Human Consumption of Insects in Sub-Saharan Africa: Comparison
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Please note this is a comparison between Version 2 by Jason Zhu and Version 1 by Rudy Caparros Megido.

There are 472 edible insect species in sub-Saharan Africa, of which 31% are Lepidoptera. Wild harvesting is still the main source of supply for these prized species to this day, with some harvesting techniques negatively impacting the environment. The successful production of edible caterpillars requires the appropriate and efficient implementation of husbandry techniques and practices.

  • entomophagy
  • insect food
  • edible caterpillars
  • insect industry

1. Introduction

By 2050, the world’s population is predicted to exceed 9 billion, which would further aggravate the problems of food security in developing countries. To feed this growing population, food production must increase by nearly 70% and, if possible, double in developing countries. This is because demographic growth in these countries will be coupled with increasing urbanization, and a rise in the middle classes [1]. In a context of increasing scarcity of natural resources and agricultural land, the use of alternative and ecologically sustainable protein sources, including insects (e.g., Tenebrio molitor), algae (e.g., Arthrospira platensis), and edible mushrooms (e.g., Psathyrella tuberculate), seems to be vital to facilitate an increase in world food production [2,3,4,5][2][3][4][5]. The Food and Agriculture Organization of the United Nations has identified edible insects as one key solution to food insecurity [6].
From a nutritional perspective, insects are not inferior to other protein sources, such as fish, chicken, and beef [7]. In parallel, insect production is considered more sustainable compared to domestic animals, because insects have a high food conversion efficiency, excellent potential (for some species) to be raised using organic by-products [8,9,10][8][9][10], high fecundity, and short development cycles [11]. Edible insects also require less space and water in the process of mass production [12,13,14,15][12][13][14][15]. For example, one gram of edible protein from beef requires eight to 14 times more land and about five times more water than mealworms [16]. Other more advanced arguments in favor of insects include the fact that they are a rich source of antioxidants and are beneficial for the intestinal microbiota of humans [17,18,19][17][18][19].
In addition to being a nutritious food for some families in developing countries, the exploitation of these non-timber forest products (NTFPs) offers employment opportunities and additional income to people that actively collect, produce, process, and market insects [20]. In developing countries, these edible insects are generally collected in the wild using a wide variety of collection methods depending on the behavior of the targeted insects, as well as the cultures and countries. Methods range from simple hand-picking to the use of specific tools (e.g., glue, sticks, nets, and baskets) [7,21][7][21]

2. Life Cycle of Lepidoptera

Published literature documenting the developmental cycle of tropical Lepidoptera remains limited. Most species widely consumed in Africa produce a single generation per year (e.g., C. forda). This phenomenon is thought to be regulated by abiotic factors, such as photoperiod, temperature and host plant availability, which mainly affect pupation [32][22]. However, species such as the caterpillars Imbrasia belina, Bunea alcinoe and the African moths Gonimbrasia zambesina, Gonimbrasia krucki, Gonimbrasia cocaulti, and Gynanisa nigra can complete two cycles in one-year while others, such as the Eri silkworm complete several cycles in a single year [30,33,34,35][23][24][25][26].

