as human food: An overview

562 Amazôn., Rev. Antropol. (Online) 5 (3) Especial: Insects as human Insects as human food: An overview food: An overview

E R A L D O M E D E I R O S C O S T A N E T O

Universidade Estadual de Feira de Santana, Brasil

563 Costa Neto, E. M.

INSECTS AS HUMAN FOOD: AN OVERVIEW Abstract Although insects and the products elaborated and/or eliminated by them are used as food source by three thousand traditional societies in over 120 countries, current attitudes of repugnance regarding the con- sumption of edible insects cause that a considerable amount of protein becomes unavailable to those individuals who suffer from pro- tein deficiencies. Considering the nutritional qualities that insects have, they should be considered as renewable resources available for sustainable exploitation aiming at reducing the problem of malnutrition and hunger in many parts of the world. Keywords: Entomophagy, food safety, renewable resources, culture, insects.

INSETOS COMO ALIMENTO HUMANO: UMA REVISÃO GERAL Resumo Embora os insetos e os produtos elaborados e/ou eliminados por eles se- jam usados como fonte de alimento por três mil grupos étnicos em mais de 120 países, as atitudes comuns de repugnância direcionadas ao consumo de insetos comestíveis levam a que uma quantidade considerável de proteína animal fique indisponível para aqueles indivíduos que sofrem de deficiências proteicas. Observando as qualidades nutricionais que os insetos possuem, eles deveriam ser considerados como recursos renováveis disponíveis para exploração sustentável, assim diminuindo o problema de desnutrição e fome em muitas partes do mundo. Palavras-chave: Entomofagia, segurança alimentar, recursos renováveis, cultura, insetos.

564 Amazôn., Rev. Antropol. (Online) 5 (3) Especial: 562-582, 2013 Insects as human food

INSECTOS COMO ALIMENTO HUMANO: UNA VISIÓN GENERAL Resumen Aunque los insectos y los productos elaborados y/o eliminados por ellos sean utilizados como fuente de alimento por tres mil grupos étnicos en más de 120 países, las actitudes comunes de repugnancia hacía al consumo de insectos comestibles provoca que una cantidad considerable de proteína animal esté indisponible para aquellos individuos que sufren de deficiencias proteicas. Observándose las cualidades nutricionales que los insectos poseen, se debería considerarlos como recursos renovables disponibles para ex- ploración sostenida, así disminuyendo el problema de mala nutrición y el hambre en muchas partes del mundo. Palabras-clave: Entomofagia, seguridad alimentaria, recursos renovables, cultura, insectos.

Endereço do autor para correspondência: Departamento de Ciências Bi- ológicas, Universidade Estadual de Feira de Santana, avenida Transnordes- tina, S/N, Bairro: Novo Horizonte, CEP: 44036-900, Feira de Santana, BA, Brasil. E-mail: [email protected]

