Insects as sources of food and bioproducts: a review from Colombia
The Journal of Basic and Applied Zoology volume 83, Article number: 56 (2022)
Insects are known to be important sources of food and bioproducts, and companies around the world are currently offering goods and services based on their production and use. Colombia is one of the richest countries in the world in terms of biodiversity, with a great variety of insects that are not exploited for these uses at this time. Most studies relating to insects in Colombia are focused on agricultural pests or disease transmitters, and in most cases the advantages and potential applications of insects in the areas of agro-industry, medicine, biotechnology, and food are poorly known. To recognize the native species previously considered as a source of bioproducts, it is necessary to better evaluate their potential uses, as well as the possibilities of innovating with products derived from them. It is also important to consider advantages and disadvantages of using insects for specific purposes, minimum quality requirements and national and international regulations for production and marketing.
The growing world population has led to an increase in the demand for food and animal products, increasing the need for animal production. This has resulted in high pressure on the environment, water resources and biodiversity, which also contribute to climate change. New strategies are required, and emerging solutions include the use of alternative sources for bioproducts or meat, changing diets, and migrating to sustainable production systems. In the present study, available information pertaining to 107 species of insects reported in Colombia that have been indicated to be sources to produce bioproducts, or that are currently being used for that purpose is revised and analyzed. The insects documented are from 67 genera and mainly include the orders Hymenoptera (59%), Coleoptera (10%), and Blattaria (11%). Seventy-one percent (71%) of the insect species included are important as foods or food supplements, with 9% related to established or commercial products currently in development; and 36% currently recognized for their importance in obtaining valuable non-edible bioproducts within the pharmaceutical industry, medicine, biotechnology, and agro-inputs sectors. A list of species is presented and uses and applications are discussed.
Despite Colombia's enormous potential for sustainable development of insect-derived products, there is a lack of studies in this area. Most of the insects reported in this work are related to local and traditional knowledge and folk medicine of some populations in the country. In addition to apiculture, there are not industrialized insect farms in Colombia; however, there have been some initiatives to produce crickets of the species Acheta domestica and mealworms Tenebrio mollitor for human and animal consumption. Recently the traditional consumption of ants and certain termite species in some areas of the country has been refreshed by some chefs experimenting with insects in gourmet restaurants. There are few studies on the nutritional value or pharmaceutical uses of the local species and there is no clear regulation for breeding or use. This highlights the need for in-depth study and discussion of the advantages and disadvantages for potential use in the country.
Insects are very diverse and abundant (comprising 85% of the fauna on the planet) and they represent vast resources of natural bioproducts and macromolecules; however, until a few years ago (c.a. approximately 1980), most of them had not been explored in these capacities (Govorushko, 2019; Seabrooks & Hu, 2017; Shrivastava & Prakash, 2015).
Although it is well-known that insects constitute a promising source of novel natural bioproducts for the pharmaceutical industry, interest in their applications in biotechnology and agriculture has recently been growing worldwide (Hemmati & Tabein, 2022; Mlcek et al., 2014; Seabrooks & Hu, 2017).
The potential for tropical countries like Colombia to be sources for the production and development of insect-derived products is enormous, both due to the natural biodiversity that they contain and also due to local knowledge of traditional insect uses (Torres & Velho, 2009; Gasca-Alvarez & Costa-Neto, 2021). Several industries and scientists from Colombia currently are working on the identification of novel compounds with potential commercial uses, as demand for these bioproducts is growing around the world. Also, due to the large diversity of natural products and their potential contributions to the development of new drugs and medicines, bioprospecting has become an active field that is becoming increasingly more important in the marketplace (Calixto, 2019; Gasco et al., 2020), and Colombia has the scientific and technological capacity to participate more actively in this activity (Duarte, 2011; Gasca-Alvarez & Costa-Neto, 2021).
Entomotherapy and entomophagy have been widely documented as common practices for different native cultures in the Americas (Cahuich-Campos & Granados, 2014; Costa-Neto et al., 2006). Many of the therapeutic and curative properties of the insect species used in folk medicine have been verified by modern medicine (Cahuich-Campos & Granados, 2014) and more than 2000 species of edible insects are known and currently used as source of food, including: beetles, caterpillars, bees, wasps and ants (Kouřimská & Adámková, 2016; Kim et al., 2019).
