Insects As a Viable Source of Proteins- a Review

Indian Journal of Entomology 83(2021) Online published Ref. No. e20190 DoI No.: 10.5958/0974-8172.2021.00017.1

INSECTS AS A VIABLE SOURCE OF PROTEINS- A REVIEW

Thirulogasundhar Balakamatchi* and Priya Sethuraman

Department of Food Processing Technology, AMET deemed to be University, Kanathur, Chennai 603112 *Email: [email protected] (corresponding author)

ABSTRACT

This review focuses on how the world population of the future needs more readily accessible and economic proteins- derived from insect meat. It addresses how man can broaden his scope of food sources. Insects can contribute to the demand for cheap and accessible proteins. The review also brings into its ambit the basic entomology of edible insects, the nutritional value of insect proteins, protein derivation methods, and industrial applications along with the rearing of insects. This article serves as a comparative review of conventional meat versus edible insects as sources of proteins and why insect meat has an advantageous edge. Apart from all these, the review article also brings into light a few disadvantages of consuming insect proteins such as the nutritional drawbacks. For the purpose of scientific research and analysis, this review would be neglecting the disgust factor associated with insects among the general population that adhere to conventional protein sources and or plant-based proteins.

Key words: Edible insects, protein, nutritional value, insect farming, sustainable food, entomophagy, entomological feed, futuristic food, insect nutrition, insect livestock

The world is constantly changing and so is the way currently facing a food shortage can benefit from an we live. But one thing has remained a constant from entomological diet (Lupton and Turner, 2018). This is time immemorial- our protein requirement. And for a broad review looking at aspects from the nutritional this protein requirement human beings have been long value of different edible insect species to their dependent on livestock. And with our current day animal incorporation in the livestock industry as an animal feed. husbandry and farming methods we are unable to feed our current day population, let alone be able to feed Edible insects our future population. According to the UN’s report, The most widely consumed edible insect species the world population is estimated to rise to 9.8 billion which have been commercialized are: crickets by 2050 (DESA, 2019), we need alternative sources of (Gryllidae), honeybee (Apis), domesticated silkworm proteins in order to satisfy a hungry population’s protein (Bombycidae), a few caterpillar varieties (Saturniidae), needs. And this alternative source of protein would be and the grubs of a few weevils (Curculionoidea) native derived from insects. The rearing of insect meat does not to the African continent and the larval stage of the only take up lesser space but produces more biological darkling beetle (Tenebrionidae) commonly referred to protein output relative to the amount of feed it consumes as meal worms. A few of the insects such as the African as well. On top of the substantially high protein levels, palm weevil, mopane caterpillar and the yellow meal they also are rich in other nutrients. Insects consume worm are eaten in their larval stages on accounts of relatively lesser amounts of resources and space to their plentiful fat reserve which is known to have a grow and can be easily cultivated in a laboratory or at good taste. The entomoculture of meal worm has been home. These dietary proteins once mass manufactured promoted to an industrial scale in many regions on the can exponentially increase protein availability rates for basis of the grub’s persistence and ability to persist the population- this would lead to a sharp decline in even in harsh conditions. Even when fed only dry and the malnutrition and protein deficiency diseases rates. low in nutritional qualities feed, they can gain a lot of weight in the form of fat and proteins (Ramos-Elorduy This review focuses on the nutritional upsides of and Pino Moreno, 2002). In the case of orthopterans incorporating an entomological diet. It also primarily like cricket, typically only adults are consumed. Their focuses on how insect proteins can suffice the future harvesting is effortless when swarmed. It is worth populations where an acute food shortage is imminent. noting that these are pests of agricultural crops in a lot This review also focuses on how populations that are of countries- wreaking havoc to plants. Due to this they 2 Indian Journal of Entomology 83(2021) Online published Ref. No. e20190 are in many cases vulnerable to harmful insecticides and here is determined by the ability of the biomass to be rise the concerns of them not being