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INTRODUCTION dietary supplement, as a replacement of other food in times of shortage, Insects have been used as foodstuffs or as the main constituent of the since the dawn of human race. Aus- diet. However, consumption tralopithecus robustus Broom, 1938 used is widespread since edible species are bone tools to dig into termite mounds used by approximately three thousand 500.000 years ago (van der Merwe et ethnic groups in 120 countries (Ra- al. 2003). There are rock paintings de- mos-Elorduy 2000). Almost all taxa picting humans collecting honey from are consumed, but some groups only beehives that date back to Paleolithic locally. While saturniid caterpillars, times (Hernández-Pacheco 1921). grubs, grasshoppers and crickets Even in the Bible there are records of are popular almost everywhere, adult the use of insects as food. The manna dragonflies are consumed only in SE- was nothing more than the excretion Asia and certain salt flies only in the of the mealybug Trabutina mannipara USA (Bristowe 1932; Essig 1934; Ber- (Hemprich and Ehrenberg 1829) (Ho- gier 1941; Bodenheimer 1951; Stone moptera: Pseudococcidae). Females 1992; Malaisse 1997; Banjo et al. 2004; eliminate a sugary liquid that in arid DeFoliart 2004; Ramos-Elorduy 2004; climates dries over leaves and builds Yen 2009b). In some cases, only se- up in layers (Buzzi & Miyazaki 1993). lected instars of an insect species are In the Mideast, people still collect the consumed, e.g. termite imagos or wasp sweet excretion of scale insects that larvae and pupae. In other taxa, almost feed on tamarisk (Tamarix mannifera all stages are exploited, e.g. juvenile Kotschy ex Bunge). They call it “man” and adult grasshoppers and crickets and it is, most likely, the manna describe or ant eggs, larvae, pupae and imagos in the Old Testament (Hölldobler & (DeFoliart 1989). Wilson 1994). The degree of entomophagy in a Estimates of the number of insect country varies greatly and is influ- species that are consumed by humans enced by history, tradition and so- vary, but worldwide at least 1,400 spe- ciety. In most developing countries, cies have been recorded as human insects are mainly consumed by in- food (Durst & Shono 2010). Depending digenous sectors of low income, on species and instar, they are rich in showing that insects, in their pres- proteins, fats, carbohydrates or salts, ent form of usage, represent an eco- providing the consumers with valuable nomical source for animal protein nutrients that are reasonably easy to (Ramos-Elorduy 2011). There are obtain, usually by selecting the ani- exceptions to this rule, e.g. Mexican mals in their natural habitat (Ramos- ant pupae (“escamole”) consumed Elorduy et al. 1997, 1998a, 1998b). In as delicatessen or an array of insects fact, most traditionally-living cultures consumed deep-fried in streets of still practice entomophagy, consuming Thailand (Maheu 2011). a set of many different species as a

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Insects are also consumed indirectly grubs and caterpillars (Ramos-Elorduy through ingestion of contaminated food et al. 2008). Some works suggested using as eggs, feces and even fragments of wild pest species as food, especially wings, legs and antennae of cockroaches, grasshoppers (Cerritos & Cano San- bees, ants, crickets and other insects tana 2008), while others express their are found. This is due to the impos- concern regarding insect consump- sibility of complete removal of in- tion from the wild (Ramos Elorduy sect parts from food products (Posey 2006; Yen 2009a). A series of works 1986). According to Myers (1983), the contemplates the health risks associated Food and Drug Administration of with managing insects (Adamolekun U.S.A. (FDA) is acceptable as the en- et al. 1997; Akinnawo et al. 2002). counter of five insects or insect parts FAO believes that the specific role of to 100g of apple butter and 30 insect edible insects and their potential in food fragments per 100g peanut butter. safety, quality diet and poverty allevia- tion is severely underestimated (van They are also eaten through the substances Huis 2012). Recently, this organization produced by them and used by us as held a meeting on entomophagy in colorants. Today, most culinary dyes Asia (Durst et al. 2010), showing both have synthetic origin, but in the past diversity and potential of insect con- the red and pink colors were obtained sumption across Asia. However, most from insects. The pigment phenoxa- data focuses on captured from zine (orange) extracted from Pachilis the wild. Still, this conference created gigas B. (Hemiptera: Coreidae) showed more awareness in seriously considering high dyeing power; it can be used as a entomophagy as a part to solving the colorant to ice creams, cheese, mayonnaise food supply problems to come. and cream (Perez et al. 1989). The red carmine pigment extracted from Dac- For each traditionally-consumed spe- tylopius coccus Costa, 1835 (Homoptera: cies there is a history of safe use that Dactylopiidae) is used as a dye for intends to minimize the consumption coloring drinks. risks. Saturniid caterpillars in Western Africa have to be boiled before further Most traditionally-consumed insects processing in order to inactivate the may be picked, handled and con- inherent thiaminase; cases of beriberi verted into nutritious foodstuff easily have been associated to indiscriminate (Johnson 2010). Traditionally, insects consumption of raw caterpillars. The are consumed either in a raw state or history of safe use is also important in heated in some fashion. Depending on order to tell inoffensive species from the culture, heating occurs in hot ashes, toxic ones (van Huis 2012). In this toasting devices or by deep-frying regard, Blum (1994) discusses on the them in oil. In dry areas, preservation toxicity of insects eaten by humans, is done by heating and posterior sun- providing several examples of species drying; eventually, evisceration was that should be avoided as food, such as performed before, as in the case of

