [PubMed]
  25. Tian, X.; Lu, Q.; Paengkoum, P.; Paengkoum, S. Effect of purple corn pigment on change of anthocyanin composition and unsaturated fatty acids during milk storage. J. Dairy Sci. 2020, 103, 7808–7812. [Google Scholar] [CrossRef] [PubMed]
  26. Bukkens, S.G. The nutritional value of edible insects. Ecol. Food Nutr. 1997, 36, 287–319. [Google Scholar] [CrossRef]
  27. Tabata, E.; Kashimura, A.; Wakita, S.; Ohno, M.; Sakaguchi, M.; Sugahara, Y.; Kino, Y.; Matoska, V.; Bauer, P.O.; Oyama, F. Gastric and intestinal proteases resistance of chicken acidic chitinase nominates chitin-containing organisms for alternative whole edible diets for poultry. Sci. Rep. 2017, 7, 6662. [Google Scholar] [CrossRef]
  28. Nyakeri, E.; Ogola, H.; Ayieko, M.; Amimo, F. An open system for farming black soldier fly larvae as a source of proteins for smallscale poultry and fish production. J. Insects Food Feed 2017, 3, 51–56. [Google Scholar] [CrossRef]
  29. Veldkamp, T.; Bosch, G. Insects: A protein-rich feed ingredient in pig and poultry diets. Anim. Front. 2015, 5, 45–50. [Google Scholar]
  30. Zuki, N.M.; Ibrahim, N.; Mat, K.; Rusli, N.; Harun, H.; Mahmud, M.; Samat, N.; Al-Amsyar, S. Hybrid treatment of black soldier fly larvae (Hermetia illucens) as a sustainable and efficient protein source in poultry diets. IOP Conf. Series: Earth Environ. Sci. 2021, 756, 012031. [Google Scholar]
  31. Schiavone, A.; Dabbou, S.; De Marco, M.; Cullere, M.; Biasato, I.; Biasibetti, E.; Capucchio, M.; Bergagna, S.; Dezzutto, D.; Meneguz, M. Black soldier fly larva fat inclusion in finisher broiler chicken diet as an alternative fat source. Animal 2018, 12, 2032–2039. [Google Scholar] [CrossRef]
  32. Nguyen, T.T.; Tomberlin, J.K.; Vanlaerhoven, S. Ability of black soldier fly (Diptera: Stratiomyidae) larvae to recycle food waste. Environ. Entomol. 2015, 44, 406–410. [Google Scholar] [CrossRef]
  33. Zhou, F.; Tomberlin, J.K.; Zheng, L.; Yu, Z.; Zhang, J. Developmental and waste reduction plasticity of three black soldier fly strains (Diptera: Stratiomyidae) raised on different livestock manures. J. Med. Entomol. 2013, 50, 1224–1230. [Google Scholar] [CrossRef] [PubMed]
  34. Mallin, M.A.; Cahoon, L.B. Industrialized animal production—a major source of nutrient and microbial pollution to aquatic ecosystems. Popul. Environ. 2003, 24, 369–385. [Google Scholar] [CrossRef]
  35. Zheng, L.; Li, Q.; Zhang, J.; Yu, Z. Double the biodiesel yield: Rearing black soldier fly larvae, Hermetia illucens, on solid residual fraction of restaurant waste after grease extraction for biodiesel production. Renew. Energy 2012, 41, 75–79. [Google Scholar] [CrossRef]
  36. Lalander, C.; Diener, S.; Magri, M.E.; Zurbrügg, C.; Lindström, A.; Vinnerås, B. Faecal sludge management with the larvae of the black soldier fly (Hermetia illucens)—From a hygiene aspect. Sci. Total Environ. 2013, 458, 312–318. [Google Scholar] [CrossRef] [PubMed]
  37. Banks, I.J.; Gibson, W.T.; Cameron, M.M. Growth rates of black soldier fly larvae fed on fresh human faeces and their implication for improving sanitation. Trop. Med. Int. Health 2014, 19, 14–22. [Google Scholar] [CrossRef]
  38. Erickson, M.C.; Islam, M.; Sheppard, C.; Liao, J.; Doyle, M.P. Reduction of Escherichia coli O157: H7 and Salmonella enterica serovar Enteritidis in chicken manure by larvae of the black soldier fly. J. Food Prot. 2004, 67, 685–690. [Google Scholar] [CrossRef]
  39. Purba, R.A.P.; Yuangklang, C.; Paengkoum, P. Enhanced conjugated linoleic acid and biogas production after ruminal fermentation with Piper betle L. supplementation. Ciência Rural 2020, 50, e20191001. [Google Scholar] [CrossRef]
  40. Paengkoum, P. Effects of neem (Azadirachta indica) and leucaena (Leucaena leucocephala) fodders on digestibility, rumen fermentation and nitrogen balance of goats fed corn silage. J. Anim. Vet. Adv. 2010, 9, 883–886. [Google Scholar] [CrossRef]
  41. Purba, R.A.P.; Yuangklang, C.; Paengkoum, S.; Paengkoum, P. Piper oil decreases in vitro methane production with shifting ruminal fermentation in a variety of diets. Int. J. Agric. Biol 2021, 25, 231–240. [Google Scholar]
  42. Liu, Q.; Tomberlin, J.K.; Brady, J.A.; Sanford, M.R.; Yu, Z. Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environ. Entomol. 2008, 37, 1525–1530. [Google Scholar] [CrossRef]
  43. James, M.T. The genus Hermetia in the United States (Diptera: Stratiomyidae). Bull. Brooklyn Entomol. Soc 1935, 30, 165–170. [Google Scholar]
  44. Shumo, M.; Khamis, F.M.; Tanga, C.M.; Fiaboe, K.K.; Subramanian, S.; Ekesi, S.; Van Huis, A.; Borgemeister, C. Influence of temperature on selected life-history traits of black soldier fly (Hermetia illucens) reared on two common urban organic waste streams in Kenya. Animals 2019, 9, 79. [Google Scholar] [CrossRef] [PubMed]
  45. Spranghers, T.; Noyez, A.; Schildermans, K.; De Clercq, P. Cold hardiness of the black soldier fly (Diptera: Stratiomyidae). J. Econ. Entomol. 2017, 110, 1501–1507. [Google Scholar] [CrossRef] [PubMed]
