Background

Lepidoptera is one of the richest Insecta orders. Their larvae serve as food for many ethnic groups around the world [1, 2]; they are often prepared charcoaled in salty water or, in some cases, fried or mixed with other food [3]. Also contribute a great amount of energy and protein to indigenous diet [4]. In general, this reflects their availability. In the forests of the Central African Republic, some species are so abundant, that when they are in the last larval stage, their excrement fall sounding like heavy raindrops, and two months later, the soil becomes white due to the mycelium that develops [Ramos-Elorduy J, Personal observations, 1990].

The inhabitants make good use of them, storing and selling. This help the people to obtain income that is necessary in a subsistence economy. Ancient Mexicans were traded larvae of Pantherodes pardalaria and Aegiale hesperiaris [5]. Peasants know very well when and where is the biggest and tasty larval stage. People even make long journeys to obtain them; however, because of an over-exploitation, as in Zambia happened, establish a law to enforce a closed season, to prevent extinction of Gynanisa maja and Gonimbrasia belina named "mumpa" [6], exploiting it in a rational way to balance preservation and exploitation [7].

The use of insects as food by the different ethnia of Mexico is a very complete study at Mexico that achieve 549 species [8]. We have documented 14 orders of the Insecta Class, including Lepidoptera.

A study of the edible species of Lepidoptera in Mexico has not yet been accomplished.

Methods

Field

Field work was conducted in 17 states of Mexico, including in 235 localities in: Chiapas (16), Chihuahua (2), Distrito Federal (22), Durango (1), Guanajuato (2) Guerrero (8), Hidalgo (64) State of México (51), Michoacán (5), Oaxaca (16), Puebla (17), Querétaro (1), Quintana Roo (2), Tlaxcala (15), Veracruz (10), Yucatán (1) and Zacatecas (2).

Emic-type interviews with an ethicist focus took place [9]; meetings were in rural areas, small towns, villages and cities. Their goal was to investigate the tracking, gathering, fixing and commercialization.

For collected, we use aerial nets, paint-brushes, knives or "machetes" and some by hand.

The larvae and pupal stages were placed in 70% alcohol solution or on dry ice if they were intended for chemical analysis. Adults were placed in potassium cyanide with plaster and then put in glassed paper envelopes labeled with the data.

Laboratory

For identification, adults were placed in a humid camera and mounted; after labeled, identified and catalogued. Forward were placed in the National Collection of Edible Insects of Mexico kept in the Institute of Biology, UNAM. The immature stages were placed in Khale Liquid for preservation. For identification, keys were used [10–17]. Our determinations were ratified by several specialists. With this information, the corresponding tables were elaborated.

The identification of hosts and the ecosystems was accomplished using different sources: De Vries [18], Martínez [19] and Rzedowski [20].

Results and Discussion

Diversity and ethnicity

We identified 67 species of Lepidoptera as being eaten in Mexico, in Table 1 shows family, subfamily, scientific name, places of consumption, developmental stage or stages consumed, common name, principal ethnia that use them as food, hosts, and principal ecosystems where they were localized.

Table 1 TAXONOMY
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The 13 families are in decreasing order of species number: Saturnidae (16), Pieridae (11), Noctuidae (9), Nymphalidae (8), Sphingidae (4), Arctiidae (4), Hepialidae (3), Hesperidae, Papilionidae and Geometridae (2) each one, Cossidae, Pyralidae, Sesiidae, Castniidae, Bombycidae, and Lasiocampidae (1) each one (Table 2, Figure 1).

Table 2 Families and species number.
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Figure 1
figure 1

Species Number by families of Edible Lepidoptera, Mexico

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The species number in each genus is indicated in figure 2. It can be seen that most of the genera have only one species included (68.75%), followed by the bispecific (18.75%) and at the end trispecific genera (12.5%).

Figure 2
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Species number of edible Lepidoptera in Mexico.

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The most represented genera were Phassus, Phoebis, Hylesia, and Spodoptera (Table 3).