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cyanogenic species (e.g., butterflies of the pederin, a non-protein compound the families Nymphalidae and Helico- that is a potent inhibitor of protein nidae), vesicants species (e.g., Lonomia synthesis and mitosis. moths), those ones that produce ste- In general, the determinants of the use roids (e.g., Ilybius fenestratus Fabricius, of insects as a food resource for humans 1781, Dysticidae) and corticosteroids result from four variables: 1) physical hormones (e.g., Dytiscus marginalis Lin- environment; 2) availability and acces- naeus, 1758, Dysticidae), necrotoxic sibility of insects that, in turn, depend alkaloids (e.g., fire ants Solenopsis spp.) on their life cycle, host plants, behavioral and toluene (e.g., cerambicids of the adaptations and general ecology; 3) genus Syllitus). According to this au- mode of production and subsistence thor, the scientific knowledge about methods of a given culture; 4) dietary the toxic effects of most natural in- restrictions, both nutritionally and tem- sects is still very scarce. He classifies porally (Miller 1997). This author says toxic insects into two groups: crypto- that an insect is suitable for use as a toxic and phanerotoxic species. food source when it is available in large Phanerotoxic insects include those that are quantities and is easily collected. The venomous, presenting a poison apparatus that importance of a particular animal as a includes a venom gland, a reservoir, a food source for humans is also deter- duct and an apparatus for injecting the mined by the efficiency by which this venom. Representatives of this group animal converts food that it consumes are insects of the orders Lepidoptera into its own body weight. The highest (urticating caterpillars), Hymenoptera weight that is obtained per gram of (ants, wasps, and bees) and Hemiptera food ingested corresponds to the more (assassin bugs), whose secretions are efficient animal in terms of feed con- distributed both by retractable stingers, version (Conconi 1984). Thus, edible mouthparts for piercing or stinging insects are highly efficient in this pro- arrows. The toxins produced by pha- cess, only competing with the chicken. nerotoxic species only become active However, insects and other arthro- by injection, becoming inactive in the pods are still insufficiently investigated gastrointestinal tract. Nevertheless, by anthropologists and entomologists, some caution is advised. being generally regarded as marginal Cryptotoxic insects are those that pro- resources in studies on the uses of duce non-toxic exocrine secretions, various available resources. Therefore, whose toxicity is manifested only when it is necessary that researchers conduct they are ingested. These species require studies using an interdisciplinary approach more careful in their selection as items and pay attention to the values and to be consumed. Staphylinid of knowledge of traditional people. It is the genus Paederus, for example, pro- essential to record the rich amount of duce vesicants which are only detected traditional knowledge, customs, and when they are crushed. One of these is practices of indigenous and non-in-