3. Nutritional Composition of Edible Caterpillars

Insects are an alternative food source that has a high content of essential nutrients (proteins, lipids, and minerals) for humans and animals [43][27]. Malaisse [44][28] provides a detailed overview of the nutritional values of some edible caterpillars from sub-Saharan Africa, confirming the empirical knowledge of local populations. The nutritional analysis of 24 species of dried edible caterpillars allowed uresearchers to determine the average proportion of proteins (63.5%), lipids (15.7%), and energy value (457 kcal/100 g) contained in these insects on a dry matter basis [22,45][29][30]. These data revealed clear variations in nutritional composition of different edible caterpillars. This variation is associated with species, stage of development, biotope, diet, method of preparation (e.g., roasted or boiled caterpillars), and analytical method used (Table 3, [46,47][31][32]). Edible caterpillars have higher protein levels (28 g/100 g on a fresh matter basis) compared to chicken meat (21 g/100 g of fresh matter protein). The energy intake of caterpillars (370 kcal/100 g) is similar to pork (416 kcal/100 g) [10]. Although a 100 g portion of insects is not enough to ensure the daily vitamin needs for humans (e.g., A and C), they also contribute different vitamins (depending on species) (e.g., thiamine/B1, riboflavine/B2, pyridoxine/B6, pantothenic acid, niacin) and minerals (e.g., K, Ca, Mg, Zn, P, Fe). Their bioavailability provides a means of combating malnutrition in Africa and preventing metabolic diseases [4,22,48,49,50,51,52][4][29][33][34][35][36][37]. Because of their high nutritional value, caterpillars are sometimes mixed with flour to prepare a porridge at breakfast to combat malnutrition in children, frail people, and pregnant women [4,45,53,54][4][30][38][39]. Proteins are major nutritional components of insects, providing essential and non-essential amino acids to the human body [43,55][27][40]. The digestibility of insect proteins is comparable to that of casein or soy proteins (77–98%) [43][27]. Some studies have reported that the digestibility of the moth Clanis bilineata was 95.8% compared to casein [51][36]. Oibiokpa et al. [48][33] also showed that the moth C. forda has a higher biological value (86.90%) compared to casein (73.45%). However, the digestibility of insect proteins could be improved by eliminating the rigid chitin-rich exoskeleton, which reduces the digestibility of their crude proteins, despite the presence of two chitinases in the human stomach [48,63,64][33][41][42]. Chemical methods can be used to remove the exoskeleton, whereby strong acids and bases are used to dissolve calcium carbonates and proteins, respectively [65][43]. For example, chitin removal by alkaline extraction increases the digestibility of bee protein from 71.5% to 94.3% [63][41]. The quality of proteins depends on the amino acid composition [66][44], with insects being particularly rich in lysine and threonine, but sometimes deficient in methionine and cysteine [67][45]. However, some amino acids could be limiting depending on insect species ([49,68][34][46]). Many amino acid sequences have been identified in a wide range of dietary proteins that are generally considered to be sources of bioactive peptides (BAPs), such as the tripeptides valine-proline-proline (VPP) and isoleucine-proline-proline (IPP), and the polypeptides phenylalanine-phenylalanine-valine-alanine-proline- phenylalanine-proline-glutamate-valine-phenylalanineglycine-lysine (FFVAPFPEVFGK) and tyrosine-leucine-glycine-tyrosine-leucine-glutamate-glutamine-leucinearginine (YLGYLEQLLR) [69,70][47][48]. These BAPs might have biological functions and hypotensive, antioxidant, antidiabetic, immunomodulatory or mineral-binding properties [69,70][47][48]. Among known edible insect species, the biofunctional properties of proteins and peptides from B. mori have been extensively studied. For example, analysis of angiotensin converting enzyme (ACE) revealed the existence of angiotensin I converting enzyme (ACE) inhibitory peptides that reduce blood pressure. For example, peptides identified in the protein of B. mori pupae include tripeptides (KHV and ASL) and the pentapeptide GNPWM [71,72,73][49][50][51]. Reference protein intake for health adults is estimated to be 0.83 g protein/kg body weight per day (i.e., 62.3 g for a 75 kg adult). Fogang et al. [74][52] reported that the consumption of a 100 g portion of Imbrasia truncata or Imbrasia epimethea caterpillars covered 30.6% and 32.3% of the required protein intake of a 75 kg adult, respectively. Lipids are the most energy-dense group of macronutrients [2]. They store and provide energy, and support and protect the various organs [83][53]. They are made up of triglycerides, each with a glycerol molecule and three fatty acids that are saturated or unsaturated [2]. Caterpillars are among the most fat-rich insects [84][54]. Like other edible insects, edible caterpillars are a source of fatty acids [45][30], with most caterpillars being rich in mono- and, even, polyunsaturated fatty acids (PUFA) [85][55]. These fatty acids are mainly linolenic (C18:3n3) and linoleic (C18:2n6) acids, commonly known as omega-3 and omega-6 fatty acids, respectively [85][55]. These PUFAs are not synthesized by the human body, and must be obtained through the diet [65][43]. Therefore, the ingested amounts and balanced proportions of these fatty acids should be provided sufficiently, as unbalanced ratios are often associated with health problems in humans, such as coronary heart disease, cancer, and autoimmune and inflammatory diseases [86][56]. The diets of people living in developing countries are generally characterized by micronutrient deficiencies, resulting in major health consequences [7]. Interestingly, the micronutrient content of edible insects is influenced by their diet [91][57]. Importantly, the consumption of edible insects would provide significant amounts of minerals that are sufficient to meet human needs. Examples include copper (e.g., Usta terpsichore, mealworm adult), iron, and zinc (e.g., B. mori), as well as vitamins (carotene and vitamins B1, B2, B6, D, E, K, and C) [51][36]. Certain minerals (such as iron and zinc) are of particular interest, because they are often the source of deficiencies in developing countries [7,11][7][11]. Fe and Zn deficiency is particularly prevalent in regions with high cereal and low animal food consumption. In fact, both Fe and Zn help prevent malnutrition and early stunting [92][58]. Mwangi et al. [92][58] compared the Fe and Zn content in meat from conventionally raised animals (8 mg/100 g Fe and 21 mg/100 g Zn beef, 4 mg/100 g Fe and 6 mg/100 g Zn pork, and 3 mg/100 g Fe and 6 mg/100 g chicken) against three edible insect species (6 mg/100 g Fe and 13 mg/100 g Zn T. molitor, 14 mg/100 g Fe and 21 mg/100 g Zn Acheta domesticus, and 19 mg/100 g Fe and 15 mg/100 g Zn L. migratoria). The reseauthorchers showed that edible insects contained Fe and Zn levels similar to, or higher than, those of conventional farm animals [92][58]. Of note, mineral content varies according to insect species, stage of development, and diet [7,43][7][27]. Better control of food intake would enable easy modification of insect mineral content [11].

