**1. Introduction**

The world population is estimated to reach 9.8 billion by 2050 with a globally expected increase of 76% in the demand for animal protein [1]. Livestock production worldwide accounts for 70% of the agricultural land and, with the growing demand for meat and the declining availability of agricultural land, there is an urgent need to find additional or alternative sources of protein to provide for the increasing global population. Humans have harvested the eggs, larvae, pupae, and adults of certain insect species from the forest or other suitable habitats for thousands of years as part of regular diets, to stave off famine, to use therapeutically for medicinal and ritual purposes [2], and to try them as novelties [3]. The workshop in Chiang Mai (Thailand) in 2008 on "*Forest insects as food: humans bite back*" [4] emphasized edible insects as a natural food resource. To combat future food insecurity and to develop insects for food and feed, as first suggested by Meyer-Rochow [5], is now considered a viable strategy [6,7]. Insects may have originally been used as a snack or an emergency food item, but even today over 2100 known species of edible insects are still consumed by millions of people of 3071 ethnic groups in 130 countries [8–11]. Entomophagy is advocated as a source to combat future food insecurity mainly because of the insects' abundance, high nutrient composition, high feed conversion efficiency, digestibility, and ease with which they can be bred [6,7,12–14]. Edible insects' nutrient profiles are often very favourable with regard to dietary reference values and daily requirements for normal human

growth and health. In marginalized societies, insect consumption has often bridged the gap between the availability and non-availability of conventional food items.

Nagaland is bestowed with natural resources and rich biodiversity supporting various plants and animals including a variety of insects associated with its natural vegetation. While conventional sources of animal-based protein are not always affordable to the rural people and also take a long time to become available, many insects are consumed as an alternative source of protein and as delicacies. The use of insects as food by the Nagas goes way back to those times when they were still called the "Naked people". Insects such as beetles, dragonflies, grubs of white ant, grasshoppers, locusts, crickets, stink bugs, grubs of all sorts of bees and wasps, bee comb, and honey were used as food and played an important role in the diet of the different ethnic groups [15–18]. Most of the studies on entomophagy reported so far from Nagaland [19–22] are preliminary in nature and are restricted to a few insect species available in certain geographical areas of Nagaland. The present study is an extension of an earlier investigation in seven tribal communities of Nagaland by Mozhui et al. [23], providing a more detailed inventory and further documentation of the traditional knowledge of using edible insects as a promising and alternative food source for Nagaland.

### **2. Materials and Methods**

#### *2.1. Study Area*

Nagaland is a state located in the north-eastern part of India covering an area of 16,579 km2. It is situated at 93◦20 –95◦15 E and 25◦6 –27◦4 N, in the confluence of East Asia, South Asia, and Southeast Asia. Considered one of the biodiversity hotspots (within the Indo-Burma region) of the world, the state has unique geographical location and varied altitudinal range. Out of the total geographical area, 85.43% (14,164 km2) constitutes the forest cover, of which 5137 km2 is dense and 9027 km2 is open forest [24]. Agriculture is the main economy of the state, which includes not only crop raising but all other allied activities such as animal rearing i.e., poultry, horticulture, pisciculture, sericulture, silviculture, livestock i.e., dairy cattle (buffalo, cow, mithun), goats, pigs, etc. Two types of farming systems—jhum or shifting cultivation and terrace or wet cultivation are practiced by the ethnic groups. Jhum cultivation is an extensive method of farming in which the farmers rotate land rather than crops to sustain livelihood [25]. Areas of jhum land are cleared once in five to eight years for better crop production. While in terrace cultivation, the entire hillside is cut into terraces and irrigated by a network of water channels that flows down from one terrace to the other and is easier to maintain than the jhum plots. However, due to the state's wide altitudinal variation, terrace cultivation is found only in some rural pockets and majority of the population are engaged in shifting cultivation. Rice is the dominant crop and the main staple food of the Nagas.