568 Amazôn., Rev. Antropol. (Online) 5 (3) Especial: 562-582, 2013 Insects as human food digenous peoples since, with no doubt, economically weaker parts of their so- they are living representatives of their cieties (Ramos-Elorduy 2011). In Thai- own culture as well as they have a land, a country that has a strong tradi- significant knowledge on the biologi- tion of entomophagy, individuals who cal resources they depend upon. In have migrated to urban centers and re- this regard, traditional peoples know ceived a formal education “learned” to where, how and when to find edible despise local entomophagous resources insect species, and they know different when they expose themselves to a ways to prepare and conserve them in cosmopolitan culture that has preju- order to have these resources in times dices against insects (Chen et al. 1998). of shortage (Ramos-Elorduy 1982). Moreover, edible insects may serve as a form of national identity as they turn into elements of identification of CULTURAL RESTRICTIONS TO individuals belonging to the same cul- ENTOMOPHAGY ture (Ramos-Elorduy 1996). Distaste Entomophagy is not practiced univer- for the consumption of insects causes sally. According to Maheu (2011), the that a considerable amount of animal greatest obstacles to consumption of protein becomes unavailable to those insects are cultural and without a deeper people who suffer from hunger and understanding of the limitations and malnutrition. possibilities crystallized by culture it In Descola’s opinion (1998), the habit will not be possible to promote ento- of eating or not eating insects depends mophagy. The idea that we are what on the variability of individual choice we eat is present in all cultures. These within an accepted norm, as well as the beliefs complicate the incorporation accessibility of the animal. The author of insects in the diet because all as- complements saying that even within sociations and assignments related to tribal societies there is great variability these influence our percep- of individual food preferences and at- tion of them as food, much more than titudes toward animals. Marvin Harris, their nutritional value. a cultural materialistic, explained the Apparently, Western societies gave it repulse on the consumption of insects up at Christianization and generally through a cost/ benefit ratio. He said consider this food habit as disgusting, there are three reasons why a food is to primitive or a sign of poverty. This exam- be banned from the menu: when food ple is currently followed by those sec- becomes expensive to be obtained or tors of traditionally entomophagous prepared, when there is more nutritious societies that seek to copy a Western and inexpensive replacement, or when lifestyle; being able to afford meat of there is a negative impact on the envi- domestic animal species is one of the ronment. Over time the food becomes ways to show social and economical culturally repelled as a food “bad to eat” progress and to mark a difference to (Harris 1999). Considering the use of

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insects, he states “the reason we do not to creatures as different and distinct eat insects is not because they are dirty from our own species (Kellert 1993). and disgusting. Instead, they are dirty and According to this author, more posi- disgusting because we do not eat them.” tive attitudes directed at invertebrates are observed when these animals have Different explanations for the consistent aesthetic, utilitarian, ecological or recre- human aversion addressed to insects and ational values. other invertebrates are available in the literature. One says that humans are Although edible insects have a high biologically predisposed or prepared nutritional value for humans, they to fear certain animals, like snakes, have not been considered a significant scorpions and spiders (Seligman 1971). source of food and studies on their use Another explanation says that com- as animal feed and waste recycling are mon and non-clinical entomophobias still scarce. It is clear that we cannot may be closely related to the human re- consume what we do not know about. action of “disgust”, whose benefits are To introduce insects in the diet, we considered as an adaptive prevention need to know which species are edible, of disease transmission (Davey 1993, and how they need to be prepared and 1994; Matchett & Davey, 1991; Ware cooked for consumption. The fact that et al. 1994). Paul Rozin (1995) shows knowing about the nutritional and eco- how foods are primarily classified as logical advantages of entomophagy, pleasant or unpleasant, categories that as well as the consumption of insects depend largely on individual varia- by indigenous peoples, can contribute tions, sometimes genetic, and secondly to arise some sympathy among en- as appropriate, inappropriate, disgust- lightened people, but it will never be ing, dangerous, beneficial, categories enough to eliminate blockages and re- that are basically determined by cul- invent the insect as a privileged food ture. The author also shows how some where it is initially viewed with despise. things can be considered edible as well To the statements of economic, eco- as taboo, and how certain foods are logical and nutritional importance of more prestigious than others. Our way entomophagy to human beings, we of classifying insects and the incorpo- also need to take into consideration rative beliefs form the basis of a reac- the very nature of our psycho-cultural tion of disgust toward them, so the limitations (Maheu 2011). majority of the population blocks the As a measure to increase the nutritional idea of consuming insects. The aver- contribution of edible insects, DeFoliart sion involves deep emotions and our (1989) suggests the following approaches: own sense of identity in a way that de- fies any kind of rationalization (Miller • Development of a stronger 1997; Rozin & Fallon 1987). global defense in order to es- tablish better communication A third interpretation was suggested and mutual support among by the notion of human alienation scientists and other interested

