From Thai to Zai: Insects as Example of Threatened Nature-Based Solutions for Sustainable Food Production

Our societies must face many dramatic environmental challenges, some of which are directly linked with the way we produce and consume or indirectly with the climate change and its consequences on ecosystems and the preservation of biodiversity [1,2]. Tropical and subtropical regions are on the front line of this battle because they host most of the human population and most of the biodiversity. In this part of the world, the destruction of natural habitats for agriculture and urbanization is recurrent and very rapid while the current trend does not suggest a slowdown in the coming years [2]. Together with climate change, this loss in natural habitats and the intensification of agricultural practices are associated with major declines in biodiversity, especially in a decrease in insect biomass and diversity [2-4]. As reported by the Global Assessment on Biodiversity and Ecosystem Services, the preservation of biodiversity and human wellbeing are intertwined and there is a need to better understand all the services that can be provided by biodiversity [5]. Insects represent most of the known biodiversity on Earth and provide both services and disservices to human populations across the world [6]. Although most of the research on insects has focused on their negative impacts (e.g., as pests and vectors of human and livestock diseases and enemies of crops and vegetation), their beneficial effects on numerous key ecological functions, and therefore sustainable development goals, including those associated with the sustainable production of food, have become widely recognized [6-8]. Here, we review some of the most recent progress that has been made on understanding the positive impact of insects on sustainable food production for humans. Because the importance of insects as pollinators [8] producers of honey and regulators of pests (often other insects) [9] has been largely studied for years, this article focuses on two research topics that have emerged in recent years: entomophagy, or the consumption of insects as food for humans and feed for other animals, and the beneficial impact of bioturbation by insects on soil and water dynamics and the maintenance of biodiversity.

Although entomophagy is likely to be as old as humanity, this practice has been relatively poorly studied until the last three years and has been very prolific in terms of scientific publications (116 and 117 articles referenced in Web of Science in 2020 and 2021, respectively, against ~50 articles year-1 between 2015 and 2017 and less than 20 year-1 before this period, keyword = ‘entomophagy’) [10]. Interestingly, this recent societal and scientific interest mainly originates in Western countries (~60% of the publications included scientists from Western countries, while entomology remains anecdotic in these countries; see below). Insects are currently considered a piece of the puzzle for reaching some sustainable development goals [11,12]. Edible insects are interesting as ‘food’, especially because they are particularly rich in proteins and contain essential amino acids, fatty acids and vitamins, and their production is considered environmentally friendly in comparison with the production of other sources of animal proteins [13]. Insects offer an alternative to the production of livestock meat, which requires much more energy, water and space than insects [12,14,15]. Some edible insect species contain as much protein as beef, more iron than spinach, as much vitamin B12 as salmon, all nine amino acids, and they are high in calcium, omega 3 and fiber contents [16]. They are therefore a means to prevent global undernutrition and food insecurity in low-income countries [17-19]. Since edible insects can also be used to feed poultry and fish in small villages, they contribute to local food security and rural development, in particular economically empowering women and supporting the livelihood of disadvantaged groups [20]. Insects are highly appreciated as edible food in many parts of the world, with at least 2 billion people occasionally eating insects, especially in South America, South and Southeast Asia and Sud-Saharan African countries [14]. Conversely, if the Western world is increasingly interested in insects for alternative sources of proteins and the positive impact of insect farming on numerous sustainable development goals [12], then this practice remains more of a possibility than a short-term solution in most Western countries. In fact, despite being considered as an emerging sector and growing business [11,16], the consumption of insects must face the challenge of reluctant Western customers, and its business model needs to be improved to become more competitive [14,21- 23]. Moreover, although the exact number of consumed species is difficult to estimate, approximately 2100 species of insects are considered edible [24]. This number must be compared with the few species that are considered to be commercially interesting and farmed. For instance, in Europe, only seven species can be farmed for feeding animals (i.e., black soldier fly, common housefly, yellow mealworm, lesser mealworm, house cricket, banded cricket and field cricket) [25]. This clearly shows that most of the insects that are consumed in the world are harvested in the wild (92%) or on small local farms (semidomestication, 6%) [12]. Specific harvesting and preparing techniques have, therefore, been locally developed and, are part of the culture and patrimony of many low-income communities [26]. These geographical characteristics are even reinforced by the high seasonality associated with insect harvesting (e.g., termites are mostly consumed during their swarming, which limits their harvesting to a few days a year). This scenario obviously increases the interdependence between local communities and the preservation of their environment since the degradation of insect habitats leads to the loss of these nature-based resources, a dependence on expensive and imported food, and as a consequence food insecurity, poverty, and malnutrition [26]. This large difference between the number of farmed insects and the total number of edible insects also shows broad efforts in terms of economic and technological validation with the creation of insect farms from a circular economy perspective [12,27], which could locally improve human wellbeing without negatively impacting environmental resources [28]. An interesting example is the development of over 20,000 small-scale family insect farms in Thailand. In this country, people moved from harvesting insects from the wild (from forests and paddy fields) to rearing them on household farms. Guiné [15] reported an insect production (mainly crickets) of 7,500tons by over 20,000 listed household farms in Thailand, generating more than a million USD. This ‘Thai’ example [12] is considered a success story because it shows that local knowledge and practices can generate income, create employment and increase the livelihood of impoverished families if they receive support from academia research and private sectors.