#### *2.2. Data Collection*

The documentation is based on a four year field survey from 2014 to 2018 across 53 villages in Nagaland (Figure 1). The methodology followed in this study for data collection and insect identification is similar to that described in detail by Mozhui et al. [23]. Prior to survey, village heads were informed in advance for selection of informants for authentic documentation. Therefore, from each village, 6–8 informants comprising of village heads, traditional knowledge holders, edible insect farmers, edible insect collectors, educated youths, and homemakers were selected for the study. The survey was conducted only after getting ethical clearance from the village heads as well as the informants. Among the 370 informants interviewed, 248 were male and 122 were female, all belonging to the age group 25–104 years (Table 1). The documentation of edible insects in the present study is based on the responses collected from the informants with the help of a semi-structured questionnaire (See Supplementary Material S1). Informants were asked questions on the stages of edible insect consumption, mode of preparation of the insect species, seasonal availability, and preferences for

selecting insect species for consumption. All the voucher specimens and photographs of edible insects are deposited at Department of Zoology, Nagaland University, Lumami, Nagaland.


**Table 1.** Demographic patterns of informants in the study area.

#### **3. Results and Discussion**

#### *3.1. Edible Insects in Nagaland*

The present study contains an inventory of 106 insect species including 82 edible insect species recorded in our earlier work [23] that are regarded as health foods by the ethnic groups in Nagaland (Table 2). Belonging to 32 families and 9 orders, the percentage contribution of 106 edible insect species is: 24% Hymenoptera, 24% Orthoptera, 21% Hemiptera, 13% Coleoptera, 7% Odonata, 7% Lepidoptera, 2% Mantodea, 1% Isoptera, and 1% Diptera (Figure 2). Photographs of certain most frequently abundant and preferred species are depicted in Figure 3.

**Table 2.** Insect species utilized as food by different ethnic groups in Nagaland (adapted from Mozhui et al., 2017) with new addition of 24 species (\*).



**Table 2.** *Cont*.

B—boiled; C—cooked; CH—chutney; F—fried; R—raw; RO—roasted; ST—steamed; TO—toasted. \* New addition of edible insect in Nagaland. \*\* New record from India, worker wasp examined, regd. no. ZSI/WGRC/I.R-INV.8972 (P. Girish Kumar and James M. Carpenter, 2018).

#### *3.2. Consumption of Edible Insects*

In Nagaland, as elsewhere [26,27] preferences in edible insect consumption are mainly due to six reasons: (a) availability of the insect species, (b) size of the insects, as generally larger insects are preferred for consumption, (c) taboos associated with the insect species, (d) one's own palatability/taste preference, (e) market value of the insect species and, (f) traditional ethno-medicinal knowledge associated with the insect species. With the advancement in technology and availability of western foods, entomophagy practices are discontinued by the locals in many parts of the world [28] in the false belief that they would be more readily accepted as civilized and cultured individuals by representatives of the western world [5]. There are also risks that the cultural and ecological knowledge of entomophagy may get lost while adopting western dietary patterns [7]. However, in Nagaland, even though tribal people are exposed to modern food stuffs, edible insects are still acknowledged and continue to be an important food source providing nutrition and income especially to the rural poor.

**Figure 2.** Percentage contribution of edible insects by each insect order.

**Figure 3.** (**Plate 1**). Certain popular edible insect species of Nagaland. (**a**) Dragon nymphs, (**b**) various aquatic insects, (**c**) katydid *Mecopoda elongata*, (**d**) the sand cricket (*Schizodactylus monstrosus*), (**e**) the dinorid bug *Coridius singhalanus*, (**f**) the red pumpkin bug *Coridius janus*, (**g**) sundried pentatomid bug *Udonga montana*, (**h**) the chrysomelid beetle *Aplosonyx chalybaeus* larvae, and, (**i**) large unidentified wood larvae.