570 Amazôn., Rev. Antropol. (Online) 5 (3) Especial: 562-582, 2013 Insects as human food people in the use of insects as In a society that rejects the consump- food for humans and animal tion of insects there are some individuals feed. who overcome this rejection, but most will continue with this attitude. It will • More consistent support for be very difficult to convince an entire scientists from developing society that insects are totally suitable countries who are interested for consumption. In Latin American in maximizing the nutritional countries, where insects are already contribution of native species consumed, a portion of the popula- of edible insects. tion despises consumption and asso- • Development of methods and ciates it with poverty and Indianness economic strategies regarding (Katz 2011). There are also examples the mass collection of edible of people who have had the habit of species that are attracted to light consuming them and abandoned that or chemical traps. habit due to shame, and because they • Development of controlled do not want to be categorized as In- mass production of native spe- dians or poor (Costa Neto 2011). cies of edible insects from de- According to Katz (2011), if the con- veloping countries. sumption of insects as food luxury is to be promoted there would be more • Development of recycling chances that some individuals who do systems using insects to con- not present this habit overcome ideas vert organic waste substances under which they were educated. And and supplements underuti- this could also help to revalue the con- lized in feed for poultry, pigs sumption of insects by those people and fish. who already eat them. • Development of strategies for mass collecting for gregarious destructive pests (e.g. Schistocerca IN FAVOR OF ENTOMOPHAGY gregaria Forskål, 1775). Entomophagy has long ceased to be • Educating the public on the an unstudied phenomenon. Notes on palatability and nutritive quality entomophagy were issued the moment of insects, as well as its impor- non-entomophagous Europeans came tance as a food resource for into contact with insect-consuming so- improving the health and life cieties. Meanwhile, scientists of many of the various ethnic groups areas studied entomophagy from their in developing countries. specific point of view, e.g. archaeology, anthropology, sociology, and life sciences • Conducting extensive studies (Allotey & Mpuchane 2003; Chakra- on food quality and safety of vorty et al. 2011; Mbata et al. 2002; selected species. Menzel & D’Alusio 1998).

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For many species, nutritional data were the upper segment (> 60%), the more raised, showing great variation according to common feeds and foods are either species and instar; while protein pre- endangered (tuna and gadiform fish), vails in many adult instars (imagos), relatively expensive (pike, crustaceans), many juvenile instars (maggots, grubs, unsuitable for non-aquatic livestock caterpillars and pupae) also tend to feeding (fish meal) or discussed con- contain elevated levels of fat. Vita- troversially (meat, blood and feather mins and mineral content also varies. meals), with algae and common mush- A Mexican study revealed that in dry rooms being the only handy alterna- matter, grasshoppers may yield up to tives. However, dry matter in these approx. 80% of protein, products is approx. 10% or lower. In- grubs 60% of fat and 35% of fiber, sects usually contain between two and and pierid caterpillars 10% of ashes three times more dry matter. In this (Ramos-Elorduy & Pino Moreno sense, it seems quite illogical the fact 1989; rounded values). Nutritional data that eating invertebrates such as lobsters, of many other local species have been crabs, shrimp, oysters, be considered gathered, e.g. from Botswana, Nigeria, as part of regular diet, while the con- Zambia, India, Japan, China, and Aus- sumption of insects, also invertebrates, is tralia (e.g. Amadi et al. 2005; Banjo et viewed with reservations by most people. al. 2006; El Hassan et al. 2008; Omotoso As mentioned above, food conver- 2006). Even data on quality deterioration sion is an important factor for farmed of processed insects exist (Mpuchane et livestock; to produce one kilogram of al. 2000). Corresponding papers usually meat, 3 to 4 kg of feed have to be ad- also include data on the species identifi- ministered to a pig, 4 to 6 to guinea cation, its life cycle, insect collection and fowls, and 7 to 10 kg to cattle. In in- preparation, so a certain data base exists. sects, conversion may be close to 1:1 Obviously, the chitinous exoskeleton is (depending on species and instar), and not digestible by humans (as well as the due the lack of bones, yield of edible bark of the apple!), but the exoskeleton is tissues is larger. Although some areas only a small part of the total biomass were already subjected to research, (about 4% in caterpillars) and does not many others still remain relatively un- affect the nutritional value of insects touched, e.g. the nitrogen use efficiency. as food (Berenbaum 1995). Insects also serve as feed for a great When comparing different feedstuffs variety of animal species, including do- and foodstuffs with regard to the pro- mesticated ones and those which are tein content (Ramos-Elorduy & Pino- being domesticated (e.g. poultry, pigs, Moreno 1989; Gordon 1998), it be- commercial fish species, frogs, ratites comes clear that insect protein levels and reptiles). Some insect species are usually range above those of most reared to satisfy the demand for feed plants, being equal to that other, more insects by keepers of herpetofauna, commonly used feed and foodstuffs. In fish and birds. Finally, zoos also pro-