  46. Woodley, N.E. A world catalog of the Stratiomyidae (Insecta: Diptera): A supplement with revisionary notes and errata. Myia 2011, 12, 379–415. [Google Scholar]
  47. Singh, A.; Kumari, K. An inclusive approach for organic waste treatment and valorisation using Black Soldier Fly larvae: A review. J. Environ. Manag. 2019, 251, 109569. [Google Scholar] [CrossRef]
  48. Üstüner, T.; Hasbenlí, A.; Rozkošný, R. The first record of Hermetia illucens (Linnaeus, 1758) (Diptera, Stratiomyidae) from the Near East. Studia Dipterol. 2003, 1, 0945-3954. [Google Scholar]
  49. Chippindale, A.K.; Leroi, A.M.; Kim, S.B.; Rose, M.R. Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. In Methuselah Flies: A Case Study in the Evolution of Aging; World Scientific: Singapore, 2004; pp. 122–144. [Google Scholar]
  50. St-Hilaire, S.; Sheppard, C.; Tomberlin, J.K.; Irving, S.; Newton, L.; McGuire, M.A.; Mosley, E.E.; Hardy, R.W.; Sealey, W. Fly prepupae as a feedstuff for rainbow trout, Oncorhynchus mykiss. J. World Aquac. Soc. 2007, 38, 59–67. [Google Scholar] [CrossRef]
  51. Yu, G.; Chen, Y.; Yu, Z.; Cheng, P. Research progress on the larvae and prepupae of black soldier fly Hermetia illucens used as animal feedstuff. Chin. Bull. Entomol. 2009, 46, 41–45. [Google Scholar]
  52. Alvarez, L. The Role of Black Soldier Fly, Hermetia illucens (L.) (Diptera: Stratiomyidae) in Sustainable Waste Management in Northern Climates. 2012; Electronic Theses and Dissertations. 402. [Google Scholar]
  53. Diener, S. Valorisation of Organic Solid Waste Using the Black Soldier Fly, Hermetia illucens, in Low and Middle-Income Countries. Eth Zurich. 2010. [Google Scholar]
  54. Park, H.H. Black Soldier Fly Larvae Manual. 2016. Available online: http://scholarworks.umass.edu.erişim.tarihi/ (accessed on 1 September 2022).
  55. Sheppard, D.C.; Tomberlin, J.K.; Joyce, J.A.; Kiser, B.C.; Sumner, S.M. Rearing methods for the black soldier fly (Diptera: Stratiomyidae). J. Med. Entomol. 2002, 39, 695–698. [Google Scholar] [CrossRef]
  56. Gold, M.; Cassar, C.M.; Zurbrügg, C.; Kreuzer, M.; Boulos, S.; Diener, S.; Mathys, A. Biowaste treatment with black soldier fly larvae: Increasing performance through the formulation of biowastes based on protein and carbohydrates. Waste Manag. 2020, 102, 319–329. [Google Scholar] [CrossRef]
  57. Lalander, C.; Diener, S.; Zurbrügg, C.; Vinnerås, B. Effects of feedstock on larval development and process efficiency in waste treatment with black soldier fly (Hermetia illucens). J. Clean. Prod. 2019, 208, 211–219. [Google Scholar] [CrossRef]
  58. Dortmans, B.; Diener, S.; Bart, V.; Zurbrügg, C. Black Soldier Fly Biowaste Processing: A Step-by-Step Guide; Eawag: Dübendorf, Switzerland, 2017. [Google Scholar]
  59. Bortolini, S.; Macavei, L.I.; Saadoun, J.H.; Foca, G.; Ulrici, A.; Bernini, F.; Malferrari, D.; Setti, L.; Ronga, D.; Maistrello, L. Hermetia illucens (L.) larvae as chicken manure management tool for circular economy. J. Clean. Prod. 2020, 262, 121289. [Google Scholar] [CrossRef]
  60. Paengkoum, S.; Petlum, A.; Purba, R.A.P.; Paengkoum, P. Protein-binding affinity of various condensed tannin molecular weights from tropical leaf peel. J. Appl. Pharm. Sci. 2021, 11, 114–120. [Google Scholar]
  61. Paengkoum, P.; Chen, S.; Paengkoum, S. Effects of crude protein and undegradable intake protein on growth performance, nutrient utilization, and rumen fermentation in growing Thai-indigenous beef cattle. Trop. Anim. Health Prod. 2019, 51, 1151–1159. [Google Scholar] [CrossRef] [PubMed]
  62. Paengkoum, P.; Paengkoum, S. Effects of supplementing rice straw with Leucaena (Leucaena leucocephala) and Madras thorn (Pithecellobium dulce) foliages on digestibility, microbial N supply and nitrogen balance of growing goats. J. Anim. Physiol. Anim. Nutr. 2010, 94, e59–e65. [Google Scholar] [CrossRef]
  63. Siddiqui, S.A.; Ristow, B.; Rahayu, T.; Putra, N.S.; Yuwono, N.W.; Mategeko, B.; Smetana, S.; Saki, M.; Nawaz, A.; Nagdalian, A. Black soldier fly larvae (BSFL) and their affinity for organic waste processing. Waste Manag. 2022, 140, 1–13. [Google Scholar] [CrossRef]
  64. Newton, G.; Sheppard, D.; Watson, D.; Burtle, G.; Dove, C.; Tomberlin, J.; Thelen, E. The black soldier fly, Hermetia illucens, as a manure management/resource recovery tool. In Proceedings of the Symposium on the State of the Science of Animal Manure and Waste Management, San Antonio, TX, USA, 5–7 January 2005; p. 57. [Google Scholar]
  65. Yildirim-Aksoy, M.; Eljack, R.; Beck, B.H. Nutritional value of frass from black soldier fly larvae, Hermetia illucens, in a channel catfish, Ictalurus punctatus, diet. Aquac. Nutr. 2020, 26, 812–819. [Google Scholar] [CrossRef]
  66. Schiavone, A.; Cullere, M.; De Marco, M.; Meneguz, M.; Biasato, I.; Bergagna, S.; Dezzutto, D.; Gai, F.; Dabbou, S.; Gasco, L. Partial or total replacement of soybean oil by black soldier fly larvae (Hermetia illucens L.) fat in broiler diets: Effect on growth performances, feed-choice, blood traits, carcass characteristics and meat quality. Ital. J. Anim. Sci. 2017, 16, 93–100. [Google Scholar] [CrossRef]