safe to eat as they recycled. The larval stages of midges and houseflies might contain pesticides. Also, such organisms are also serve the purpose of live fishing bait and aquatic feed key players in the bio-magnification of toxins. (Awoniyi et al., 2004). The pet food for common amphibian house pets consists of meal worms. The Bombyx mori or the silkworm has been reared by man for a long time - more prominent in Asian countries. Food additives: Insects are a great source of food The natural protein fibre- silk is the fundamental reason additives too. Carmine which is a common natural behind sericulture. Silk was the basis of establishment of colorant that has been used from centuries ago, is the early trades between Asia (China) and the countries obtained from Dactylopius coccus (Van Huis et al., belonging to the Mediterranean region. Silkworm 2013). It yields a dye that is bright red which can rearing plays a major role in the textiles and garments be used for clothes, cosmetics and also food. The economy even today. However, it is worth noting that demand for natural dyes has seen a sharp increase in silk is not the primary product from B. mori- they are the recent times. The lac dye is a water-soluble poly also eaten as food in their larval stages. Apart from hydroxy-anthraquinone pigment which is bright red, it China, they are served as delicacies in Asian countries is commonly sourced from the Kerria lacca- commonly such as Thailand, Vietnam and Japan, the possibility known as the lac insect. The dye can also be used as could extend to other countries in the future as well. a dye fixative for a transitional array of colors. The The (European) honey bee Apis mellifera is one of the spectrum of possible colours range from red, brown to few insects that is fit to be eaten at nearly all stages. even violet. The initial purpose of this lac dye was in Honey bees play a major role in pollination and besides the textile industry but now it is even used in beverage food, they are reared for this purpose all around the industries as well (Raman, 2014; Srivastava et al., worlds. Bee brood extracts are a luxury nourishment in 2013). These dyes find their most common functions Asia (You and Chen, 1999). Some people consume the now in the coatings of fruits and candies (Siddiqui). hive of the honey bee as delicacies high in nutritional Pharmaceuticals: Apart from being consumed value and also as a natural food sweetener (O’dea, just to alleviate hunger of for their nutritional values, 1991). Undoubtedly, honey is a widely used sweetener insects have a vital role in the medical line as well. relished all over the world. But there have been other Their extracts are used in the form of medicines and contesting trends coming up as well now in the field healthcare products. Black soldier flies (Hermetica of entomic sugars. The current trend involves a new illucens) home the industrial enzymes required for the crystalized honey dew structure by the name lerp and production of bio-diesel (Nguyen et al., 2018). The is becoming increasingly famous. Lerp is the secreted exoskeleton of adult insects are primarily composed of by the larvae of psyllids. Apart from being primarily a compound called chitin. Chitin has found to improve composed of monosaccharides and other carbohydrates the immunity in a large number of organisms (Mack which are insoluble in water, lerp is rich in minerals such et al., 2015; Van Dyken and Locksley, 2018). More as phosphorous and potassium (Ernst and Sekhwela, than 3000 antibacterial products have their sources in 1987). Since lerp can be only collected from crops and insects. Antimicrobial peptides are becoming popular plant damaged by psyllids, the rate at which they can be day by day with the advent of numerous researches. produced is restricted and heavily depended on nature Invertebrates are known to produces around 170 (Van Huis et al., 2013; Yen, 2002). defensins out of which the majority can be sources from Economic prospects insects (Józefiak et al., 2016). Livestock feed: Insects that are consumable also The common house fly Musca domestica are great serve as feed for livestock and aquaculture. Poultry sources of AMPs. Lac resin (cited above) has a wide that is insect-fed is more nutritional than grain-fed ones variety of uses in various industries. Besides coating (Hwangbo et al., 2009) Using entomic feed is common food, it is widely used in insulating substances, print in areas where vegetable feed is not economic (Józefiak and adhesion industries (Wang et al., 2016). And et al., 2016) (Veldkamp and Bosch, 2015; Krishnan et besides, it is of great importance to the medicinal al., 2011). The expenses are too much for livestock drugs manufactory with the possibility of production industries to manage with feed that are