3.2.6. Order Hymenoptera

Hymenopterans are differentiated as ants, bees, hornets, and wasps. Depending on the species Hymenopterans are available all throughout the year. Ants are mostly available for consumption from May to July; bees, especially *Apis cerana indica* are reared and available in every season, while hornets and wasps are most abundant for consumption from May to February.

Six (6) species of honeybees (Apis cerana indica, Apis dorsata dorsata, Apis dorsata laboriosa, Apis florea, Lepidotrigona arcifera, Lophotrigona canifrons) are commonly used as food in the region. Of all bee species, Apis cerana indica is the most important species as it is commonly available and can be reared or domesticated more easily than the other bee species. All bee stages (larva, pupa, adult) as well as the bees' products are widely used for their food value as well as their medicinal value (Figure 8a,b). Honey is considered to be a strong and effective medical agent for treating cold, conjunctivitis, cough, diarrhoea, and pneumonia.

**Figure 8.** (**Plate 6**). Widely consumed and marketed Hymenopterans; (**a**) *Apis cerana indica* honey comb, (**b**) honeycomb of *Apis florea*, (**c**) wasp nest of *Vespa soror*, (**d**) large nests of *Vespa tropica tropica*, (**e**) fried wasps (*Provespa barthelemyi*), (**f**) nest of giant hornet (*Vespa mandarinia*), (**g**) healthy hornet grubs, (**h**) freshly harvested *Vespa auraria* by smoking method, and (**i**) worker ants *Oecophylla smaragdina*.

Besides bee and bee products, paper wasps (e.g., *Provespa barthelemyi*) and hornets (e.g., *Vespa soror*, *Vespa tropica tropica*, and *Vespa mandarinia*) are important edible insects (Figure 8c–h). Preferences in preparation of wasps (larva, pupa, and adult) depend on one's own taste and the preparation is done by frying or cooking (Figure 8c). The giant hornet (*Vespa mandarinia*) is an important edible species mainly because the grubs are a delicacy, but it is difficult to capture and has a high market value

(Figure 8d). For consumption, the larvae, pupae, and the adult are prepared by frying or cooking with local spices replacing the conventional meat sources (beef, chicken, pork etc.).

Different methods are followed to capture/collect the bees, wasps, and hornets. The common honeybee (*Apis cerana indica*) is collected by smoking. In the process, a piece of cloth is burnt, and the smoke is blown into the bees' nest. The adults fly away and do not return until the smoke disappears. The rock honeybees *Apis dorsata dorsata* and *Apis dorsata laboriosa* are collected in two steps. Firstly, the beehive is pierced to allow honey to drip down; after which the honey is applied on the exposed body areas. This way, although the bees remain on the hive they do not sting the collector and are easily collected. The nest entrance of the underground stingless bee *Lophotrigona canifrons* is very small; therefore, a stick is inserted into the entrance so as to keep track of the nest. The bees' nest and the bee products are then collected by digging the soil away.

Giant hornet of the species *Vespa mandariana* are collected by the meat trap method, but for other hornet species the smoking out method is used [23]. With only its honey balls considered edible, the violet carpenter bee (*Xylocopa violacea*) is preferred by only a few Nagas and is eaten raw. The weaver ant (*Oecophylla smaragdina*), which had its chemical composition analysed by Chakravorty et al. [34], is considered as an important food item by all members of the Naga tribes (Figure 8i). While, the immature stages (eggs, larvae, and pupa) of the ant are boiled or cooked (with local spices) for consumption, the adult ants are prepared as chutney in a mixture of chilly, salt, and dry fish ground to powdered form and are also preserved for longer use.