  67. Council, N.R. Nutrient Requirements of Swine; Natl Acad Press: Washington, DC, USA, 2012. [Google Scholar]
  68. Onsongo, V.; Osuga, I.; Gachuiri, C.; Wachira, A.; Miano, D.; Tanga, C.; Ekesi, S.; Nakimbugwe, D.; Fiaboe, K. Insects for income generation through animal feed: Effect of dietary replacement of soybean and fish meal with black soldier fly meal on broiler growth and economic performance. J. Econ. Entomol. 2018, 111, 1966–1973. [Google Scholar] [CrossRef] [Green Version]
  69. Tyshko, N.V.; Zhminchenko, V.M.; Nikitin, N.S.; Trebukh, M.D.; Shestakova, S.I.; Pashorina, V.A.; Sadykova, E.O. The comprehensive studies of Hermetia illucens larvae protein’s biological value. Probl. Nutr. 2021, 90, 49–58. [Google Scholar] [CrossRef]
  70. Finke, M.D. Estimate of chitin in raw whole insects. Zoo Biol. Publ. Affil. Am. Zoo Aquar. Assoc. 2007, 26, 105–115. [Google Scholar] [CrossRef] [PubMed]
  71. Swiatkiewicz, S.; Swiatkiewicz, M.; Arczewska-Wlosek, A.; Jozefiak, D. Chitosan and its oligosaccharide derivatives (chito-oligosaccharides) as feed supplements in poultry and swine nutrition. J. Anim. Physiol. Anim. Nutr. 2015, 99, 1–12. [Google Scholar] [CrossRef] [PubMed]
  72. Li, J.; Shi, B.; Yan, S.; Jin, L.; Guo, Y.; Xu, Y.; Li, T.; Guo, X. Effects of dietary supplementation of chitosan on humoral and cellular immune function in weaned piglets. Anim. Feed Sci. Technol. 2013, 186, 204–208. [Google Scholar] [CrossRef]
  73. Wang, H.; ur Rehman, K.; Feng, W.; Yang, D.; ur Rehman, R.; Cai, M.; Zhang, J.; Yu, Z.; Zheng, L. Physicochemical structure of chitin in the developing stages of black soldier fly. Int. J. Biol. Macromol. 2020, 149, 901–907. [Google Scholar] [CrossRef] [PubMed]
  74. Shumo, M.; Osuga, I.M.; Khamis, F.M.; Tanga, C.M.; Fiaboe, K.K.; Subramanian, S.; Ekesi, S.; van Huis, A.; Borgemeister, C. The nutritive value of black soldier fly larvae reared on common organic waste streams in Kenya. Sci. Rep. 2019, 9, 10110. [Google Scholar] [CrossRef] [PubMed]
  75. Rawski, M.; Mazurkiewicz, J.; Kierończyk, B.; Józefiak, D. Black soldier fly full-fat larvae meal as an alternative to fish meal and fish oil in Siberian sturgeon nutrition: The effects on physical properties of the feed, animal growth performance, and feed acceptance and utilization. Animals 2020, 10, 2119. [Google Scholar] [CrossRef]
  76. de Souza Vilela, J.; Alvarenga, T.I.; Andrew, N.R.; McPhee, M.; Kolakshyapati, M.; Hopkins, D.L.; Ruhnke, I. Technological quality, amino acid and fatty acid profile of broiler meat enhanced by dietary inclusion of black soldier fly larvae. Foods 2021, 10, 297. [Google Scholar] [CrossRef]
  77. Crosbie, M.; Zhu, C.; Shoveller, A.K.; Huber, L.-A. Standardized ileal digestible amino acids and net energy contents in full fat and defatted black soldier fly larvae meals (Hermetia illucens) fed to growing pigs. Transl. Anim. Sci. 2020, 4, txaa104. [Google Scholar] [CrossRef]
  78. Müller, A.; Wolf, D.; Gutzeit, H.O. The black soldier fly, Hermetia illucens–a promising source for sustainable production of proteins, lipids and bioactive substances. Z. Nat. C 2017, 72, 351–363. [Google Scholar] [CrossRef]
  79. Shah, A.A.; Totakul, P.; Matra, M.; Cherdthong, A.; Hanboonsong, Y.; Wanapat, M. Nutritional composition of various insects and potential uses as alternative protein sources in animal diets. Anim. Biosci. 2022, 35, 317. [Google Scholar] [CrossRef]
  80. Romano, N.; Fischer, H.; Kumar, V.; Francis, S.A.; Sinha, A.K. Productivity, conversion ability, and biochemical composition of black soldier fly (Hermetia illucens) larvae fed with sweet potato, spent coffee or dough. Int. J. Trop. Insect Sci. 2022, 42, 183–190. [Google Scholar] [CrossRef]
  81. Ewald, N.; Vidakovic, A.; Langeland, M.; Kiessling, A.; Sampels, S.; Lalander, C. Fatty acid composition of black soldier fly larvae (Hermetia illucens)–Possibilities and limitations for modification through diet. Waste Manag. 2020, 102, 40–47. [Google Scholar] [CrossRef] [PubMed]
  82. Daszkiewicz, T.; Murawska, D.; Kubiak, D.; Han, J. Chemical composition and fatty acid profile of the pectoralis major muscle in broiler chickens fed diets with full-fat black soldier fly (Hermetia illucens) larvae meal. Animals 2022, 12, 464. [Google Scholar] [CrossRef] [PubMed]
  83. Nayohan, S.; Susanto, I.; Permata, D.; Pangesti, R.T.; Rahmadani, M.; Jayanegara, A. Effect of dietary inclusion of black soldier fly larvae (Hermetia illucens) on broiler performance: A meta-analysis. Proc. E3S Web Conf. 2022, 335, 00013. [Google Scholar] [CrossRef]
  84. Rabani, V.; Cheatsazan, H.; Davani, S. Proteomics and lipidomics of black soldier fly (Diptera: Stratiomyidae) and blow fly (Diptera: Calliphoridae) larvae. J. Insect Sci. 2019, 19, 29. [Google Scholar] [CrossRef]
  85. Bulak, P.; Wiącek, D.; Bieganowski, A. Hermetia illucens exhibits bioaccumulative potential for 15 different elements-Implications for feed and food production. Sci. Total Environ. 2020, 723, 138125. [Google Scholar]