People living in rural areas know very well which species to collect for consumption and this knowledge is acquired by their children, as in other countries with a tradition of consuming insects [29]. It is important to note that edible insects are not only an important source of protein but have ecological advantages over meat [30] and simultaneously aid in maintaining the diversity of habitats for other life forms by sustaining the local environment. The reported benefits of the human consumption of insects as an alternative to conventional food animals are numerous, including comparable levels of protein coupled with lower environmental impact due to lower emissions of greenhouse gases and lower land requirements during production [31,32]. Further, collection of edible insects (those considered as pests) for human consumption has a positive impact on the agricultural crops, being an alternative and efficient biological control method. Thus, consumption coupled with conservation of edible insects can benefit people as well as nature in an area and lead to a sustained use of this important bio-resource [33]. While the use value of different insect species has demonstrated that every Naga tribe has a preference of its own with regard to insect consumption [23], members of the Naga tribes are very specific with the way an insect is prepared for consumption such as boiling in a little amount of water (boiled), cooking with local spices/local ingredients (cooked), frying in hot oil (fried), cooking over fire or over hot charcoal (roasted), as chutney, or eaten raw. Local spices (garlic, ginger), fermented bamboo shoot, dried bamboo shoot, powdered fruits of *Rhus semialata* (Murray) are important local ingredients for preparation. Depending on one's own palatability, the mentioned ingredients are added to enhance the flavour of the insect food, be it as main dish or replacement of conventional meat sources (e.g., beef, chicken, pork). Modes of consumption and preparation of different insects belonging to the nine orders are discussed below.

#### 3.2.1. Order Odonata

Although both adult and nymphal stages of dragonflies are consumed, the nymphs are greatly preferred (Figure 3a). Adult dragonflies are collected in large quantities during the months of July–October, while nymphs are collected mostly during the winter season (December–March). For consumption purpose, the dragon nymphs are prepared by boiling in a little amount of water and cooked until dry, while the adults (wings are removed) are fried and eaten as snacks.

#### 3.2.2. Order Orthoptera

Orthopterans are broadly grouped into (a) grasshopper and katydids, and (b) crickets.

#### Grasshoppers and Katydids

The Nagas are agriculturalist and look after extensive farmlands, where varieties of locusts and grasshoppers are commonly available. During harvest season (September–October), important edible insect species such as *Melanoplus bivittatus*, *Elimaea securigera*, *Hieroglyphus banian*, *Oxya fuscovittata* (Figure 4a), and *Oxya hyla* are collected in large quantities. The harvested surplus grasshoppers are sundried or smoked and preserved for future use. Grasshoppers are prepared as fried or are cooked with local spices (Figure 4b), while giant katydids (e.g., *Mecopoda nipponensis*, *Mecopoda elongata*, and *Pseudophyllus titan*) are roasted/toasted and eaten as snacks (Figure 4c). Some members of Naga tribe regard *Elimaea securigera* as a "health food" and prepare the insects as cooked or fried to be served as the main dish, replacing conventional meat sources (for e.g., beef, chicken, and pork).

**Figure 4.** (**Plate 2**). Commonly utilized Orthopterans; (**a**) freshly harvested grasshoppers (*Oxya fuscovittata*), (**b**) grasshoppers cooked with fermented bamboo shoot, (**c**) roasted giant katydid (*Pseudophyllus titan*).