grain or legume- of anti-obesity and hepatoprotective drugs (Manzoor based. Entomic feed, however, can provide enough et al, 2013). White wax secretions of Ericerus pela nutrition at low expenses. The sustainability of protein or the Chinese wax insect is almost the same in terms Insects as a viable source of proteins- A review 3 Thirulogasundhar Balakamatchi and Priya Sethuraman of functionality to lac resin and has its industrial Nutritional values purpose as tablet coatings (Qin, 1997). The umbuga Insects have an advantageous edge when it comes is an oil derived from the Coridius vidutus or more to nutrition. Their compositional nutrients share commonly known as melon bugs. This special oil is resemblance with those of conventional animal food a vital source of AMPs that have resist the growth of sources (Raubenheimer and Rothman, 2013) bacteria, especially gram-positive strains. It is being used in some African areas already. The common fungi- Amino acids: Entomic food are rich sources of entomic complex of the dried larvae of the silk worm animal proteins at almost all stages of the developmental and white muscardine disease fungus is an ancient cycle. The amount of amino acids present and their Chinese medicine for the bourgeois. There is proof compositional levels are portrayed in Table 1. The crude of it to home multipharmacologic functions ranging protein ration usually ranges from 40 to 75% on non- from anticoagulation, anticonvulsant, hypnogenesis, wet basis, with the mean per each taxonomical order antifungal, hypolipidemic and even anticarcinogenic ranging in-between 33 to 60%. Insect meat is higher in properties. There have been compounds ranging from crude protein content than conventional meat despite the beauvericin, polysaccharides and flavones which make composition of amino acid for both conventional and up the functional components of many allopathic insect meat being similar. When consumed, they can be medicines targeting the respective ailments mentioned a great source of essential amino acids out of which 76 to above (Hu, 1779). Many of the reared insects exhibit 96% of it being digestible by the human body (Belluco potential in allopathic medicines, even including et al., 2015; Verkerk et al., 2007; Lehnert et al., 2016; antioxidants sourced from insects (Atkinson and Israel, Ramos-Elorduy et al., 1997). Some insects do not have 1973). or only contain trace quantities of methionine, cysteine, Table 1. Amino acid content of common edible insects (% in crude protein of dry weight) Name Stage/ Crude Essential Semi-essential Part protein Ile Leu Lys Met Phe Thr Trp Val Arg His Cys Tyr (%) Amino acid 30 59 45 16 23 6 39 15 16 requirement in human nutrition (mg) Common Meat Beef 5.1 8.4 8.4 2.3 4 4 5.7 6.6 2.9 1.4 3.2 Pork 4.9 7.5 7.9 2.5 4.1 5.1 5 6.4 3.2 1.3 3 Chicken Broiler, 4.2 6.9 7.8 2.1 2.5 3.7 4.6 6.4 4.4 3.5 breast Blattodea (cockroach) 68.33 4.57 7.77 7.8 3.13 4.6 4.93 0.97 7.7 7.43 3.13 1.23 8.93 Blatta lateralis Nymph 76 7.7 12 12.8 3.4 7.7 7.9 1.7 12.3 14 5.5 1.4 14.3 Periplaneta Adult 66 3.1 5.6 5 3.6 3.1 3.6 0.6 6.5 5.1 2 2 6.9 americana Periplaneta Adult 63 2.9 5.7 5.6 2.4 3 3.3 0.6 4.3 3.2 1.9 0.3 5.6 australasiae Coleoptera 41.75 5.58 8.13 5.55 1.38 3.68 3.25 0.78 5.9 5.1 2.6 1.13 4.5 Callipogon barbatus Larva 41 5.8 10 5.7 2 4.7 4 0.7 7 5.9 2 2 4.2 (longhorned beetle) Rhynchophorus Larva 33 7.8 5.9 6.4 1.2 3.3 1.4 0.5 5.5 1.1 1.4 phoenicis (African palm weevil) Tenebrio molitor Larva 48 4 6.9 4.9 1.2 3.2 3.6 1 5.9 4.5 2.7 0.6 5.4 (Yellow mealworm beetle) Zophobas morio Larva 45 4.7 9.7 5.2 1.1 3.5 4 0.9 5.2 4.9 3.1 0.8 7 (superworm) Diptera 48.8 3.74 6.48 5.74 2 4.76 3.98 1.43 5.12 5.05 2.38 0.83 5.52 Copestylum anna Larva 37 4 7.4 5.5 1.9 5.4 4.9 0.7 6.1 6.3 2.9 1.8 6.6 (hover fly) Ephydra hians Larva 42 4 7.4 5.5 1.9 5.4 4.9 0.7 6.1 1 5.1 Hermetia illucens Larva 49 4 6.6 5.6 1.4 3.8 3.6 1.1 5.6 4.8 2.6 0.7 6 (soldier fly) (Contd.) 4 Indian Journal of Entomology 83(2021) Online published Ref. No. e20190

(Table 1 Contd.) Musca domestica Pupa 62 3.5 5.3 5.2 2.6 4.2 3.2 3.4 4.2 2.6 0.4 4.8 (house fly) Musca domestica Larva 54 3.2 5.7 6.9 2.2 5 3.3 3.2 4.4 4.9 2.8 0.4 5.1 (house fly) Hemiptera 48.83 3.93 6.45 3.93 2.78 5.93 3.9 0.78 5.38 3.76 2.5 1.8 5.62 Aspongubus viduatus Adult 27 2.1 2.3 1.6 3.6 1.1 1.8 2.6 1.3 2.1 2.1 1.7 (melon bug) Euschistus egglestoni Adult 46 4.4 7 3 2.8 3.3 4.8 0.6 6.1 4.3 3.2 1 4.8 (stink bug) Hoplophorion Adult 62 4.1 7.7 5.3 1.9 4.7 4.5 1 7.4 4.5 1.5 2.1 9 monogramma (treehopper) Krizousacorixa azteca eggs 64 5 8 3.5 2.9 6.2 4 1.1 6 (waterboatman) Pachilis gigas Adult 65 4.2 6.9 4.5 3.6 14.4 3.6 0.6 6.2 4.1 2 2.4 5.8 Umbonia reclinata Adult 29 3.8 6.8 5.7 1.9 5.9 4.7 0.6 4 4.6 3.7 1.4 6.8 Hymenoptera 51.43 5.2 8.27 6.27 1.85 2.6 4.7 0.39 6.1 5.03 2.61 1.6 4.87 Apis mellifera