  86. Petlum, A.; Paengkoum, P.; Liang, J.; Vasupen, K.; Paengkoum, S. Molecular weight of condensed tannins of some tropical feed-leaves and their effect on in vitro gas and methane production. Anim. Prod. Sci. 2019, 59, 2154–2160. [Google Scholar] [CrossRef]
  87. Smets, R.; Verbinnen, B.; Van De Voorde, I.; Aerts, G.; Claes, J.; Van Der Borght, M. Sequential extraction and characterisation of lipids, proteins, and chitin from black soldier fly (Hermetia illucens) larvae, prepupae, and pupae. Waste Biomass Valorization 2020, 11, 6455–6466. [Google Scholar] [CrossRef]
  88. Liu, X.; Chen, X.; Wang, H.; Yang, Q.; ur Rehman, K.; Li, W.; Cai, M.; Li, Q.; Mazza, L.; Zhang, J. Dynamic changes of nutrient composition throughout the entire life cycle of black soldier fly. PLoS ONE 2017, 12, e0182601. [Google Scholar] [CrossRef] [PubMed]
  89. Tschirner, M.; Simon, A. Influence of different growing substrates and processing on the nutrient composition of black soldier fly larvae destined for animal feed. J. Insects Food Feed 2015, 1, 249–259. [Google Scholar] [CrossRef]
  90. Diener, S.; Zurbrügg, C.; Tockner, K. Conversion of organic material by black soldier fly larvae: Establishing optimal feeding rates. Waste Manag. Res. 2009, 27, 603–610. [Google Scholar] [CrossRef] [PubMed]
  91. Myers, H.M.; Tomberlin, J.K.; Lambert, B.D.; Kattes, D. Development of black soldier fly (Diptera: Stratiomyidae) larvae fed dairy manure. Environ. Entomol. 2014, 37, 11–15. [Google Scholar] [CrossRef]
  92. Larouche, J.; Deschamps, M.-H.; Saucier, L.; Lebeuf, Y.; Doyen, A.; Vandenberg, G.W. Effects of killing methods on lipid oxidation, colour and microbial load of black soldier fly (Hermetia illucens) larvae. Animals 2019, 9, 182. [Google Scholar] [CrossRef] [PubMed]
  93. Purba, R.A.P.; Paengkoum, S.; Paengkoum, P. Development of a simple high-performance liquid chromatography-based method to quantify synergistic compounds and their composition in dried leaf extracts of Piper sarmentosum Robx. Separations 2021, 8, 152. [Google Scholar] [CrossRef]
  94. Saucier, L.; M’ballou, C.; Ratti, C.; Deschamps, M.-H.; Lebeuf, Y.; Vandenberg, G. Comparison of black soldier fly larvae pre-treatments and drying techniques on the microbial load and physico-chemical characteristics. J. Insects Food Feed 2022, 8, 45–64. [Google Scholar] [CrossRef]
  95. Caligiani, A.; Marseglia, A.; Leni, G.; Baldassarre, S.; Maistrello, L.; Dossena, A.; Sforza, S. Composition of black soldier fly prepupae and systematic approaches for extraction and fractionation of proteins, lipids and chitin. Food Res. Int. 2018, 105, 812–820. [Google Scholar] [CrossRef]
  96. Kamau, E.; Mutungi, C.; Kinyuru, J.; Imathiu, S.; Tanga, C.; Affognon, H.; Ekesi, S.; Nakimbugwe, D.; Fiaboe, K. Moisture adsorption properties and shelf-life estimation of dried and pulverised edible house cricket Acheta domesticus (L.) and black soldier fly larvae Hermetia illucens (L.). Food Res. Int. 2018, 106, 420–427. [Google Scholar] [CrossRef]
  97. Chia, S.Y.; Tanga, C.M.; Khamis, F.M.; Mohamed, S.A.; Salifu, D.; Sevgan, S.; Fiaboe, K.K.; Niassy, S.; van Loon, J.J.; Dicke, M. Threshold temperatures and thermal requirements of black soldier fly Hermetia illucens: Implications for mass production. PLoS ONE 2018, 13, e0206097. [Google Scholar] [CrossRef]
  98. Tomberlin, J.K.; Adler, P.H.; Myers, H.M. Development of the black soldier fly (Diptera: Stratiomyidae) in relation to temperature. Environ. Entomol. 2009, 38, 930–934. [Google Scholar] [CrossRef]
  99. Holmes, L. Role of Abiotic Factors on the Development and Life History of the Black Soldier Fly, Hermetia illucens (L.) (Diptera: Stratiomyidae). 2010. Electronic Theses and Dissertations. 285.. Available online: https://scholar.uwindsor.ca/etd/285 (accessed on 1 September 2022).
  100. Zhang, J.; Huang, L.; He, J.; Tomberlin, J.K.; Li, J.; Lei, C.; Sun, M.; Liu, Z.; Yu, Z. An artificial light source influences mating and oviposition of black soldier flies, Hermetia illucens. J. Insect Sci. 2010, 10, 202. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  101. Cheng, J.Y.; Chiu, S.L.; Lo, I.M. Effects of moisture content of food waste on residue separation, larval growth and larval survival in black soldier fly bioconversion. Waste Manag. 2017, 67, 315–323. [Google Scholar] [CrossRef]
  102. Meneguz, M.; Gasco, L.; Tomberlin, J.K. Impact of pH and feeding system on black soldier fly (Hermetia illucens, L; Diptera: Stratiomyidae) larval development. PLoS ONE 2018, 13, e0202591. [Google Scholar] [CrossRef] [PubMed]
  103. Ma, J.; Lei, Y.; Rehman, K.u.; Yu, Z.; Zhang, J.; Li, W.; Li, Q.; Tomberlin, J.K.; Zheng, L. Dynamic effects of initial pH of substrate on biological growth and metamorphosis of black soldier fly (Diptera: Stratiomyidae). Environ. Entomol. 2018, 47, 159–165. [Google Scholar] [CrossRef]
  104. Maurer, V.; Holinger, M.; Amsler, Z.; Früh, B.; Wohlfahrt, J.; Stamer, A.; Leiber, F. Replacement of soybean cake by Hermetia illucens meal in diets for layers. J. Insects Food Feed 2016, 2, 83–90. [Google Scholar] [CrossRef]
