Study site

The Lao People’s Demographic Republic (Lao PDR, Laos) is a landlocked, mountainous country where ca. 58% of the country’s area is forest [25]. The northern part of the country is lined with mountains over 1,000 meters high, while the elevation around the Vientiane capital is only about 100 meters. The country is surrounded by Cambodia, China, Myanmar, Thailand, and Vietnam. More than two-thirds of the country’s 7 million people live in rural areas and earn their living mainly through agriculture. The development of the road network and the increase in the number of people owning cars has led to an increase in automobile-mediated exchanges between regions.

We conducted the surveys at food markets located in the Vientiane capital, Vientiane Province, Luang Prabang Province, Oudomxai Province, and Xaignabouri Province in northern Laos (Fig 1). In recent years, foreign investment in infrastructure has increased, and the Vientiane capital is undergoing rapid urbanization [24, 26]. From 1995 to 2015, the built-up area in the Vientiane capital has increased from 3.4% to 12.81% [27]. The plains around the city are covered with rice paddies and marshlands [28]. The southern part of Vientiane Province is dominated by farmlands. In Luang Prabang Province, many people have migrated from rural areas to cities, and urbanization is progress in central cities [29]. The northern part of Luang Prabang Province, Oudomxai Province, and Xaignabouri Province, are mostly mountainous.

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Fig 1. Geographical locations of food markets under observations in Laos.

(a) dry season, (b) rainy season. Red circles indicate markets where at least one species of edible insects was observed. Blue circles indicate markets where no edible insect was observed.

https://doi.org/10.1371/journal.pone.0267307.g001

There is at least one food market in all the towns in Laos [30]. In the food markets, in addition to edible insects, plants, mushrooms, seafood, and meats are also sold [15, 30].

Investigation methods

From September 3^rd to 13^th 2015 (rainy season), we visited 37 food markets. From February 4^th to 13^th 2017 (dry season), we visited 55 food markets. We walked through each market and recorded whether edible insects were sold or not. Sold insects were photographed with a digital camera. The status of the insects at the time of sale (i.e., alive, dead and uncooked, or cooked) was also recorded. Insect species observed for the first time were purchased and specimens were preserved in 95% ethanol. Multiple species of insects were often sold together without sorting on a single plate (Fig 2A); for example, Atractomorpha spp., Acrida sp., Euconocephalus spp., and Locusta migratoria were sold together as "grasshoppers" (Fig 2C). Since the purpose of this study was not to make a detailed list of sold insects, but rather to identify the potential factors that influence the sales of edible insects, we tabulated the data for 23 functional groups, which were often sold together without sorting on a single plate, in reference to previous studies about edible insects in Laos [2, 13]. Latitude, longitude, and elevation of the markets were recorded using GPS. The area of the market was also measured based on aerial photographs from the Laos national forest monitoring system [31]. The area was measured as the entire building area, excluding the parking lot. In addition, as an indicator of urbanization around the market (urbanization index), we drew a circle with a radius of 1 km around the market and visually judged the percentage of buildings occupying the circle, and recorded the results in five levels (0: <10%, 1: 10–30%, 2: 30–50%, 3: 50–70%, 4: 70–100%).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Fig 2. Edible insects observed at food markets in Laos.

(a) Insects are usually classified roughly and sold on one dish. (b) Dragonfly nymphs are sold together with freshwater fish and shrimps. (c) Adults and nymphs of grasshoppers (Atractomorpha sp., Acrida spp., Euconocephalus sp., etc.). (d) Adults of short-tailed crickets (Brachytrupes portentosus). (e) Larvae, pupae, and adults of weaver ants (Oecophylla smaragdina). (f) Larvae of dobsonflies (Family Corydalidae). (g) Fried rhinoceros beetles (Trichogomphus martabani), (h) Dung balls of elephant dung beetle (Heliocopris bucephalus). (i) Fried bamboo caterpillars (Omphisa fuscidentalis).