Adult 51 5.6 9.6 6.6 0.9 5.5 0 6.9 5.9 2.5 1.7 4.5 (honeybee) Apis mellifera Pupa 49 5.6 7.7 7.3 0.5 4.6 0 5.9 5.6 2.7 1 4.9 (honeybee) Apis mellifera Larva 42 6 9.4 7 0.8 6.1 0 6.2 6 2.6 1.3 2 (honeybee) Atta Mexicana Adult 58 5.3 8 4.9 1.9 4.1 4.3 0.6 6.4 4.7 2.5 1.5 4.7 (leafcutting ant) Brachygastra azteca Pupa 70 5.1 8.5 6.1 1.4 4.1 4.4 0.7 6.4 4.4 2.8 1.6 6.5 (wasp) Parachartegus Pupa 50 4.2 7.7 5.8 2 4.3 4.7 0.5 5.7 4.3 2.9 2 7.1 apicalis (wasp) Bee brood Immature 40 4.6 7 6.2 2.1 3.5 3.3 0.9 5.2 4.3 2.3 2.1 4.4 stages Isoptera (termite) 33 5.1 7.8 5.4 0.8 4.4 2.8 1.4 7.3 6.9 5.1 1.9 3 Macrotermes Dewinged 33 5.1 7.8 5.4 0.8 4.4 2.8 1.4 7.3 6.9 5.1 1.9 3 bellicosus adults Lepidoptera 65.25 4.58 6.45 6.33 1.38 5.1 3.75 1 7.45 4.17 1.5 1.23 Anaphe venata Larva 58 2.1 1.3 0.9 0 2.1 0.4 0 1.8 0.3 0.8 0 2.5 (African silkworm) Imbrasia epimethea Larva 62 2.9 8.1 7.4 2.2 6.5 4.8 1.6 10.2 6.6 2 1.9 7.5 (mopane caterpillar) Imbrasia truncate Larva 65 2.4 7.3 7.9 2.2 6.2 4.7 1.7 10.2 5.6 1.7 1.7 7.6 (mopane caterpillar) Usta Terpsichore Larva 76 10.9 9.1 9.1 1.1 5.6 5.1 0.7 7.6 1.3 3.3 (mopane caterpillar) Orthoptera 59.17 3.98 7.4 5.12 1.45 4.37 3.53 0.65 5.12 5.35 1.93 1.3 Acheta domesticus Adult 62 2.6 4.5 3.5 0.9 1.4 2.2 0.4 3.7 3.7 1.6 2.5 (cricket) Boopedon flaviventris Adult 56 4.7 8.8 5.5 1.8 4.1 4.4 0.6 5.7 4.3 2.4 2 7.4 (boopies) Gryllus assimilis Adult 56 3.4 6.6 5 1.2 2.9 3.3 0.7 5.3 5.8 2.1 0.5 4.5 (cricket) Gryllodes silligatus Nymph 56 3.7 6.9 5.3 1.6 3.1 3.5 0.9 5.2 5.7 2.2 0.9 4.2 (cricket) Sphenarium histrio Adult 60 5.3 8.7 5.7 0.7 4.4 4 0.6 5.1 6.6 1.1 1.3 7.3 (grasshopper) Sphenarium Adult 65 4.2 8.9 5.7 2.5 10.3 3.8 0.7 5.7 6 2.2 1.8 6.3 purpurascens (grasshopper) Ile- Isoleucine, Leu-Leucine, Lys-Lysine, Met- Methionine, Cys-Cysteine, Phe- Phenylalanine, Tyr-Tyrosine , Thr-Threonine, Trp-Tryptophan, Val -Valine, Arg-Arginine, His-Histidine (Tang et al., 2019) Insects as a viable source of proteins- A review 5 Thirulogasundhar Balakamatchi and Priya Sethuraman and tryptophan. Hence a diet that is balanced is vital if sources of protein. On a comparative basis, nymphs insects are to be consumed as a major part. contain the most amino acids than other stages of the growth cycle. They are abundant source of arginine Most edible insect species are in line with World which is said to be beneficial to the heart and the Health Organization’s recommendation for amino acids structural integrity and conditions of blood vessel. (World Health Organization, 2007). Entomic food help Apart from all these, it also serves as immunity booster. in acquiring the necessary levels of essential amino Arginine is found to be twofold the amount in nymphs acids when consumed as a part of a diet consisting of of cockroaches (Blatta lateralis) than when compared other foods as well. All edible insects have satisfactory to conventional livestock. levels of the amino acids viz., lysine, leucine, arginine, isoleucine, histidine, valine, threonine and tyrosine. Fatty acids: Insects are a great source of fats. The The leucine content in beetles is higher than that what fatty acids spectrum of a few edible insects that are is present in most other forms of proteins sources, not common on dry matter basis are given in Table 2. Apart exclusive to livestock. Phenyl alanine content in true from the listed acids, trace amounts of odd-numbered bugs are substantially more than that in all other known fatty acids, even-numbered saturated fatty acids and

Table 2. Fat content (%) of common edible insects (% in crude fat of dry weight) Name Develop- Crude Saturated fatty acids - SFA Monounsaturated fatty Polyunsaturated fatty mental fat (%) acids - MUFA acids - PUFA Stage Total C14:0 C16:0 C18:0 Total C16:1 C18:1 Total C18:2 C18:3 SFA MUFA n7 n9 PUFA n6 n3 Human fatty acid 26.9 30.85 16.9 14.95 1.5 requirement (g) Common meat Beef Adults 32.25 0.77 16.74 9.53 18.83 10.52 49.08 36.1 6.16 Pork Adults 41.04 3.43 21.68 12.71 43.04 2.93 39.39 16 7.29 1.71 Chicken Adults 33.33 1.33 22.67 8 46.67 0.27 41.33 20 14 0.67 Blattodea 25.05 37.18 1.22 23.13 11.41 45.02 2.33 41.88 17.85 16.43 0.75 (cockroach) Blatta lateralis Nymphs 21.9 48.3 1.9 26.8 18.1 42.2 3.3 38 9.6 8.7 0.7 Periplaneta Nymphs 28.2 26.07 0.54 19.47 4.72 47.84 1.35 45.76 26.09 24.17 0.79 americana Coleoptera 35.81 37.68 1.62 29.77 5.4 53.12 7.32 44.91 13.01 11.61 0.99 Copris nevinsoni Larvae 13.6 44.02 1.76 28.97 13.29 50.41 2.75 47.66 5.57 3.92 0.84 Rhynchophorus Larvae 50.23 39.9 2.85 34.2 1.7 55 19.65 35.05 22.85 19.5 2.75 phoenicis (African palm weevil) Tenebrio Larvae 38 30.12 0.39 28.2 0.89 66.77 5.98 60.63 3.11 2.84 0.18 molitor (Yellow mealworm beetle) Zophobas morio Larvae 41.42 36.69 1.47 27.7 5.7 40.31 0.91 36.29 20.51 20.19 0.18 (superworm) Diptera 21.94 45.74 6.63 22.53 2.18 34.65 16.87 17.63 16.04 15.08 0.88 Hermetia illucens Larvae 26 67.93 9.87 13.25 2.02 17.39 4.08 12.84 14.67 13.91 0.53 (soldier fly) Musca Pupae 15.5 33.4 3.2 27.6 2.2 38.9 20.6 18.3 17 14.9 2.1 domestica (house fly) Musca domestica Larvae 24.31 35.89 6.83 26.74 2.31 47.67 25.92 21.75 16.44 16.44 0 (house fly) Hemiptera 32.25 45.44 1.17 11.42 32.33 21.75 5.45 17.91 34.17 4.9 0.45 Aspongubus Adults 54.2 37.87 0.34 31.33 3.47 56.78 10.62 45.53 5.35 4.9 0.45 viduatus (melon bug) Tessaratoma 23.55 41.46 0.46 41 7.27 7.27 53.35 papillosa (Contd.) 6 Indian Journal of Entomology 83(2021) Online published Ref. No. e20190