The economic and environmental advantages of using insects as food have been widely documented. Insect farming produces lower greenhouse gas emissions, requires less land and water use compared to traditional livestock farming (Collins et al., 2019; Govorushko, 2019).
More recently controversial aspects as microbial contamination of insect-derived foods, chitin allergies or even phobias, are subject of great debate and consideration (Govorushko, 2019; Avendaño et al., 2020; Grabowski et al., 2021).
In Colombia, Paoletti et al. (2000) documented that more than 115 insects have been traditionally consumed in the Amazon basin, and according to their estimates, more than 100 belong to order Blattaria, while thousands belong to the order Coleoptera. Many insects used as food are also considered to be pests of crops of economic importance, including sugar cane, corn, cassava, pineapple, tomato and oil palm (Cerritos, 2009).
The present study presents information related to several insects whose use and application has been explored with the aim of obtaining products and compounds of importance in the fields of biotechnology, medicine, industry, and agro-inputs. The potential uses of these insects have been reported in Colombia, as there are a few initiatives for their industrial production. For example, in 2015, the ArthroFood SAS company was founded in Bogota with the purpose of producing insect protein foods for rural communities and for commercial distribution. Other initiatives were recently socialized at congresses and academic events that were open to the public have sought to provide opportunities for attendees to experience insect consumption with the purposes of introducing people to entomophagy and of highlighting the importance of insects as sources of protein and nutrients. There are many promising aspects for a future insect bioeconomy in Colombia, both for startups and for potential investors. This article provides basic information as a starting point for further study.
Insects used as food
Insects constitute a significant source of proteins and a sustainable alternative to supply global dietary demands and to enhance food security (Churchward-Venne et al., 2017; Govorushko, 2019; Kim et al., 2019; Silva et al., 2020). There are at least 72 species of insects present in Colombia which are currently or may potentially be used as food sources. Most of the insects that are used directly for human consumption are from the orders Coleoptera, Blattaria, Lepidoptera and Hymenoptera. Hymenoptera is the order of greatest representation (64%) and includes several edible insects such as ants and wasps.4 However, a wide variety of bees comprises most of the species listed, many of which are used to produce honey and other natural products. Table 1 lists the insect species that have been used or can be considered as sources for food production.
Documented cases of insects used as food in Colombia
Although entomophagy is not a widespread practice in all regions of Colombia, there are reports of consumption of a wide variety of insects by different indigenous groups. According to Gasca-Álvarez and Costa-Neto (2021), 69 edible insects are currently reported as food resources, ingested in approximately 13 ethnic groups belonging principally to the Amazon and Caribbean regions. Several insect species are commonly consumed by indigenous amazonian peoples (Dufour, 1987; Paoletti et al., 2000; Gasca & González, 2021). Some authors have documented the insect consumption preferences of several indigenous groups including the Yukpa, the Guajibos, the Yanomamos and the Tukanoans. These groups consume a large variety of insects (grasshoppers, earthworms, flies, battle larvae, wasp, ants and termites), with a preference for immature forms in many cases. In addition, as Ruddle (1973) mentioned in his article, most of the insects consumed are crop pests, thus, this is a practice that may help to reduce agricultural losses without resorting to the use of insecticides.
Dufour (1987) documented the use of 20 insect species by the Tukanoans belonging to the orders Coleoptera, Lepidoptera, Blattaria and Hymenoptera. The coleopteran species commonly used by these people are Euchroma gigantea, Rhynchophorus spp., Acrocinus longimanus and Megaceras crassum (Dufour, 1987). The beetle Dynastes hercules is also eaten by some indigenous groups (Ramos-Elorduy et al., 2009; Ratcliffe, 2006). This scarab has a wide distribution, ranging from Mexico to South America (Dutrillaux & Dutrillaux, 2013) and can easily be bred in captivity (Gasca, 2011). In general, beetle larvae are widely appreciated by indigenous groups due to their high caloric and protein contributions to the diet (Dufour, 1987; Gasca & González, 2021).