https://doi.org/10.1371/journal.pone.0267307.g002

Statistical analyses

To determine whether the percentage of markets where edible insects were sold differed between in the dry and rainy seasons, the percentage of markets where one or more insects were sold and the percentage of markets where sales were confirmed for each group of insects were compared using Fisher’s exact probability test. A generalized linear model (GLM) analysis was conducted to determine the potential factors affecting insect sales at food markets. The response variables were whether insects were sold (1/0; binary) or the number of groups of edible insects, and the explanatory variables were the province/capital of the market, urbanization index, elevation, and market area. When the response variable was whether the insects were sold, the error structure was a binomial distribution and the link function was logit. When the response variable was the number of groups of edible insects, the error structure was a Poisson distribution and the link function was log. For each of the dry and rainy season, a total of 24 models were computed and examined for the overall and each insect group’s respective sales. Multicollinearity among explanatory variables was checked based on the VIF statistic; VIF < 10 for each variable in all models, indicating that the effect of multicollinearity was small. Significance was confirmed using the likelihood ratio test. All statistical analyses were performed using R [32] and the package "car" [33].

Seasonality in groups of insects sold at food markets

There was no significant difference in the percentage of markets selling insects between in the dry and rainy seasons; insects were sold in 40–50% of the markets in both seasons. The composition of sold insects differed between in the dry and rainy seasons, which reflects the seasonality and life history of each insect group. In particular, for insect groups that are used as foods on specific life-history stages, such as eggs, larvae, nymphs, pupae, and adults, as food, sales were confirmed only during the seasons when those stages were observed. For example, bamboo caterpillars (O. fuscidentalis) exhibit annual life cycles, with adults emerging in July and August, laying eggs on bamboo shoots in early August, followed by the emergence of larvae [13]. Since only the larvae are edible, their sales were observed only during the rainy season (September 2015) when the larvae can be caught. Similarly, for short-tailed crickets (B. portentosus), rhinoceros beetles (T. martabani), five-horned rhinoceros beetles (E. gracilicornis), and wasps (V. affinis), which exhibit an annual life cycle and have specific developmental stages for food use [13], sales were confirmed only during the rainy season, and sales of weaver ants (O. smaragdina) were confirmed only during the dry season. The seasonality of these sales was consistent with previous studies that examined insect use as food in Laos [13]. In contrast, for aquatic dragonfly nymphs, seasonality of sales was not consistent with the seasonality of insect use as food in Laos described in previous studies; their sales were more often observed during the dry season compared to the rainy season, while previous studies showed that harvesting of dragonfly nymphs occurs throughout the year and the peak of harvesting is during the rainy season [13]. One possible reason for the difference is that during the rainy season, many temporary water places suitable for dragonfly nymphs to habit are formed, and as a result of the ease with which local people can capture them in their immediate surroundings, the demand for them in markets may become lower. This possibility will be tested through interviews with buyers and sellers.

The effects of geographical factors and the urbanization on groups of edible insects sold at food markets

We expected a negative correlation between the urbanization index and the diversity of edible insects sold at markets. However, the findings were the opposite; in the rainy season, there was a positive correlation between the urbanization index and the diversity of edible insects. In addition, in both dry and rainy seasons, there tended to be more groups of insects for sale in the urbanized Vientiane capital than in the other provinces. From these findings, we can point out two suggestions about the effects of urbanization on the sales of edible insects in Laos. First, even in urbanized cities, collectors have access to edible insects. However, it may be becoming more difficult to collect insects than before. Boulidam (2010), who studied the availability of edible insects at markets in the Vientiane capital, reported that the number of collectors was increasing and collectors needed more time to harvest enough amounts of edible insects nowadays [15]. Second, in urban areas, the commercial demand for edible insects of people is high. This may reflect the situation that it is difficult for local people to capture insects by themselves in urban areas. Even in the urbanized Vientiane capital, the percentage of people using insects as food frequently was over 80% [14]. On the other hand, farmlands and forests, which are the main fields for harvesting edible insects [16], have been reclaimed, and the proportion of houses, stores, and factories has been increasing [24], making it difficult to get edible insects in the wild. Furthermore, with the modernization of life, people do not have enough time for wild harvesting [24]. Therefore, the commercial demand for edible insects is likely to be higher in urban areas. In our study, the positive correlation between the urbanization index and insect diversity was found only in the rainy season and not in the dry season. According to an interview survey to sellers [14], 88% of sellers felt that it was more difficult to sell insects during the rainy season than the dry season because it was easier for people to harvest insects by themselves in the rainy season, and they tended to get insects not by purchasing but by wild harvesting. Therefore, the commercial demand of people in urbanized areas may be more evident in the rainy season than in the dry season.