(Table 2 Contd.) Meimuna Adults 19 56.99 1.99 2.47 52.53 1.2 0.28 0.92 43.8 opalifera Hymenoptera 18.71 34.58 1.54 23.83 8.46 50.97 2.57 43.99 4.07 3.39 0.6 Apis mellifera Adults 12.3 25.2 0.6 14.4 9.3 67 2.6 45.2 7.8 7.8 (honeybee) Apis mellifera Pupae 20.1 51.1 2.9 35.1 12.6 48.9 0.6 47.6 (honeybee) Apis mellifera Larvae 18.91 51.8 2.4 37.3 11.8 48.2 0.7 47.5 (honeybee) Polyrhachis vicina Pupae 22 24.1 0.6 17.67 4.3 72.27 8.77 61.43 3.6 2.07 0.8 (ant) Bee brood Immature 20.25 20.7 1.2 14.7 4.3 18.5 0.2 18.2 0.8 0.3 0.4 stages Isoptera (termite) 36.8 48.98 2.17 42.45 2.86 17.94 2.1 15.84 33.08 24.24 3.9 Macrotermes Dewinged 36.8 48.98 2.17 42.45 2.86 17.94 2.1 15.84 33.08 24.24 3.9 bellicosus Adults Lepidoptera 37.95 36.42 0.36 26.92 9.11 22.6 1.37 21.23 40.57 6.51 33.94 Bombyx mori Pupae 35 28.8 0.1 24.2 4.5 27.7 1.7 26 43.6 7.3 36.3 (domesticated silkworm) Imbrasia Larvae 23.38 37.88 1.15 31.9 4.71 36 1.8 34.2 26.12 6.02 19.6 belina (mopane caterpillar) Imbrasia Larvae 16.4 46.5 0.2 24.6 21.7 7.6 0.2 7.4 44.4 7.6 36.8 truncate (mopane caterpillar) Samia ricinii Larvae 77 32.5 0 26.97 5.53 19.1 1.78 17.33 48.17 5.11 43.06 (mopane caterpillar) Orthoptera 19.92 35.17 13.86 20.65 0.67 18.81 1.56 17.25 46.14 32.2 1.7 Acheta confirmata Adults 21.14 32.8 26.1 5.5 1.2 33.5 2.4 31.1 33.9 32.2 1.7 (cricket) Brachytrupes Adults 18.7 37.53 1.61 35.79 0.13 4.11 0.71 3.4 58.37 portentosus SFA- Saturated fatty acids, C14:0-myristic acid, C16:0-palmitic acid, C18:0-stearic acid, MUFA, C16:1 n7-palmitoleic acid, C18:1 n9-oleic acid, PUFA: C18:2 n6- linoleic acid, C18:3 n3- α-linolenic acid (Tang et al., 2019) some unsaturated fatty acids have been found in a few in linoleic acid. Caterpillars contain high amounts insects. Insects in the early stages of development have of polyunsaturated fatty acids and are abundant in from 8 to 70% of fat based on dry weight. The fatty acid α-linolenic acid. α-linolenic acid and linolenic acid compositions resemble most meat (Bukkens, 1997). It are essential amino acids as the human body cannot has been found that caterpillars and true bugs have the synthesize them on its own. highest fat content. Fats are abundant in larvae stages. The adults generally have a fat content <20%. In insects, Minerals: Insects are an excellent source of the fats are usually composed of triacyl glycerol (Arrese micronutrients such as minerals and vitamins. Studies and Soulages, 2010). SFA-saturated fatty acids and have been conducted which suggest that the contents MUFA-monounsaturated fatty acids make up > 80% can be altered in terms of quality and quantity through of nearly most fats. The saturated fatty acids content feed. They are a source of vitamins ranging from A, B1- in edible insects are primarily made up of palmitic and 12, C, D, E to K- all of which are vital for development stearic acids. SFAs are generally more than MUFAs and maintenance (Kourimska and Adamkova, 2016). among adults. Oleic acid is a common monounsaturated Butterfly and moth larvae are abundant in vitamins B1, fatty acid present in insects. Adult insects are the best B2 and B6 while the pupae of honey bees are plentiful in source of polyunsaturated fatty acids in comparison to vitamins A and D, and the red palm weevil is also rich in other conventional protein sources. Linoleic acid is the vitamin E (Rumpold and Schlüter, 2013) (Finke, 2005; primary constituent of poly unsaturated fatty acids in Bukkens and Paoletti, 2005). A huge array of essential insects. Grasshoppers and crickets are most abundant minerals is present in entomic foods ranging from iron, Insects as a viable source of proteins- A review 7 Thirulogasundhar Balakamatchi and Priya Sethuraman magnesium, manganese, phosphorus, potassium, zinc, abundant in fats and proteins and hence subsequently sodium to even selenium (Rumpold and Schlüter, 2013). have a higher calorific value. Thus, entomic products deriving from different developmental stages can cater The micronutrient composition of a few edible insect different sets of people with respect to their needs. The orders is summarized in Table 3. Mineral composition key takeaway is the fact nutritional value alone does on a dry weight basis. The