572 Amazôn., Rev. Antropol. (Online) 5 (3) Especial: 562-582, 2013 Insects as human food duce insects as a feed additive for the animals they exhibit (DeFoliart 1995; Schickler 2011). While most research papers deal with traditional (in situ) entomophagy, only some authors issued cookbooks for the Western taste (Gordon 1998; Fritzsche Figure 1 – Cricket-based dishes (Cantonese & Gitsaga 2002) combining insect with stew, brochette, and cheese rolls). Photo by known ingredients to a great variety Janette Lagunas Raya (2009). of dishes. These dishes however still contain and display entire insects and might therefore still frighten off pho- bic consumers. Indeed, people are able to consume insects since these animals are presented in a disguised form. During the First National Symposium on Anthro- poentomophagy held at Feira de San- tana State University, Brazil, in March 2009, this scenario could be observed. In the workshop of insect cuisine, par- Figure 2 – Canapés made of dulce de leche ticipants tasted salty and sweet culinary and fried Atta ants. Photo by Gloria Patri- preparations containing some insects cia Arango Gutiérrez (2009). (crickets, mealworms, and leaf-cutting known (or better, despised) since the ants). During this workshop, “in na- consumption of insects is taken as a ture” insects brought greater resistance practice of ‘primitive people’ (Costa to consumption, while preparations Neto 2003, 2004, 2011). It is a dis- with crickets (Cantonese stew, pizza, service to state that insects are eaten brochette, and cheese rolls) (Figure only in times of scarcity and famine, as 1), strawberries with mealworms, and these organisms provide a significant dulce de leche ant canapés (Figure 2) amount of calories and nutrients that are were readily accepted and tasted by available to people (Ramos-Elorduy 2004). all participants. It might be noted also that most people, after consumption, reacted positively to the flavor and tex- HYPOTHESIS OF NUTRACEUTICAL ture of the insects, while the look and ENTOMOFAUNA sociocultural issues were factors of lower It is known that insects are very prolific in receptivity (Linassi & Borghetti 2011). the synthesis of chemical compounds, such Despite the growing number of arti- as alarm and mating pheromones, defensive cles, reviews and books published on sprays, venoms and toxins sequestered from the potential of insects as human food, plants or their prey and later concentrated or the entomophagous habit remains un- transformed for their own use (Pemberton