Given that urbanization is expected to continue, the commercial demand for edible insects in the Vientiane capital and other major cities may be even higher in the future. In addition, the FAO’s promotion of edible insects as a source of protein in Laos [13], may also facilitate the demand for insects as foods. The over-harvesting of insects by collectors due to increasing commercial demand in urban areas may reduce the population sizes of edible insects in suburban areas, resulting in either local or total extinction of insects [21]. It will also lead to difficulties in securing food for local people who harvest insects as a subsistence diet. In fact, due to the increase in the number of collectors and the decrease in the forest area, the number of a popular edible insect species, weaver ant (O. smaragdina) has been decreasing, making it difficult for local people to collect them [34]. Considering that insects are a valuable source of protein, vitamins, and minerals for local people, the negative impact of difficulty in collecting edible insects for subsistence use on food security is significant. There are three ways to reduce the chance of decrease and local extinction of edible insects in the wild: 1: managing wild harvesting, 2: farming, and 3: managing consumer experience [21]. In order to effectively manage wild harvesting, it is important to collect scientific knowledge on the ecology of edible insects and traditional ecological knowledge about harvesting edible insects from local people. Local people monitor the development of edible insects to determine the appropriate time and method of harvesting for sustainable use [35, 36]. In Laos, observations on collection practices and semi-structured interviews of local people harvesting weaver ants suggested that they intentionally refrained from collecting the majority of their nests, which led to the maintenance of ant populations [34]. Research on sustainable insect use by local people in Laos is scarce compared to other regions, and further studies are needed. The cultivation of domestic house crickets has recently started in Laos through technology transfer from Thailand [13]. FAO has conducted training courses to teach farmers breeding techniques, insect marketing, and the nutritional values of the major four edible insects (i.e., domestic house crickets, mealworms, palm weevils, and weaver ants) and some farmers are now cultivating these insects [13]. There is a possibility that local insect species such as grasshoppers and other crickets can be cultivated in a similar way to domestic house crickets, and further research is desirable.

Novel use of edible insects in Laos

In this study, to the best of our knowledge, the food use of dobsonflies (Corydalidae) was confirmed for the first time in Laos. In the dry season, larvae of dobsonflies were sold at a market in one mountainous area in Oudomxay province. The larvae of dobsonflies inhabit running water environments and are used as food in mountainous areas in China, Japan, Peru, and Mexico [37]. The use of natural resources for food in mountainous areas has not been fully elucidated, and insects inhabiting unique habitats are likely being used as unknown food. It is desirable to continue field research from a cultural anthropological perspective.

Limitations and future research directions

This study revealed the relationship between seasonal/geographical factors and sales of edible insects at food markets in northern Laos. Some insect species were not found for sale even though they were reported as major edible insect species in Laos (e.g., cicada nymphs; [13]). This could reflect the difference between the insect species that are purchased for sale and those that people harvest by themselves around their homes. However, we should be cautious in interpreting this. Our survey was conducted only once for each market in each season, so we may not have a comprehensive picture of the diversity of insects that are collected and brought in by accident. To understand the relationships between seasonal/geographical factors and sales of edible insects more accurately, it is necessary to conduct surveys over multiple days and hours at a single market.