4. Availability, Host Plants, Harvesting, and Storage

Availability and Relationship of Lepidoptera with Host Plant(s)

The seasonal availability of edible caterpillars varies with region and reflects variation in climatic conditions [16,22,30][16][23][29]. In the Central African Republic (CAR), caterpillars are available from mid-June to late September [20], whereas they are available from July to October in Cameroon and from August to January in Congo-Brazzaville. In the Democratic Republic of Congo (DRC), edible caterpillars are available between July and September in the western Kasai region, between June and September in the Kisangani region [20], and from September to December in the Bandundu region [20]. This seasonality is related to the presence of plants on which caterpillar feed at the beginning of the rainy season, because caterpillars specifically feed on one or more host plants that only grow in certain ecosystems [30,94][23][59]. Several studies have provided information on the host plants of edible caterpillars in tropical Africa [27,94,95,96,97,98][59][60][61][62][63][64]. These studies show that edible caterpillars are generally polyphagous, associating with several host plants. For example, the caterpillar C. forda feeds on Vitellaria paradoxa (Sapotaceae) in West Africa, Autranella congoensis in CAR, and Burkea africana in South Africa. In the DRC, these caterpillars are associated with Crossopteryx febrifuga in Bas-Congo, E. suaveolens in the Kisangani-Tshopo region, Erythrophleum africanum in Bandundu, and Albizia antunesiana in Katanga [99][65]. Of note, the abundance and availability of edible caterpillars is sometimes affected by the felling of host plants. For example, the woody plants, Sapelli (Entandrophragma cylindricum) and Tali (Erythrophleum suaveolens) are both widely harvested for timber and edible caterpillars (I. oyemensis and C. forda, respectively). Consequently, conflict has risen between one-time timber harvests and the annual harvests of edible caterpillars spanning decades [105][66]. Forest management approaches should support the production of these wood and non-wood resources to benefit multiple stakeholders in these forests. This would minimize potential conflicts between logging and the needs of local people who consume these wild foods [105][66]. To improve the management of these resources, it is important to provide information on the yields of edible caterpillars inhabiting timber trees, and how logging affects their availability. For instance Muvatsi et al. [105][66] quantified the density of Sapelli and Tali trees of different size classes within a 10 km radius of four villages in the Kisangani region (DRC) in 2012, along with the annual cutting areas of two logging concessions. Stumps of these two forest species were identified and measured in 21 five-hectare plots around each village and 20 five-hectare plots in each concession. Around the villages and in the concessions, Sapelli were present at densities of 0.048 ± 0.008 harvestable trees (≥80 cm diameter at breast height [dbh]) ha−1 and 0.135 ± 0.019 precommercial trees ha−1. Harvestable Tali trees (≥60 cm dbh) were seven times more abundant with 0.347 ± 0.032 ha−1, while precommercial Tali trees were present at densities of 0.329 ± 0.033 trees ha−1. Based on estimated tree densities, caterpillar yields were estimated for a 15,700-ha semicircle within a 10 km radius of the villages. Depending on the village, yields were estimated at 11.6–34.5 kg yr−1 for I. oyemensis on Sapelli trees, and 65.8–80.9 kg yr−1 for C. forda on Tali trees, averaging 0.74–2.2 kg ha−1 yr−1 and 4.2–5.2 kg ha−1 yr−1 fresh weight, respectively (0.23–0.68 kg ha−1 yr−1 and 1.3–1.6 kg ha−1 yr−1 dry weight, respectively).

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