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1999). This huge quantity of chemicals in- WHAT ABOUT BRAZIL? cludes compounds that are emetic, vesicant, Brazil has an extremely rich and lush irritating, cardioactive, or neurotoxic (Beren- biosociodiversity, represented both by baum 1995). one of the highest rates of biodiver- Based on the use of insects as a food sity on the planet and a vast cultural source and medicine at the same time, diversity, as there are currently a total Costa Neto &Ramos-Elouduy (2006) of 222 indigenous ethnic groups recog- have postulated the hypothesis of nu- nized by the State (Instituto Socioambi- traceutical entomofauna. According to ental 2005). In addition to indigenous this hypothesis, there are many species people, there are several non-indigenous of insects that are sources of functional populations such as artisanal fishermen, foods also provide improvements du- Amazon ‘caboclos’ (river-dwellers.), ally added health by providing services Afro-Brazilian descendents (‘quilombo- or utility facilities, including prevention las’ communities), and others (Diegues & and treatment of diseases. The practice Arruda 2001). of using insects as nutraceuticals occurs Ethnographic data on the practice of in many parts of the world for individu- entomophagy in Brazil date back to the als in a multitude of ethnic groups with sixteenth century, when the first chroni- different beliefs localized on five con- clers made the first records about the tinents and employs people of all ages nature and indigenous peoples. However, (Ramos-Elorduy 2004; Zimian et al. the number of species of edible in- 2005; Pemberton 2005; Yhoung-Aree & sects in Brazil is undervalued. DeFo- Viwatpanich 2005). Vegetarians in India, liart (2005) only records seven orders, for example, get thaire source of vita- 14 families, 19 genera, and 23 species, min B from insects and bacteria that 12 while Pereira (1974) records 54 species typically contaminate their food (Allport for the Amazon region. Posey (1987a, 2000). Many active compounds of nutra- 1987b) briefly discusses the cultural ceutical insects have been obtained and and ecological implications of insects evaluated pharmacologically (Costa Neto as food and summarizes the use of & Ramos-Elorduy 2006). insects for the indigenous peoples of Indeed, at the time in which insects were Brazil. Bordotti (2001) made an analysis prescribed as therapeutic purposes by of literature data published from 1560 to healers and practitioners of traditional 1999 on the various ways insect diversity medicine, people were familiar with the is used in Neotropical region, including idea of ingestion them (Holt 1988). It is entomophagy. interesting mention that the word medi- Several references provide ample evi- cine owes its origin to the honey, be- dence that many insects were (and still cause the first syllable has the same root are) considered important food for as mead, an alcoholic drink made from Brazilian indigenous groups. In 2006, honeycomb that was often consumed as Costa Neto & Ramos-Elorduy published an elixir (Hogue 1987). a review on the practice, presenting

574 Amazôn., Rev. Antropol. (Online) 5 (3) Especial: 562-582, 2013 Insects as human food the use of insects as food by 39 in- the intestines and consumed them raw digenous groups (Table 1) and urban or cooked (Santos 1957). communities. A total of 135 types of In the northwest Amazon, insects pro- edible insects have been reported in 14 vide approximately 5 to 7 percent of (54%) of the 26 states of the Brazilian total protein intake during the year. territory. These resources are divided Their contribution increases to 12 to into nine orders and 23 families. Only 26 percent during May to June when 95 are identified to species level while availability peaks (Dufour 1987). This 18 are at the genus level, and some are period coincides with the mature stage reported only by their native names. of insects. Sutton (1995) studied gen- Species belong to the Hymenoptera der differences in insect consumption are the most abundant (63%), followed and found that men consumed more in- by those in the order of Coleoptera sects than women, contributing to more with 22 species (16%), and Orthoptera than three times the protein intake. with 9 species (7%). These resources are consumed as immature (nymphs, Ribeiro & Kenhíri (1987) reported the larvae and pupae) and as adult, in part use of seven caterpillars consumed by or whole, as well as products made by the Desâna Indians. The local species them such as honey, propolis, pollen named as bali’i is highly appreciated and wax. In general, people consume not only for its excellent flavor, but edible species depending on their also because it has a gland that secretes presence, abundance and availability. an enzyme that Indians use to remove warts. Larvae can be boiled (after the With the purpose of exemplifying the gland is removed) or prepared by roasting use of insect as food resources, it is them, then grinding them and then mixing described below some native uses in them with salt and dried peppers. the Amazon region. Grasshoppers are important insects in the diet of vari- The Tukuna who live in the Amazon ous indigenous tribes, particularly for basin appreciate the abdomen of red the Nhambiquara from the state of ants (probably Atta sexdens Linnaeus, Rondônia and the Bakairi from the 1758), which is eaten roasted and state of Mato Grosso. For example, mixed with cassava flour. The Sateré- both the nymphs (in the rainy sea- Maué Indians use to eat a paste made son) and adults (in the dry season) with roasted termites and ants in ba- of Rhammatocerus schistocercoides (Rehn) nana leaves (Lenko & Papavero 1996). are collected by the Nhambiquara, In a recent ethnoentomological study, who consume it roasted or as a pow- Petiza (2011) recorded that the Baniwa der (Embrapa 2000). The Mundurucu Indians living in the town of São Gabriel people from Pará State used to col- da Cachoeira, in northwestern Amazon, lect grasshoppers by making holes in still use different insect as food resources, the ground and then pushing them to such as termites (dáane, keétto, maáki, these caves, after that they took away kanaliére), ants (kaiwiri, kadáadali, píite,