Table 3 Genus and species number.
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Lepidoptera are eaten in 85.41% as larvae, 8.33% as larvae and pupae and in 6.25% as adults.

We found 29 ethnic groups that consume Lepidoptera in Mexico: Amuzgo, Chatinos, Chinantecos, Cholos, Huasteco, Huaves, Lacandones, Matlazinca, Maya, Mazahua, Mazatecas, Mixes, Mixtec, Nahuatl, Otomi, Otopame, Popolucas, Tarahumara, Tarascan, Tepehuano, Tlapaneco, Totonaco, Tojolabal, Triques, Tzeltal, Tzotzil, Yutoazteca, Zapotec and Zoques.

Geographic Distribution

These Lepidoptera species were found in those states of the central, south and southeast regions of the country. The highest number of species (22) was recorded in the eastern part of Veracruz, followed by Hidalgo (17), Distrito Federal (the capital) (16), and Chiapas and Puebla (12 species each). The remaining states, each one had six or fewer edible species.

With regard to the ecosystems [20], these species are attached from the pine oak forest, to the savannah and palmar. The Lepidoptera are also present in several agronomic plants, such as maize, alfalfa, cabbage and cauliflower, depending on the species.

Anthropolarvifagia of Lepidoptera in the World

Bergier [21] reports 15 species for the world, for America only one species Hesperiaris sp., in two countries. Taylor [22] registered 25 species in 12 families. Silow [23] describes 42 species of the genera Gonimbrasia, Imbrasia, Bunaea, Bunaeopsis, Cirina, Pseudantheraea, Micragone, Olocerina, and Melanocera, 33 of them are eaten in Zambia. It is important to mention that all these authors only did bibliographic research. In contrast, Malaisse and Parent [24] performed long-term field work studying Meridian Shaba area in Republic of Congo and in Zambia reporting 37 species (70% classified) and Latham [25] in Low-Congo, documented 31 species (77% classified). In both studies, the principal families were Attacidae and Notodontidae. Banjo et al. [26] reported six species in Nigeria, four of Anaphe genus. Oliveira et al. [27] also reported four species eaten in Angola. We note that six references are books and almost all refer to Africa.

Wen [28] in China presented 66 species, 20 genera and 17 families; 36 species of Hepialus genus. Mitsuhashi [29] reported five species in Japan.

Paoletti et al. [30] noted that larvae of Castniidae, Noctuidae and Sphingidae families are consumed in the Amazon area. Our report has 67 species occurring in just a part of the country.

Rural Nutritional Importance

For rural peasants, the big diversity that Edible Lepidoptera has, besides the good nutritive value achieve (18-57% proteins, 7-77% fats, 0.7-8% minerals, 0.8-25% carbohydrates and 3-29% crude fiber, 231-777 kcal/100 g, [4], and their good flavor that gives their fats, united to the abundance of their populations, conspicuity of their specimens (latest larval stage) that save various important nutrients as proteins and the numerous muscles they posses, combined with their quick preparation (only roasted or boiled), and their innocuity, the easiness to store, make of them an item very searched plus their versability of fix make the Lepidopterans a suitable food, for helping people to have a good health and satisfaction of energy and proteins requirements.

Marketing and Gastronomy

The trade of Lepidoptera larvae still persist being sold in markets in several areas of the country and even at the capital, as the red and white agave worms. In five forks restaurants of Mexico City. These species are in great demand, in large part due to their exquisite flavor, though the eating of these worms is also an ancestral tradition and a signal of power in diverse sectors of the population. Due to the high demand for these species, some sellers of them have special refrigerators for freezing and storing them. In this way, they can offer and prepare them at high prices after the collecting season.

There are other genera, such as Phassus, for which people search laboriously, it has a very similar flavor to chicken, while Laniifera cyclades "nopal worm" has a flavor of a fried potato. In the humid-tropical areas, "cuetla" and "cuecla" larvae, corresponding to Latebraria amphipyroides and Arsenura armida are pickled to give the larvae a flavor similar to herring, while the Spodoptera spp. is similar to that of corn (Table 4).