#### 3.2.7. Order Lepidoptera

Lepidopterans are mostly available for consumption from May to December. However, the eri silkworm (*Samia cynthia ricini*), which is reared widely in the region, is available for consumption throughout the year. The carpenter worm (*Cossus* sp.) with high protein and fat content, total phenol, and total antioxidant content [35] is the most popular and valued edible species, mainly because of its enticing aroma, its high market value, and ethno-medicinal properties. Although, some people prefer the larvae raw, most of the consumers prefer the larvae boiled or cooked with local spices served as a main dish on the menu (Figure 9a). The bamboo larvae (*Omphisa fuscidentalis*) are also an important edible insect that is preferred mainly for its crispness after being fried and eaten as snacks (Figure 9b). With *Omphisa fuscidentalis*, besides cooking or frying of the larvae, the traditional way of steaming is followed by some Nagas. For instance, the larvae (properly mixed with local spices) are wrapped with banana leaves that are then placed under warm ash. After 20–30 min, the packages are taken out and the larvae which are perfectly steamed are eaten as snacks.

The eri silkworm (larva and pupa) is relished by all Naga tribes and is prepared fried or cooked with local spices for consumption (Figure 9c,d). Tent caterpillars (*Malacosoma* sp.) are also a delicacy among the ethnic groups and are cooked or fried for consumption. The caterpillars are handpicked, when collected in plenty; the caterpillars are smoked for future use.

#### 3.2.8. Order Diptera

The only dipteran species consumed, i.e., *Tipula* sp. (larva) is an important edible species and is prepared by boiling or cooking (faeces and gut removed) with local spices and served as a main dish on the menu. The larvae are mostly available for consumption during winter season (September–January).

**Figure 9.** (**Plate 7**). Mode of preparation of important Lepidopterans; (**a**) fried carpenter worms (*Cossus* sp.), (**b**) fried bamboo caterpillars (*Omphisa fuscidentalis*), (**c**) silkworm larvae and pupae cooked with fermented bamboo shoot and local spices, (**d**) fried silkworms.

#### **4. Rearing and Marketing of Edible Insects**

Having a high feed conversion and low feed consumption ratio, coupled with fast production of protein as compared to conventional animal and plant sources [36], rearing of edible insects is found to be more advantageous in providing unconventional protein to humans. While most of the insects documented from Nagaland are collected from the wild, the eri silkworm, muga silkworm (*Antheraea assamensis*), and *Apis cerana indica* are reared for personal consumption as well as for marketing (Figure 10a,c). However, wasps (e.g., *Provespa barthelemyi*) and hornets (*Vespa a*ffi*nis indosinensis*, *Vespa auraria*, *Vespa basalis*, *Vespa bicolor*, *Vespa soror*, *Vespa tropica tropica*, *Vespa mandarinia*, and *Vespula otrbata*) are semi-domesticated. All throughout the year, different kinds of edible insects and insect products are sold in the markets (Figure 10b,c). While most of the edible insect species that are sold in the markets are freshly harvested ones, different honeybee products are now packaged and sold at specialized stores. The Nagaland Beekeeping and Honey Mission (NBHM) set up by the Government of Nagaland implements programs and policies for the promotion and development of beekeeping in the state. NBHM-brand processed honey is commercially available; besides many local entrepreneurs are also putting in an effort to commercialize different bee products of Nagaland. Apart from honey, all the other edible insects documented in the present study are not packaged and cannot be kept for longer durations. Therefore, even though there is potentiality of edible insects to become a staple food, ways for packaging edible insects and increasing their shelf-life to promote them as food nationally and internationally is the need of the hour.

**Figure 10.** (**Plate 8**). Local insect rearing and various marketed edible insects; (**a**) rearing of eri silkworm (*Samia cynthia ricini*) at Socunoma village, Dimapur district, ( ¯ **b**) different species of wood larvae sold at local market, Kohima district, (**c**) a woman selling eri silkworms at local market, Dimapur district, (**d**) sundried termites sold at local market, Mokokchung district, (**e**) sundried grasshoppers sold at local market, Dimapur district, (**f**) smoked tent caterpillars sold at local market, Mokokchung district.