  105. Murawska, D.; Daszkiewicz, T.; Sobotka, W.; Gesek, M.; Witkowska, D.; Matusevičius, P.; Bakuła, T. Partial and Total Replacement of Soybean Meal with Full-Fat Black Soldier Fly (Hermetia illucens L.) Larvae Meal in Broiler Chicken Diets: Impact on Growth Performance, Carcass Quality and Meat Quality. Animals 2021, 11, 2715. [Google Scholar] [CrossRef] [PubMed]
  106. Dabbou, S.; Gai, F.; Biasato, I.; Capucchio, M.T.; Biasibetti, E.; Dezzutto, D.; Meneguz, M.; Plachà, I.; Gasco, L.; Schiavone, A. Black soldier fly defatted meal as a dietary protein source for broiler chickens: Effects on growth performance, blood traits, gut morphology and histological features. J. Anim. Sci. Biotechnol. 2018, 9, 49. [Google Scholar] [CrossRef]
  107. Kawasaki, K.; Hashimoto, Y.; Hori, A.; Kawasaki, T.; Hirayasu, H.; Iwase, S.-i.; Hashizume, A.; Ido, A.; Miura, C.; Miura, T.; et al. Evaluation of Black Soldier Fly (Hermetia illucens) Larvae and Pre-Pupae Raised on Household Organic Waste, as Potential Ingredients for Poultry Feed. Animals 2019, 9, 98. [Google Scholar] [CrossRef]
  108. Bellezza Oddon, S.; Biasato, I.; Imarisio, A.; Pipan, M.; Dekleva, D.; Colombino, E.; Capucchio, M.T.; Meneguz, M.; Bergagna, S.; Barbero, R. Black Soldier Fly and Yellow Mealworm live larvae for broiler chickens: Effects on bird performance and health status. J. Anim. Physiol. Anim. Nutr. 2021, 105, 10–18. [Google Scholar] [CrossRef]
  109. Gariglio, M.; Dabbou, S.; Crispo, M.; Biasato, I.; Gai, F.; Gasco, L.; Piacente, F.; Odetti, P.; Bergagna, S.; Plachà, I. Effects of the dietary inclusion of partially defatted black soldier fly (Hermetia illucens) meal on the blood chemistry and tissue (Spleen, Liver, Thymus, and Bursa of Fabricius) histology of muscovy ducks (Cairina moschata domestica). Animals 2019, 9, 307. [Google Scholar] [CrossRef]
  110. Gariglio, M.; Dabbou, S.; Gai, F.; Trocino, A.; Xiccato, G.; Holodova, M.; Gresakova, L.; Nery, J.; Oddon, S.B.; Biasato, I. Black soldier fly larva in Muscovy duck diets: Effects on duck growth, carcass property, and meat quality. Poult. Sci. 2021, 100, 101303. [Google Scholar] [CrossRef]
  111. Loponte, R.; Nizza, S.; Bovera, F.; De Riu, N.; Fliegerova, K.; Lombardi, P.; Vassalotti, G.; Mastellone, V.; Nizza, A.; Moniello, G. Growth performance, blood profiles and carcass traits of Barbary partridge (Alectoris barbara) fed two different insect larvae meals (Tenebrio molitor and Hermetia illucens). Res. Vet. Sci. 2017, 115, 183–188. [Google Scholar] [CrossRef]
  112. Marono, S.; Loponte, R.; Lombardi, P.; Vassalotti, G.; Pero, M.; Russo, F.; Gasco, L.; Parisi, G.; Piccolo, G.; Nizza, S. Productive performance and blood profiles of laying hens fed Hermetia illucens larvae meal as total replacement of soybean meal from 24 to 45 weeks of age. Poult. Sci. 2017, 96, 1783–1790. [Google Scholar] [CrossRef]
  113. Cullere, M.; Schiavone, A.; Dabbou, S.; Gasco, L.; Dalle Zotte, A. Meat quality and sensory traits of finisher broiler chickens fed with black soldier fly (Hermetia illucens L.) larvae fat as alternative fat source. Animals 2019, 9, 140. [Google Scholar] [CrossRef]
  114. Moula, N.; Scippo, M.-L.; Douny, C.; Degand, G.; Dawans, E.; Cabaraux, J.-F.; Hornick, J.-L.; Medigo, R.C.; Leroy, P.; Francis, F. Performances of local poultry breed fed black soldier fly larvae reared on horse manure. Anim. Nutr. 2018, 4, 73–78. [Google Scholar] [CrossRef]
  115. Schiavone, A.; Dabbou, S.; Petracci, M.; Zampiga, M.; Sirri, F.; Biasato, I.; Gai, F.; Gasco, L. Black soldier fly defatted meal as a dietary protein source for broiler chickens: Effects on carcass traits, breast meat quality and safety. Animal 2019, 13, 2397–2405. [Google Scholar] [CrossRef]
  116. Cullere, M.; Tasoniero, G.; Giaccone, V.; Acuti, G.; Marangon, A.; Dalle Zotte, A. Black soldier fly as dietary protein source for broiler quails: Meat proximate composition, fatty acid and amino acid profile, oxidative status and sensory traits. Animal 2018, 12, 640–647. [Google Scholar] [CrossRef]
  117. Chia, S.; Tanga, C.; Osuga, I.; Alaru, A.; Mwangi, D.; Githinji, M.; Dubois, T.; Ekesi, S.; Van Loon, J.; Dicke, M. Black soldier fly larval meal in feed enhances growth performance, carcass yield and meat quality of finishing pigs. J. Insects Food Feed 2021, 7, 433–447. [Google Scholar] [CrossRef]
  118. Driemeyer, H. Evaluation of Black Soldier Fly (Hermetia illucens) Larvae as an Alternative Protein Source in Pig Creep Diets in Relation to Production, Blood and Manure Microbiology Parameters. Ph.D. Thesis, Stellenbosch University, Stellenbosch, South Africa, 2016. [Google Scholar]
  119. Biasato, I.; Renna, M.; Gai, F.; Dabbou, S.; Meneguz, M.; Perona, G.; Martinez, S.; Lajusticia, A.C.B.; Bergagna, S.; Sardi, L. Partially defatted black soldier fly larva meal inclusion in piglet diets: Effects on the growth performance, nutrient digestibility, blood profile, gut morphology and histological features. J. Anim. Sci. Biotechnol. 2019, 10, 12. [Google Scholar] [CrossRef] [PubMed]