Table 4 Genus and Species most consummed in México.
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Unfortunately, these organisms are the subject of massive gathering in several of the States of Mexico, where they are profusely eaten. Thus, they could be in danger of extinction, due to the lack of rules regarding their collection, distribution and commercialization [31].

Cultures and Proto-cultures

In Mexico, some Lepidoptera are raised. Leptophobia aripa elodia, Pieris brassicae also the silk worm Bombyx mori in the States of Oaxaca and San Luis Potosí. Their industrial management is widely known, because of their economical importance in China, Japan, India, France, and Italy.

Eucheira socialis socialis the green worm of the Huasteca region widely distributed has larvae that are located inside a secreted silk enclosure of papyraceous consistency. The larvae hang on the branches of Arbutus xalapensis, feeding on young leaves [32]. In some parts of it, people make a "protoculture" that maintain on the edges of their house roof. They hang at least three silk enclosures (each bag contains only one sex), if they do that, the protoculture will survive. In the zone of the Oaxaqueña Mixteca, specially in the towns of Santa María Nduayaco and Santiago Apoala, this species disappeared due to the great degree of consumption; this species has since been reintroduced from Durango and Mexico states [33].

Some ethnobiological studies have been conducted on the red and white agave worms [34]. We investigate on their biology, ecology, and ethology, to increase their production by optimization of their culture particularly in Santo Tomàs, Montecillo, and Apan in the State of Hidalgo and in the laboratory [35, 36] with this we developed the biotechnology that would allow their culture on a greater scale. In fact, this technology for such cultures can be purchased in the Intelectual Property Direction of the UNAM [37]. Also, studies have been conducted to characterize the development of the larvae of the red agave worm [38].

Sustainable Management

The management and conservation of the species Paradirphia fumosa has been implemented in Mexico at the Biosphere Reserve of Tehuacán-Cuicatlán [39, 40].

In this aspect we must also recognize the deep knowledge that indigenous people all over the world have, as they possess 90% of the planet's germplasm [41, 42] because they have maintained a high degree of sustainability with the majority of their resources.

Biomass obtention

These species are recollected by their abundance, because in some ones their recollection could be measure in tons [43] as it happens today with Ascalapha odorata or Latebraria amphypirioides stored in big cotton sacs of 50 kg and offered in market day or in a "tianguis" (market of little towns). Other species they could also sell alive while they are inside a little sac that they build in silk form their nests, as it is in gregarious species, Eucheira socialis or Hylesia frigida. Other species are captured by the use of net as is Phoebis agarithe, or the "monarch butterfly" (Danaus plexipus plexipus, D. gilippus thersippus) or Pterourus multicaudata multicaudata where people do not eat the larvae because this makes the heart stop, but adults. In other species they could be found many individuals together inside their hosts as in Comadia redtenbacheri or Laniifera cyclades, with the help of a hunting knife or even collected the prepupa digging the soil around.

Preparation

Generally is the larvae that are eaten. They are prepared roasted with salt, and in populations with a higher economic purchase they are fried with oil or lard joining always pepper, salt, in tortillas (maize crepes). They could be boiled and roasted in a "pan" or justly fried with salt and pepper, wormseed leaves. Also, boiled split into longitudinale axis, mixed with oil. Boiled, drained and stuffed with fresh cheese, or it could be with tuna or cooked with eggs, like an omelette. Also in a pie accompanied or mixed with rice, as are the shrimps in the "paella" transfering to rice a very special and good flavour.

They could be preserved in brine, and cutted into small pieces in the same way as used crouttons or bacon.

The flavours are really peculiar and it is dificult to compare with something known, but we can said they varied from light delicious flavours to strong and different unkown flavours.

Peasants qualified them as a very good and nutritious "worms", ¡pure vitamine!, to refer to the quantity of proteins they lodged.