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Table 1 Orders of edible insects among the indigenous groups in Brazil. Data from Costa Neto & Ramos-Elorduy (2006). Orders of edible insects Ethnicity ORT ISO BLA ANP COL HOM HYM LEP DIP Amondawa x Araweté x x Ashaninka x Bakairi x Bororo x Botocudo x Cinta Larga x Cocama Enawenê-Nawê x x x Desâna x x x x x Gavião x Guarani (subgrupo M'byá) x x Jamamadi x Kaingang x x x Kayapó x x x Macu x x x x Makuna Matis Mundurucu x x x x x Nhambiquara x x x x x x x Omágua Pancararé x Parakanã x x Sateré-Maué x x Suruí x x x Tapirapé x x Tariano x Timbira x Tucano x x x Tukuna x x Tupinambá x x Tuyuca x Uru-eu-wau-wau x

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Wanana x Xokleng x Xukuru-Kariri x Yanomamo x x Yawalapiti x Zoró x kóowhenai), beetles (móodi, haliére, déeto), human diet (educational campaigns), caterpillars (kadaápali), leafhoppers (tsi- and we should also think of marketing iríto, máami), and crickets (dzíiro). strategies to launch products based on edible species. Methods for mass pro- As Posey (1976) points out, using in- duction of insects in adequate sanitary sects and their products in any quan- conditions should be done in order to tity presupposes a sophisticated folk not depend on the collection of speci- knowledge about these organisms and mens directly from nature. their behavior, which is revealed through the analysis of oral traditions that some- Edible insects are one of the renewable how encompass insects. Indigenous peo- resources that are available for sustainable ples have an intimate knowledge of their exploration to relieve malnutrition and biological environment, since they are ex- hunger in the world. Through selecting pert manipulators of processes and eco- suitable insects for human consump- logical relationships, and tend to adopt tion, Western populations need to re- sustainable management practices. The view their eating habits and consider, role that insects play in any economic sys- in the light of current knowledge, the tem is important, although they represent nutritive potential offered by insects, only a small part of total resources. How- given the large quantity of proteins, fats, ever, due to ethnocentric reasons, since vitamins and minerals they present. The insects are not considered appropriately discovery of a new dish does more for in other cultures, there has been a ten- the happiness of mankind than the dis- dency to ignore or omit their relevance covery of a new star (Boyle 1992). to other cultures. Or, when mentioned, we have only their indigenous or generic names, making it difficult to know which REFERENCES species they belong to. Adamolekum, B., D. W. McCandless, and Considering the rich biosociodiversity R. F. Butterworth. 1997. Epidemic of sea- found in Brazil, it could be stated that sonal ataxia in Nigeria following ingestion of the African silkworm Anaphe venata: entomophagy in the country is much role of thiamine deficiency? Metabolic underestimated, since nutritious edible Brain Disease 12(4):251-258. insects are abundantly available. We must change the idea that insects can Akinnawo, O. O., M. O. Abatan, and A. O. Ketiku. 2002. Toxicological study on the edible not be included as food items of the larva of Cirina forda (Westwood). African

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