mineral composition of not correspond to healthy food. Healthy food is a food insects varies greatly amongst orders. For example, the that is balanced between its calorific significance and majority of edible insect species are known to contain nutritive contents. only trace quantities of calcium whereas house fly larvae and adult melon bugs are rich in calcium (Mustafa et Cultural values al., 2008). Camoati (a swarming wasp species) pupae provides a trace quantity of potassium- a meagre 54 India: A huge variety of edible insect species mg/ 100 g while the honey bee at all stages of its can be eaten at various stages of their life cycles, for developmental cycle provides a whopping 1500 mg of example, silkworms are eaten at both larval and pupa potassium/ 100 g in the least. Adult termites can provide stages. Local residents have put to use their traditional only 6.1 mg of magnesium/ 100 g adult stink bugs can knowledge from a long time to eat each insect species provide 1910 mg/ 100 g. However, most insects which in a different way but according to them healthy insects are edible are particularly abundant with iron. Entomic must be caught alive and processed immediately. Ethnic meat claims to contain more iron than fresh beef. tribe members belonging to the north eastern parts of and Arunachal Pradesh when interviewed explained Apart from just being micro and macronutrient that they eat both immature as well as adult stages sources, entomic foods also play a significant role in of insects. Almost all of the Odonata whose aquatic calorific contributions that may range anywhere between larvae were preferred to be consumed over adults, but 290-750 kcal/ 100g (Ramos-Elorduy et al., 1997). in others, as with the Orthoptera and Hemiptera the Usually, adults contain a high amount of chitin- in the adult stages were more highly appreciated. Katydid form of exoskeleton, which cannot be digested by the species were also preferably consumed as immature human body and hence is subsequently low in calorific specimens. Hymenopterans were eaten at all stages of and nutritive values. Generally, the larvae and pupae are the lifecycle: eggs, larvae, pupae and adults and even

Table 3. Mineral composition (mg/g- dry weight) Species Stage/ Part Common elements Trace elements Ca K Mg P Na Fe Zn Mn Cu I Se Recommended daily 1300 4700 240 700 <=1500 33 8.5 2.2 1.1 0.03 intakes [mg/ day] for adults Blattodea (cockroach) Blatta lateralis Nymph 24 160 21 122 53 Periplaneta Nymph 38.5 224 25 176 74.4 1.48 3.27 0.26 0.79 0.03 0.03 americana Coleoptera Callipogon Larva 157 15.2 135 15.2 47.2 barbatus (longhorned beetle) Rhynchophorus Larva 54.1 1025 131.8 352 52 14.7 26.5 0.8 1.6 – phoenicis (African palm weevil) Tenebrio molitor Larva 47.18 895.01 210.24 748.03 140.94 5.41 13.65 1.36 1.6 0.01 0.07 (Yellow mealworm beetle) Zophobas morio Larva 81.02 750.59 118.29 562.95 112.83 3.92 7.29 1.02 0.86 – (superworm) Diptera Drosophila Larva 140 130 1100 45.42 14.7 1.61 0.87 melanogaster (fruit fly) (Contd.) 8 Indian Journal of Entomology 83(2021) Online published Ref. No. e20190

(Table 3 Contd.) Hermetia illucens Larva 934 453 174 356 88.7 6.66 5.62 6.18 0.4 0.03 0.03 (soldier fly) Musca domestica Adult 76.5 303 80.6 372 135 12.5 8.58 2.66 1.29 0.01 0.02 (house fly) Musca domestica Larva 2010 1320 660 60.4 23.7 5.6 3.4 (house fly) Hemiptera Aspongubus Adult 1021.21 200.08 301.1 1234.33 401.1 viduatus (melon bug) Agonoscelis Adult 759.51 412.52 309.22 923.11 340.41 pubescens Euschistus Adult 204 108 1910 397 57 59 egglestoni (stink bug) Hymenoptera Apis mellifera Adult 222.9 1585.4 201.7 860.1 75.6 37.7 14 4.6 (honeybee) Apis mellifera Pupa 97 2207.3 193.9 900 60.8 15.3 11.7 3.7 (honeybee) Apis mellifera Larva 84.9 1871.9 177 782.5 59.4 13.3 11.6 3.6 (honeybee) Oecophylla Adult 79.7 957 122.1 936 270 109 16.9 6.3 2.17 virescens (tree ant) Polybia occidentalis Pupa 93 54 982 59 35 28 Bee brood Immature 59.48 1159.48 90.95 771.55 55.17 5.56 6.9 0.26 1.72 stages Isoptera (termite) Macrotermes Dewinged 0.1 336 6.1 1.49 112 0.96 0.1 0.08 0.07 0 nigeriensis adults Lepidoptera Anaphe venata Larva 40 1150 50 730 30 10 10 40 1 (African silkworm) Bombyx mori Larva 102.31 1826.59 287.86 1369.94 274.57 9.54 17.75 2.49 2.08 0.08 (domesticated silkworm) Bombyx mori Pupa 158 207 474 26 23 0.71 0.15 (domesticated silkworm) Imbrasia epimethea Larva 224.73 1258.06 402.15 666.67 75.27 13.01 11.08 5.81 1.18 (mopane caterpillar) Imbrasia truncate Larva 131.61 1348.44 192.02 841.42 183.39 8.74 11.11 3.24 1.4 (mopane caterpillar) Usta Terpsichore Larva 391 3259 59 766 3340 39.1 25.3 6.7 2.6 (mopane caterpillar) Orthoptera Acheta domesticus Adult 132.14 1126.62 109.42 957.79 435.06 6.27 21.79 3.73 2.01 0.06 (cricket) Boopedon Adult 88 66 521 173 24 32 flaviventris (boopies) Ruspolia differens Adult 