Trade and Marketing Nets

Many species are traded and sell by fits or sardine cans. Another way to sell them is already boiled in salt water or preserved in brine. Generally, they are not offer in fixed places in trough the market, but street sellers are walking in different corridors of these, asking people to buy them, by example Comadia redtenbacheri, Aegiale hesperiaris, Arsenura armida, Ascalapha odorata, and Latebraria amphipyroides are sold on the plaza days, market days, in ambulant markets or on roadsides and even in the Mexico City market. They are offered in big plastic boxes or baskets and are measured in tuna or sardine cans, or frequently in "cazuelitas" (little ceramic dishes of different sizes). Some of the recorded edible Lepidoptera thus clearly constitute an important part of the nutrition and economy of the Mexican people [33, 34], particularly for the indigenous collectors, middlemen, distributors, salesmen, and restaurant owners. In addition, canned white agave worms are exported to the United States and Canada by the enterprises Clemente Jacques and Elan, S.A., and thus generate foreign income for Mexico. This worm has been sold for $250.00 USD per kilogram (2006), which is ten times more expensive than a fish or beef fillet. The exported cans cost $50.00 Canadian dollars; these cans contain only 5 or 6 larvae of the last or penultimate larval stage.

Other species have also been commercialized, such as "zacamiches", Hemileuca sp. at Toluca market, "gusanillo", Phassus triangularis, and P. trajesa at different markets in the Veracruz State and "cuchama" (Paradirphia fumosa) in Tehuacán, Puebla.

A little more than 10% (8 species) of edible Lepidoptera larvae are commercialized, but many more species are sold in the adult stage at very high prices.

Some African species in the larval stage are preserved by pickling and are then exported to European cities. In Paris, France, for example, they are offered in the market of La Rue Moufetard in the Latin neighborhood. These are sold in huge fiber baskets, and can be seen in the street markets in several localities for sale on different days of the week. They are mostly bought by immigrants in those countries [32].

Some examples of Edible Lepidoptera of Mexico are Figures 3, 4,5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17 and 18.

Figure 3
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Comadia redtenbacheri (♂)

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Figure 4
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Castnia synpalamides chelone (♂)

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Figure 5
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Aegiale hesperiaris

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Figure 6
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Protographium philolaus philolaus (♂)

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Figure 7
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Phoebis agarithe agarithe (♂)

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Figure 8
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Eucheira socialis socialis (♀).

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Figure 9
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Catasticta teutila teutila (♂)

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Figure 10
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Catasticta teutila teutila (♀)

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Figure 11
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Danaus gilippus thersippus (♀)

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Figure 12
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Arsenura armida (♂)

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Figure 13
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Actias luna (♂)

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Figure 14
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Cocytius antaeus (♂)

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Figure 15
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Ascalapha odorata (♂)

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Figure 16
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Elysius superba (♂)

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Figure 17
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Amastus ochreaceator (♂)

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Figure 18
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Estigmene acrea (♂)

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Authors' information

Dra. Julieta Ramos-Elorduy: has the highest position as researcher at the Institute of Biology of the National University of Mexico and professor of postgraduate courses at the Faculty of Science of the same University. She have 104 scientific publications and four books published. 1153 cites of its publications and 1316 on internet. She lead 152 thesis and publish 289 divulgation articles.

M.en C. José Manuel Pino Moreno: Biologist and M.Sc. by the Faculty of Science of the UNAM (National University of Mexico), Academic Technical of the Institute of Biology and Professor of the Faculty of Sciences both of the UNAM. He has published like co-author several articles about antropoentomophagy and medicinal insects and one book.

Adolfo Ibarra Vázquez. Technical Lepidoptera collection of the Institute of Biology of the UNAM.

M en C. Ivonne Landero Torres. Biologist and M.Sc. by the University of Veracruz, Urban Management and Promotion, Professor of the Faculty of Biology, Cordoba. She has published like co-author several articles about anthropoentophagy.

Héctor Oliva-Rivera. Biologist and M.Scy by the University of Veracruz, Plant Taxonomy Professor of the Faculty of Biology, Cordoba.

Biologist Victor Hugo Martínez Camacho by the Faculty of Science of the UNAM (National University of Mexico), he has published like co-author one chapter of book and several articles of edible insects.