  120. Ipema, A.F.; Gerrits, W.J.; Bokkers, E.A.; Kemp, B.; Bolhuis, J.E. Live black soldier fly larvae (Hermetia illucens) provisioning is a promising environmental enrichment for pigs as indicated by feed-and enrichment-preference tests. Appl. Anim. Behav. Sci. 2021, 244, 105481. [Google Scholar] [CrossRef]
  121. Yu, M.; Li, Z.; Chen, W.; Rong, T.; Wang, G.; Ma, X. Hermetia illucens larvae as a potential dietary protein source altered the microbiota and modulated mucosal immune status in the colon of finishing pigs. J. Anim. Sci. Biotechnol. 2019, 10, 50. [Google Scholar] [CrossRef] [Green Version]
  122. Altmann, B.A.; Neumann, C.; Rothstein, S.; Liebert, F.; Mörlein, D. Do dietary soy alternatives lead to pork quality improvements or drawbacks? A look into micro-alga and insect protein in swine diets. Meat Sci. 2019, 153, 26–34. [Google Scholar] [CrossRef]
  123. Wang, Y.-S.; Shelomi, M. Review of black soldier fly (Hermetia illucens) as animal feed and human food. Foods 2017, 6, 91. [Google Scholar] [CrossRef] [PubMed]
  124. Rehman, K.u.; Hollah, C.; Wiesotzki, K.; Rehman, R.U.; Rehman, A.U.; Zhang, J.; Zheng, L.; Nienaber, T.; Heinz, V.; Aganovic, K. Black soldier fly, Hermetia illucens as a potential innovative and environmentally friendly tool for organic waste management: A mini-review. Waste Manag. Res. 2022, 0734242X221105441. [Google Scholar] [CrossRef]
  125. Valdés, F.; Villanueva, V.; Durán, E.; Campos, F.; Avendaño, C.; Sánchez, M.; Domingoz-Araujo, C.; Valenzuela, C. Insects as Feed for Companion and Exotic Pets: A Current Trend. Animals 2022, 12, 1450. [Google Scholar] [CrossRef]
  126. Żuk-Gołaszewska, K.; Gałęcki, R.; Obremski, K.; Smetana, S.; Figiel, S.; Gołaszewski, J. Edible Insect Farming in the Context of the EU Regulations and Marketing—An Overview. Insects 2022, 13, 446. [Google Scholar] [CrossRef]
  127. Veldkamp, T.; Meijer, N.; Alleweldt, F.; Deruytter, D.; Van Campenhout, L.; Gasco, L.; Roos, N.; Smetana, S.; Fernandes, A.; van der Fels-Klerx, H. Overcoming Technical and Market Barriers to Enable Sustainable Large-Scale Production and Consumption of Insect Proteins in Europe: A SUSINCHAIN Perspective. Insects 2022, 13, 281. [Google Scholar] [CrossRef]
  128. Ribeiro, J.C.; Gonçalves, A.T.S.; Moura, A.P.; Varela, P.; Cunha, L.M. Insects as food and feed in Portugal and Norway–cross-cultural comparison of determinants of acceptance. Food Qual. Prefer. 2022, 102, 104650. [Google Scholar] [CrossRef]
  129. Sogari, G.; Menozzi, D.; Mora, C.; Gariglio, M.; Gasco, L.; Schiavone, A. How information affects consumers’ purchase intention and willingness to pay for poultry farmed with insect-based meal and live insects. J. Insects Food Feed 2022, 8, 197–206. [Google Scholar] [CrossRef]
  130. Chung, A.Y.C.; Khen, C.; Unchi, S.; Binti, M. Edible insects and entomophagy in Sabah, Malaysia. Malay. Nat. J. 2002, 56, 131–144. [Google Scholar]
  131. Purba, R.A.P.; Paengkoum, P.; Paengkoum, S. The links between supplementary tannin levels and conjugated linoleic acid (CLA) formation in ruminants: A systematic review and meta-analysis. PLoS ONE 2020, 15, e0216187. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  132. Olutegbe, N.S.; Ojuoluwa, O. Overcoming Social Barrier to Adoption of Black Soldier Fly (Hermetia illucens) as a Protein Source for Poultry: How Tall Is the Order? Chem. Proc. 2022, 10, 73. [Google Scholar]
Table
Table 1. Regular nutrition facts of BSFL (g kg−1 dry matter basis).
Table 1. Regular nutrition facts of BSFL (g kg−1 dry matter basis).
BSFLCSBMFM
TypeFFDFDFFFFFFFFFFFDF
Crude protein431.0655.0216.0411.0439.0350.0401.0275.4554.2494.4675.3
Crude fat386.046.063.0301.0294.0298.0325.0515.398.514.0103.6
Crude fiber41.0 70.0 213.079.0 74.074.32.6
Ash27.093.093.093.0132.053.0104.065.981.071.9171.5
Chitin67.069.0 38.772.1
References[23][18][65][74][68][75][76][69][69][67][67]
CSBM = conventional soybean meal, FM = fish meal, FF = full-fat, DF = defatted.
Table
Table 2. Amino acid composition of BSFL (g kg−1 dry matter basis).
Table 2. Amino acid composition of BSFL (g kg−1 dry matter basis).
BSFLCSBMFM
Indispensable amino acids
TypeFFDFFFFFFFFFFF
Arginine19.920.721.154.762.021.918.735.741.0
Histidine13.816.313.532.548.09.813.714.215.4
Isoleucine19.124.017.747.348.019.120.622.127.3
Leucine30.636.727.878.377.032.129.438.647.7
Lysine23.025.228.168.274.027.225.931.148.7
Methionine7.18.568.021.26.06.07.1.6.818.5
Phenylalanine16.421.816.477.662.018.318.725.526.4
Threonine16.221.816.344.345.026.516.719.827.5
Tryptophan5.4 5.66.36.66.7
Valine28.234.525.067.967.028.728.821.732.7
Dispensable amino acids
Alanine27.843.725.682.162.0 26.621.641.9
Aspartic acid36.948.838.773.0103.0 35.655.057.7
Cysteine2.20.23.57.65.04.23.27.76.5
Glycine25.230.324.661.554.026.824.821.350.3
Glutamic acid45.863.746.1131.0102.0 38.488.684.1
Proline25.132.723.666.862.0 23.127.430.8
Serine15.926.817.648.841.019.215.224.125.9
Tyrosine 34.1 67.160.026.526.915.520.1
References[23][18][68][75][78][79][80][67][67]
CSBM = conventional soybean meal, DF = defatted, FM = fish meal, FF = full fat.
Table
Table 3. Fatty acid composition of BSFL (g kg−1 dry matter basis).
Table 3. Fatty acid composition of BSFL (g kg−1 dry matter basis).