Traditional way of increasing their shelf-life is practiced by the local insect sellers by simply smoking or sun drying the insect species (Figure 10d–f). The traditional method is nothing but minimizing the moisture content of the insect to reduce the rate of deterioration. The pentatomid bug *Udonga montana* that is boiled and further smoked/sundried (maintains its crispness) is also available in the local markets. Boiling and steaming an insect (larva and adult) not only maintains its size and keeps the desired aroma and flavour but also gives a higher score in terms of crispness [37]. Food dehydration is one way for the commercialization of edible insects, while the other way is to turn them into pickles. All over the world, the main concern with edible insect consumption, collection, and marketing is overexploitation. Entomophagy is an age-old practice in Nagaland and the different ethnic groups believe in sustainable utilization of the edible insect species. For instance, while collecting different kinds of bees and wasps, the queen along with some workers is left behind in a brood to enable them

for further development and production. This effort for sustainability has been followed through generations and till today apiculture is successful in the region.

#### **5. Conclusions and Recommendations**

For the different ethnic groups in Nagaland, edible insects are a natural, renewable resource that plays an important role in providing nutrition. Currently, edible insects are mainly harvested from the wild and sometimes from agricultural crops where they occur as pests. However overharvesting edible insects from the wild to supply to the urban market for improving livelihood is not sustainable and is a strain to the rural biodiversity. Therefore, while edible insects have the potential to improve rural livelihood, semi-cultivation and farming of insects has to be seen as a priority. Looking into the Indian scenario, Nagaland has the potentiality of commercializing insects as a bio-resource. At present, only bees (especially *Apis cerana indica*), eri silkworm, and muga silkworm are mass produced in Nagaland. However, besides the mentioned three edible insects, there are groups of insects e.g., crickets, giant water bug, water beetles, palm weevil larvae, grasshoppers, etc. that are successfully reared in other parts of the world [38,39]. Nagaland harbours large number of edible insects such as aquatic bugs and beetles (*Cybister limbatus*, *Cybister tripunctatus lateralis*, *Lethoceruus indicus*, *Hydrophilus cashmirensis*) bees (*Apis cerana indica*, *Apis dorsata dorsata*, *Apis dorsata laboriosa*, etc.), crickets (*Tarbinskiellus orientalis*, *Tarbinskiellus portentosus*, *Teleogryllus occipitalis*), grasshoppers (*Oxya fuscovittata* and *Oxya hyla*), palm weevil (*Rhynchophorus ferrugineus*) and wasps (*Vespa mandarinia*, *Vespa soror*, *Vespa tropica tropica*, *Vespula orbata*, etc.), which have the potential for mass production in the region.

A study undertaken by the International Livestock Research Institute (ILRI), reported an increasing demand for livestock products and the present state production is not enough to feed the growing population. As per sample survey report of 2017–2018, the state produced 45.23% of total requirement of livestock worth 1206.15 crore Indian rupees but leaving a shortfall of 54.77%. Out of this shortfall, the state imported animal husbandry products worth 212.05 crore Indian rupees in monetary terms. In the backdrop of the growing demand for meat and the declining availability of agricultural land in the state, edible insects could be the alternative source of protein. Therefore, the present study, not only raises awareness among the tribal communities but also develops deep interest amongst policy makers and stake holders of the potential growth of the edible insect sector and thereby to promote funding into edible insect research and development. We believe that mass production, proper commercialization, and marketing strategies can improve livelihoods of tribal communities (especially the womenfolk) living in remote villages.

**Supplementary Materials:** The following are available online at http://www.mdpi.com/2304-8158/9/7/852/s1, Supplementary Material S1: Questionnaire format.

**Author Contributions:** Conceptualization, L.M. and L.N.K.; methodology, L.M., L.N.K., P.K., and S.C.; validation, L.N.K. and S.C.; formal analysis, L.M.; investigation, L.M., L.N.K., P.K., and S.C.; resources, L.M., P.K., and S.C.; data curation: L.M., L.N.K., and S.C.; writing—original draft preparation, L.M.; writing—review and editing, L.N.K. and S.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Acknowledgments:** The authors would like to acknowledge the field guides, local interpreters, and the different ethnic groups without whom the study would not have been possible. Lobeno Mozhui would like to thank National Fellowship for Higher Education of Scheduled Tribe Students (NFST) for financial assistance to pursue Ph.D.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


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