Insects can also impact the sustainable production of food indirectly through their impact on soil chemical, physical and biological quality. Although insects are mainly considered in terms of their negative effects as pests and herbivores, a significant number of articles show that some taxa can play a significant role in cycling nutrients and maintaining soil fertility [29,30]. Many insect species also spend part of their life cycle hidden in soil, for example during their underground larval stages (e.g., cicadas and many coleopteran species) or nesting in soil stages (e.g., some wasp and bee species and many termite and ant species). Their burrowing activities impact soil dynamics, with effects on soil structure and the dynamics of water, nutrients and biodiversity [31-33], although their effects are considered negligible in comparison with the action of earthworms [34] and termites [35]. If earthworms are currently the banner of sustainable agriculture, because of their positive effects on soil porosity and nutrient cycling, then most of the literature has focused on the negative impacts of termites as pests for plantations and crops [35,36]. However, the trend is perhaps reversed with the publication of several recent articles highlighting the positive impacts of termites and insects in general on ecosystem services [35,37-40]. Recent articles also showed the possibility of termites to favourably impacting not only soil porosity, water infiltration and the resistance of soil to erosion but also chemical elements that are important for improving the resistance of plants to environmental stresses such as silicon [35,41]. Here again, local knowledge and practices have been locally proposed for increasing the sustainable production of agrosystems. The most interesting example is the Zai system practiced in sub-Sahelian ecosystems, and it consists of stimulating termite activity in the field to increase soil fertility and water infiltration and thereby plant growth and yield [35,42]. This traditional practice increases the productivity of the system from 0.5 to 5.3tons ha-1 for straw and from 0.15 to 1.7tons ha-1 for sorghum [43]. At a larger scale, termites can also create large islands of fertility and biodiversity hotspots at landscape scales. In the lower Mekong basin, in Laos, northeastern Thailand and Cambodia, these mounds can be used directly as amendments for increasing soil fertility (because of their higher soil organic matter and nutrient contents and amount of available Si, Muon pers. com.), or they can be used to harvest plants, arthropods and other small mammals that shelter on or in them. This last use of termite mounds contributes to reducing food insecurity and provides improved access to health [35]. If most of the work on the impact of insects on the ecological functioning of soil has focused on natural or non-arable ecosystems, then these two examples provide interesting perspectives for the sustainable management of agro-ecosystems. They also highlight the need for a better understanding of the diversity of local knowledge and practices associated with the utilization of insects and, more generally, soil biodiversity to improve the fertility of soil and the sustainable production of food.

The link between the sustainable production of food and the preservation of biodiversity is not only biological but also cultural. Considerable advances have been achieved in recognizing the importance of local or traditional knowledge. The utilization of natural resources by local communities or ethnic groups can be very vast and should be seen as a source of inspiration for scientists [44]. Here, we used two examples to show that local knowledge and customs can sometimes be sources of inspiration for the development of innovative, environmentally friendly and effective practices: the Thai and Zai examples. Unfortunately, the degradation of natural resources and the shift to ‘westernization’ constitute major threats to the preservation of this traditional knowledge and, in parallel, to all the energy spent to find new technological sources of food and agricultural practices. This review advocates for consideration the diversity of solutions and adaptations that have been found in nature by local populations.

The authors would like to thank the CoSav SyAD initiative (Communautés de Savoirs Systèmes Alimentaires Durables) from IRD for having initiated this discussion and the writing of this review.

Pascal Jouquet: Conceptualization, Writing; Ratha Muon, Saran Traoré, Ajay Harit: Reviewing and editing.

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