24.5 259.7 33.1 121 229.7 13 12.4 2.5 0.5 (cricket) Sphenarium histrio Adult 82 177 420 1142 16 78 (grasshopper) Sphenarium Adult 112 377 424 609 18 42 purpurascens (grasshopper) (Tang et al., 2019) Insects as a viable source of proteins- A review 9 Thirulogasundhar Balakamatchi and Priya Sethuraman their products like honey, propolis, and wax were used. also highly sought after in the form of chutney. Only Adult termites are consumed either roasted or dry fried the adult stages of termites are consumed either roasted after removing the wings and sometimes also eaten or dry fried after discarding wings. Rajan (1987) stated raw. A large number of the edible beetles are eaten at in his works that in Tamil Nadu, winged termites are their adult stage, although some like Xylorhiza sp. are collected and sold to the merchants in the market by a increasingly being preferred in their larval stages. forest tribe. The wings are removed and the termites are deep fried in oil or fried along with groundnut by Prosopocoilus sp. and Odontolabis gazelle beetles adding bengal gram, puffed rice and salt. are consumed equally readily as larvae and adults. Preferences for specific stages of development Although insects are plenty in number in India typically depended on a variety of factors: palatability and a large percentage of the population live in rural of the insects - which is subject to change between or semiurban areas, the diversity of insects consumed developmental stages, availability and how easily the is much lower especially in south and central parts of insects can be harvested, and in addition taboos or India; besides there are no conclusive reports of entomic religious beliefs may be involved as well. In the case food being consumed in other parts of India. of Odonata their aquatic larvae are more convenient to harvest than their adults and so is the case in Coleoptera The West: In a lot of western countries, especially as well with their wood-boring larval grubs. Preparatory European ones, the issue of rearing edible insects as methods for insects for human consumption include food and feed has become a hot topic among scientific frying, boiling, and roasting. Stink bugs, bees, ants and communities, companies and policy makers, as well as termites are consumed both cooked and raw. Members among consumers who view entomophagy with either the ethnic tribes when interviewed exclaimed that they curiosity or disgust. Historically speaking, eating insects incorporate various ways to impart flavor to an insect is not a common eating practice in western societies and dish. Short-horned grasshoppers (Acrididae) are deep is considered new. However, there have been findings fried after having their wings removed from their of the ancient Greeks and Romans considering some s body and are then simply eaten with salt; they are also of insects, especially grasshoppers and beetle larvae, sometimes stuffed in a bamboo pipe, smoked dried as a delicacy (DeFoliart, 1995; 1999). Van Huis (2013) for 3-4 days, infused with pepper and salt and then estimated that about two billion people in the world eaten along with rice meals. Long horned grasshoppers consider insects as a food source. However, in Europe (Tettigonidae) are collected in fewer counts than their and other western countries, this has never been the short-horned relatives because of their solitary lifestyles- case and remains rare (Bodenheimer, 1951). Although making them harder to harvest of the former. They are the Food and Agriculture Organization- FAO in 2013 deep fried after having the wings removed from the has identified numerous social, environmental, and body. They are generally fed to children or aged persons. nutritional benefits associated with entomophagy, Crickets (Gryllidae) and mole crickets (Gryllotalpidae) western society generally considers these insects only are extensively harvested during summer nights between as an emergent food source, and associates eating the months of May and July. Yet the most highly valued insects with low prestige and poverty (Van Huis et al., orthopteran foods amongst the Galo tribe belonging to 2013; Henry, 2009; Sogari, 2015). Only in the recent the Himalaya are the Asian dune crickets of the specific past has the media, research institutes and the food species Schizodactylus monstrosus (Schizodactylidae). industry paid considerable attention to entomophagy. The grasshoppers are harvested fresh put inside a Many institutions are leading research in topics such bamboo pipe and smoked dry for nearly a time period as the costs and benefits of introducing edible insects of 7 days. Then the completely grasshoppers are crushed as food and feed (Deroy, 2015; Van Huis et al., 2013). into a dry powder and mixed with seasonings to make a These indicate the