### Crickets

Crickets are commonly available from August to November and are generally handpicked or captured by various methods. For instance, field crickets (e.g., *Tarbinskiellus orientalis* and *Tarbinskiellus portentosus*) are dug out after pouring water inside their burrow making them float on the surface. The burrow of the cricket is easily recognisable, as they leave a mound of loose soil at the top of the burrow. Generally, a long stick is put in into the hole so as to keep track of the burrow; after which, the soil is removed slowly and the crickets residing in the burrow are collected. Other crickets such as *Acheta domesticus* and *Teleogryllus occipitalis* are light trapped and collected in large numbers at night. People also spread wheat bran along the paddy fields where crickets are most available. The crickets get attracted to the wheat bran and when they come to feed on it, they are either handpicked or trapped with nets. Crickets are generally preferred in cooked form (with bamboo shoots and local spices). However, some prefer them deep fried or boiled (Figure 5a–c). Besides cooking or frying, the traditional way of preparing crickets such as *Tarbinskiellus orientalis*, *Tarbinskiellus portentosus*, and *Teleogryllus occipitalis* are followed by some members of the Naga tribes. For example, the insects may be properly mixed with salt and dry bamboo shoot, stuffed inside cut bamboo pipes (approximately 30 cm in length) and closed with a banana leaf (the use of banana leaf is to enhance the flavour). The bamboo pipe is placed under the fire, and after 20–30 min the dish prepared is served as the main dish replacing the conventional meat sources.

**Figure 5.** (**Plate 3**). Preferences in preparation of important cricket species; (**a**) crickets cooked in fresh bamboo shoot, a delightful delicacy, (**b**) fried crickets, a much sought after delicacy, (**c**) boiled cave crickets for consumption.

#### 3.2.3. Order Mantodea and Isoptera

Although, the mantises (*Tenodera sinensis* and *Hierodula coarctata*) are consumed by only some members, the preferred way for consumption is toasting and they are eaten as snacks. Besides toasting, the head and the digestive tract are removed before preparation and then the insects are cooked with local spices until dry. Termite (*Macrotermes* sp. and *Odontotermes* sp.) are popular edible insect species of the Nagas with a high fat content [34] and are collected in plenty during the months of March–May and November–December. While some consumers prefer boiled termites, most prefer cooked or fried termites. When termites are collected in large quantities, they are sun dried to preserve them for longer use.

#### 3.2.4. Order Hemiptera

#### Stinkbugs

Depending on the species, stink bugs are available all throughout the year. For instance, the most preferred stink bugs such as *Coridius janus*, *Coridius singhalanus*, *Darthula hardwickii*, *Tessaratoma javanica*, and *Udonga montana* are found during the months of May–November. Stink bugs are mostly handpicked during the daytime. The red pumpkin stink bug *Coridius janus* (Fabr.) completes its developmental stages on its host plant (*Cucurbita moschata* Dutch) and is easily handpicked for consumption. They are also available on different bean plants such as string bean: *Phaseolus vulgaris* L.; cowpeas such as *Vigna sinensis* (Savi), *Vigna unguiculata* L.; and Goa bean: *Psophocarpus tetragonolobus* DC, etc.

Most of the stink bugs are preferred in their adult stage; however, the leafhopper (*Darthula hardwickii*) is preferred in its nymphal stage. Preference for consuming only the nymphal stage of *Darthula hardwickii* is mainly because of two reasons: (a) the nymphs are tastier than the adults and, (b) the strong pungent smell of the leafhopper once it gets matured is disliked. While the pentatomid bug *Eurostus grossipes* and the tessaratomid bug *Tessaratoma javanica* are preferred roasted, *Aspongopus nepalensis*, *Coridius janus*, *Coridius chinensis*, and *Coridius singhalanus* are preferred as chutney or cooked for consumption (Figure 6a). With *Udonga montana*, the freshly harvested insects are first boiled (boiling is done to reduce the strong pungent smell), and only then further prepared (with local spices and filtrate of fresh bamboo shoots) as chutney or fried for consumption (Figure 6b). During the month of April and May, *Udonga montana* species are collected in large quantities and people boil the insect and sun dry or smoke them for longer use.

**Figure 6.** (**Plate 4**). Mode of preparation of various hemipterans: (**a**) roasted stink bugs (*Coridius singhalanus*), (**b**) fried pentatomid bug (*Udonga montana*), (**c**) fried giant water bugs (*Lethocerus indicus*), (**d**) boiled water scorpions (*Laccotrephes ruber*).