TypeFFFFFFFFFFFF
C10:020.3 8.614.3 8.6
C12:0575.675.0459.7526468.6407.9
C14:071.423.08785.498.765.6
C15:0 1.5 143.81.3
C16:010.3192.0122.1109143.8162.7
C18:09.869.025.315.317.914.3
SFA782.9362.0707.2750.0742.4664.2
C16:133.48.019.119.827.823.6
c9C18:179.7266.0112.461.677.3182.4
c11C18:11.2 2.4
MUFA119.9287.0134.185.5115.8218.8
C18:2n-678.3314.038.0116.0127.7100.7
n-6 PUFA80.0314.0142.2119.0106.0100.9
C18:3n-311.036.016.510.19.816.0
C18:4n-30.5
C20:5n-32.3 0.2
C22:6n-30.1
n-3 PUFA14.336.016.510.19.816.2
MUFA /SFA, % 15.379.318.911.415.632.9
n-3 PUFA/ n-6 PUFA, %17.911.511.68.59.016.1
References[23][81] [82][75][83][84]
DF = defatted, FF = full fat, MUFA = monounsaturated fatty acid, PUFA = polyunsaturated fatty acids, SFA = saturated fatty acid.
Table
Table 4. Mineral compositions of BSFL (g kg−1 dry matter basis).
Table 4. Mineral compositions of BSFL (g kg−1 dry matter basis).
TypeFFDFFFFFFF
Calcium (Ca)1.213.01.9.034.635.7
Copper (Cu)0.115.00.610.70.7
Iron (Fe)0.1125.02.1191.014.0
Magnesium (Mg)2.13.01.03.53.4
Manganese (Mn)0.245.00.3166.033.5
Phosphorus (P)4.18.01.010.37.0
Potassium (K)6.011.01.715.49.2
Sodium (Na)0.75.03.31.715.6
Zinc (Zn)0.790.00.9103.09.0
References[23][65][74][79][87]
DF = defatted, FF = full fat.
Table
Table 5. Effects of BSFL on the growth performance of poultry.
Table 5. Effects of BSFL on the growth performance of poultry.
ReferencesBreedTypeLevel, %AgePerformance
[104]Lohmann Selected LeghornDF50, 100128 daysNo difference in feed intake, egg production, yolk and shell weight.
No mortality occurred.
[107]Laying HensFF10168 daysNo difference in feed intake, BW, liver weight, and the egg-laying rate.
No difference in egg yolk weight, egg shell weight, egg shell strength, and Haugh unit.
Increases the richness of cecal microbiota.
[106]Ross 308DF5, 10, 151–35 daysNo difference in FCR (days 1–10).
Increases the LW, ADG, DFI and FCR (days 10–35).
[31]Ross 308FF50, 10021–48 daysNo difference in DWG, DFI and FCR.
No difference in LW, chilled carcass, breast, thighs, abdominal fat, liver, heart and spleen.
[68]Cobb 500FF5, 10, 151–79 daysNo difference in final weight, DFI and FCR (days 7–28).
Increases the final weight (days 28–79).
No effects on breast meat weight, abdominal fat content, and internal organ (liver, heart, gizzard, and spleen) weights.
[108]Ross 308FF51–39 daysNo difference in final weight DFI and FCR.
No difference in slaughtering performance.
[105]Ross 308FF50, 75, 1001–42 daysReduces the LW of the whole stage. Decreased ADG (days 1–14, days 14–35).
Reduces DFI and FCR in the 100% groups.
Reduces carcass weight and muscle weight.
Increases abdominal fat deposits.
Increases carcass fat content and the proportion of viscera to the total weight.
[109]R71 LFF3, 6, 93–50 daysNo difference in LW, ADG, DFI and FCR.
Reduces mortality (from 4.16% to 2.08%).
[110]Canedins R71 L WhiteDF3, 6, 93–50 daysNo difference in LW, ADG, DFI and FCR.
SW, and consequently the HC and CC weights, and abdominal fat showed a quadratic response with the minimum corresponding to the 6% group.
ADG = average daily gain, BW = body weight, CC = chilled carcass, DF = defatted, DFI = daily feed intake, DWG = daily weight gain, FCR = feed conversion ratio, FF = full-fat, HC = hot carcass, LW = live weight, SW = slaughter weight.
Table
Table 6. Effects of BSFL on the antioxidants and immunity of poultry.
Table 6. Effects of BSFL on the antioxidants and immunity of poultry.
ReferencesBreedTypeLevel, %AgePerformance
[106]Ross 308DF5, 10, 151–35 daysNo difference in erythrocyte, AST, creatinine, triglycerides, cholesterol, H/L, leukocyte, and uric acid.
Increases the activity of GPx and TAS.
[31]Ross 308FF50, 10021–48 daysNo difference in GGT, H/L, ALT, AST, cholesterol, creatinine, erythrocyte, iron, leukocyte, magnesium, phosphorus, total protein, triglycerides, and uric acid.
[108]Ross 308FF51–39 daysNo difference in erythrocyte, ALT, uric acid, Albumin, AST, cholesterol, creatinine. GGT, H/L, HDL, LDL, leukocyte, total protein and triglycerides.
[109]R71 L WhiteFF3, 6, 93–50 daysNo difference in erythrocyte, heterophils, lymphocytes, basophils, eosinophils, H/L, leukocyte, monocytes, and total protein.
No difference in AST, ALT and GGT.
Reduces triglycerides and cholesterol (from 30.23% to 23.86%).
No difference in GPx, TAS and MG.
Reduces MDA and nitrotyrosine.
[112]Lohman Brown Classic laying hensFF10021–45 weeksIncreases cholesterol, globulin and triglycerides.
No difference in erythrocyte, eosinophils, basophils, H/L, heterophils, leukocyte, lymphocytes, monocytes and total protein. Reduces albumin.
[111]Alectoris barbaraFF25, 507–28 daysReduces albumin and BUN.
No difference in erythrocyte, AST, ALT, total protein and H/L.
[109]Canedins R71 L WhiteDF3, 6, 93–50 daysNo difference in AST, ALT and GGT.
No difference in GPx, TAS and MG.
Reduces MDA.
ALT = alanine aminotransferase, AST = aspartate amino transferase, BUN = blood urea nitrogen, BW = body weight, DF = defatted, FF = full-fat, GGT = gamma-glutamyl transferase, GPx = glutathione peroxidase, H/ L = heterophiles to lymphocytes ratio, HDL = high-density lipoproteins, LDL = low-density lipoproteins, MDA = malondialdehyde, MG = methylglyoxal, TAS = total antioxidant status.
Table
Table 7. Effects of BSFL on the meat quality and nutritional content of poultry.
Table 7. Effects of BSFL on the meat quality and nutritional content of poultry.
ReferencesBreedTypeLevel, %AgePerformance
[113]Ross 708FF50, 10021–48 daysNo difference in moisture, protein, lipids and ash of meat.