rise of a plausible niche market in special type of chutney (traditional recipe). This chutney the future. Numerous studies conducted in European eaten with rice or even as sides for a local fermented countries such as Italy, Belgium and the Netherlands rice-based drink known as Apung and is regarded as a have indicated that consumers have not overcome the savory by all members of the tribe. These insect-based fear and disgust factor related to insects, but at the chutneys can also be based on other species as well- same time are also curious to try these novel products dried or even raw, which are turned into a paste with (Caparros Megido et al., 2014; Materia and Cavallo, chili and salt. Stink bugs such as the species Aspongopus 2015; Pascucci and Magistris, 2013; Menozzi et al., nepalensis and others collected from river banks are 2017; Van Huis and Oonincx, 2017). 10 Indian Journal of Entomology 83(2021) Online published Ref. No. e20190

CONCLUSIONS Awoniyi T A, Adetuyi F C, Akinyosoye F A. 2004. Microbiological investigation of maggot meal, stored for use as livestock feed The burning question at the end is whether people component. Journal of Food, Agriculture and Environment 2 (3- can be convinced enough to reduce their conventional 4): 104-106. proteins consumption and switch to entomic proteins. Belluco S, Losasso C, Maggioletti M, Alonzi C, Ricci A, Paoletti M G. 2015. Edible insects: a food security solution or a food safety This question was in fact somewhat addressed recently concern?. Animal Frontiers 5(2): 25-30. (Van Huis and Oonincx, 2017). In European and most Berger J, Blanchard G, Ponce M C, Chamnan C, Chea M, Dijkhuizen M, other western countries, the consumption of edible Doak C, Doets E, Fahmida U, Ferguson E, Hulshof P. 2020. The insects will primarily depend on their availability in SMILING project: A North- South-South collaborative action to the market- which is a direct relation to the industrial prevent micronutrient deficiencies in women and young children in Southeast Asia. Food and Nutrition Bulletin 34(2_suppl. 1): reverence, regulatory frameworks, communication S133- 139. and also (Menozzi et al., 2017). However, it is worth Bodenheimer F S. 1951. Insects as human food. In insects as human noting that just sheer willingness to try entomic food. Springer, Dordrecht. pp. 7-38. products does not necessarily imply that consumers Bukkens S G, Paoletti M G. 2005. Insects in the human diet: nutritional are ready to incorporate insects as a part of their diet aspects. Ecological implications of Minilivestock 2005: 545-577. (Tan, 2015). Moreover, stressing upon the sustainability Bukkens S G. 1997. The nutritional value of edible insects. Ecology of benefits alone has no practical difference in the taste Food and Nutrition 36(2-4): 287-319. or palatability of these insect products (Tan, 2015; Van Caparros Megido R, Sablon L, Geuens M, Brostaux Y, Alabi T, Blecker C, Drugmand D, Haubruge É, Francis F. 2014. Edible Huis and Oonincx, 2017). Therefore, transcending the insects acceptance by Belgian consumers: Promising attitude for negative annotations tagged to the taste experience is entomophagy development. Journal of Sensory Studies 29(1): crucial (Sogari et al., 2018). It is also worth noting that 14-20. it would be helpful in the first stage of insect-based Cavallo C, Materia V C. 2018. Insects or not insects? Dilemmas or attraction for young generations: A case in Italy. International products if they do not contain any visible parts of insect Journal on Food System Dynamics 9(3): 226-239. explicitly and should be sold in the most appealing DeFoliart G R. 1995. Edible insects as minilivestock. Biodiversity and form of packaging in order to be successful (Cavallo Conservation 4(3): 306-321. and Materia, 2018). Shelomi (2015) suggests that DeFoliart G R. 1999. Insects as food: why the western attitude is stakeholders interested in developing entomic foods important. Annual Review of Entomology 44(1): 21-50. should be aware that smarter marketing strategies may Deroy O, Reade B, Spence C. 2015. The insectivore’s dilemma, and how work better than just plainly convincing consumers that to take the West out of it. Food Quality and Preference 44: 44-55. “eating bugs is healthy”. There might be opportunities DESA 2019. UN. World population prospects 2019: Highlights. New to create profitable businesses in entomophagy, but York (US): United Nations Department for Economic and Social Affairs. the growth of the industry will mostly depend on the Dobermann D, Swift J A, Field L M. 2017. 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(Manuscript Received: May, 2020; Revised: September, 2020; Accepted: September, 2020; Online Published: November, 2020) Online published (Preview) in www.entosocindia.org Ref. No. 20190