No difference in cholesterol and TBARs.
No difference in pH, L*, a*, b*, thawing loss and cooking loss.
Increases the total SFA and n-6/n-3 ratio.
Decreases MUFA, PUFA and n-3 PUFA.
[105]Ross 308FF50, 75, 1001–42 daysIncreases pH, a* and b*.
Reduces cooking losses.
No difference in aroma intensity or desirability.
[114]ArdennaiseFF230–80 daysIncreases total FA (BSF 36.7%, control 33.8%) and C20: 4ω6.
No difference in ω6/ω3 ratio.
No difference in the protein content of meat (control 24%, BSF 26%).
[116]QuailsFF10, 1510–28 daysIncreases alanine, serine, aspartic acid, glutamic acid, tyrosine and threonine.
Increases the SFA (C10: 0, C12: 0, C14: 0, C16: 0 and C20: 0) and n-6/n-3 ratio.
Decreases PUFA, especially n-3.
[115]Ross 308FF5, 10, 151–35 daysIncreases a*, protein and the FA/ PUFA ratio.
Reduces b* and moisture.
[110]Canedins R71 L WhiteDF3, 6, 93–50 daysNo difference in pH 24 and the color of the breast and thigh muscles.
Increases C12: 0, C14: 0 and α- linolenic acid.
No difference in SFA brisket.
Decreases C18:3 n-3, the lowest in the 9% group, the ratio of ∑n-6/∑n-3 decreases linearly.
a* = red/green value, b* = blue/yellow value, DF = defatted, FA = fatty acid, FF = full fat, L* = lightness, MUFA = monounsaturated fatty acid, PUFA = polyunsaturated fatty acids, SFA = saturated fatty acid, TBARs = thiobarbituric acid reactant. ∑n-6/∑ n-3 = ∑PUFA n-6/∑PUFA n-3 ratio.
Table
Table 8. Effects of BSFL on the growth performance of swine.
Table 8. Effects of BSFL on the growth performance of swine.
ReferencesPhaseTypeLevel, %AgePerformance
[117]Weaning swineFF25, 50, 75, 10014 weeksIncreases ADG, FBW, fasted weight and carcass weight.
Reduces FCR.
[118]Weaned pigletsFF3.510–28 daysNo difference in ADG, DMI and digestibility.
[77]Weaned pigletsFF25, 507–21 daysIncreases body weight at day 7.
Reduces ADFI and G: F at days 14–21.
[119]Weaned pigletsDF5, 101–61 daysNo difference in ADG, ADFI, BW, WG and FCR.
[120]Weaned pigletsFFD 21-25, 75g/day, D 25-35, 150g/day24–35 daysNo difference in ADG, final body weight, feed efficiency and energy efficiency.
[121]Fattening pigFF4, 8Initial weight 76 kg, raised for 46 days.Increased the abundance of lactobacillus, pseudo-butyric vibrio, Rosella, and faecalibacterium of the 4% group.
Decreased the abundance of streptococcus.
Increased the number of Clostridium cluster XIVa of the 8% group.
ADFI = average daily feed intake, ADG = average daily gain, BW = body weight, D = days, DMI = dry matter intake, FBW = final body weight, FCR = feed conversion ratio, G: F = gain: feed, WG = weight gain.
Table
Table 9. Effects of BSFL on the antioxidant, immunity, and meat quality of swine.
Table 9. Effects of BSFL on the antioxidant, immunity, and meat quality of swine.
ReferencesPhaseTypeLevel, %AgePerformance
[119]Weaned pigletsDF5, 101–61 daysNo difference in white blood cells, lymphocytes, monocytes, neutrophils, eosinophils, basophils, red blood cells, MCV, hematocrit, MCH, GOT, GPT, ALP, total protein, and triglycerides.
No difference in albumin, alpha globulin, beta globulin, beta globulin and gamma globulin.
[122]Fattening pigFF50, 75, 10022–75 kgReduced back fat (L*) and all physicochemical parameters were not affected.
Increases the PUFA, GLA and C18:2; C12:0 was five times higher.
[117]Weaning swineDF25, 50, 75, 10014 weeksIncreases protein, lipids and OM of meat.
No difference in moisture.
ALP = alkaline phosphatase, GLA = gamma linolenic acid, GOT = glutamic oxaloacetic transaminase, GPT = glutamate-pyruvate transaminase, L* = lightness, MCH = mean corpuscular hemoglobin, MCV = mean corpuscular volume, OM = organic matter, PUFA = polyunsaturated fatty acids.
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Lu, S.; Taethaisong, N.; Meethip, W.; Surakhunthod, J.; Sinpru, B.; Sroichak, T.; Archa, P.; Thongpea, S.; Paengkoum, S.; Purba, R.A.P.; et al. Nutritional Composition of Black Soldier Fly Larvae (Hermetia illucens L.) and Its Potential Uses as Alternative Protein Sources in Animal Diets: A Review. Insects 2022, 13, 831. https://doi.org/10.3390/insects13090831

AMA Style

Lu S, Taethaisong N, Meethip W, Surakhunthod J, Sinpru B, Sroichak T, Archa P, Thongpea S, Paengkoum S, Purba RAP, et al. Nutritional Composition of Black Soldier Fly Larvae (Hermetia illucens L.) and Its Potential Uses as Alternative Protein Sources in Animal Diets: A Review. Insects. 2022; 13(9):831. https://doi.org/10.3390/insects13090831

Chicago/Turabian Style

Lu, Shengyong, Nittaya Taethaisong, Weerada Meethip, Jariya Surakhunthod, Boontum Sinpru, Thakun Sroichak, Pawinee Archa, Sorasak Thongpea, Siwaporn Paengkoum, Rayudika Aprilia Patindra Purba, and et al. 2022. "Nutritional Composition of Black Soldier Fly Larvae (Hermetia illucens L.) and Its Potential Uses as Alternative Protein Sources in Animal Diets: A Review" Insects 13, no. 9: 831. https://doi.org/10.3390/insects13090831

APA Style

Lu, S., Taethaisong, N., Meethip, W., Surakhunthod, J., Sinpru, B., Sroichak, T., Archa, P., Thongpea, S., Paengkoum, S., Purba, R. A. P., & Paengkoum, P. (2022). Nutritional Composition of Black Soldier Fly Larvae (Hermetia illucens L.) and Its Potential Uses as Alternative Protein Sources in Animal Diets: A Review. Insects, 13(9), 831. https://doi.org/10.3390/insects13090831

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