Several authors have reported the consumption of Hymenopteran ants of the genus Atta by different indigenous groups in the amazonian region (Dufour, 1987; Paoletti et al., 2000). There is evidence that ants of the genus Atta were reared for eating by the Panches indigenous community in the Magdalena region (Patiño, 1990); nevertheless, the consumption of these ants is also widespread throughout the country. Ants are collected manually from nests and roasted after the removal of their wings and legs (Granados et al., 2013).
Tukanoans eat the wasps Agelaia angulate, Apoica thoracica and Polybia rejecta (Dufour, 1987). Ruddle (1973) reported that the Yukpa tribe frequently consumed larvae from the genus Polistes by first collecting and then eating their nests (Ruddle, 1973). There are also reports of the harvesting and consumption of bee larvae after honey is extracted (Patiño, 1990). The stingless bees Trigona clavipes and Trigona trinidadensis are also important in the diet of the Yukpa tribe (Ruddle, 1973).
Termites from the order Blattaria, particularly those belonging to the genera Syntermes, Nasutitermes and Labiotermes are also widely consumed (Dufour, 1987; Paoletti et al., 2000; Ruddle, 1973). The Tucumans also included termites of the genus Termes as part of their diet (Patiño, 1990).
Of the lepidopterans, Dufour (1987) showed evidence that caterpillars from the families Lacosomidae and Saturniidae were collected by Tukanoans. In a study by Patiño in 1990, species of Orthoptera were also reported as consumed; communities from Tucumán collected grasshoppers of the genus Schistocerca and natives from islands near Cartagena filled baskets with dried crickets and grasshoppers for trading.
Most of the natural insect products marketed in Colombia come from bees, mainly from Apis mellifera. Bees offer several products such as honey, pollen, wax and propolis; however, honey is still the most commercialized product. In fact, although Colombia has the potential to produce very high-quality propolis, the amount of production does not supply national demand (Velasquez & Montenegro, 2017). Other products, such as mead are also produced artisanally on a small scale (Quicazán et al., 2018).
Meliponiculture has recently emerged in Colombia and is becoming important as an economic activity which generates environmental services and products that contribute to food security and that provide additional income for producers (Fuenmayor et al., 2013; Nates-parra & Rosso-londoño, 2013; Salatino et al., 2019). Around 120 native species have been identified in Colombia for this purpose, among which Tetragonisca angustula is the most common species reared (comprising 57% of registered colonies) (Jaramillo et al., 2019; Nates-parra & Rosso-londoño, 2013). According to Nates-Parra and Rosso-Londoño (2013), 34 species of stingless bees are reared in Colombia, belonging to the genera Tetragonisca, Melipona, Paratrigona and Nannotrigona (Jaramillo et al., 2019). Despite this, there are a dearth of studies that elucidate the characteristics, uses and practices used to obtain products from these bees, and there is also a lack of knowledge about their biology and therefore techniques for breeding and handling products that are obtained from them (Nates-Parra & Rosso-Londoño, 2013; Salomon et al., 2021).
Several edible insects present in the country can be cultivated on a large scale and are suitable for obtaining edible products for human and animal consumption in the forms of fried, dried, roasted and cooked insects; as well as powder made from dried insects and feed for breeding animals and pets (Grabowski & Klein, 2017; Mutungi et al., 2019). However, many insects that have been produced on a large scale in other countries to produce goods and services related to the food and agricultural industries have neither been explored nor seen as economic alternatives in Colombia (Dicke et al., 2020).
Based on its nutritional properties and ease of rearing, the cricket Gryllus assimilis is a promising alternative for the development of human and animal dietary supplements (Alfaro et al., 2019; Ruiz et al., 2016; Soares et al., 2019). Previous studies have shown that G. assimilis has a high protein content (varying from 51 to 65% dry mass) and essential amino acids and minerals such as Fe and Zn (Adámková et al., 2017; Mwangi et al., 2018; Soares et al., 2019). In particular, Rosa and Thys (2019) evaluated the use of cricket powder from this species as an alternative for the enrichment of gluten-free breads, which allowed them to obtain a product with a high protein content and therefore better nutritional quality. The same authors reported a 40% increase in the dry matter protein content of breads with a 10% addition of cricket powder by dry mass (Rosa & Thys, 2019).
The giant mealworm (Zophobas morio) can be also produced on a large scale due to its easy handling and growth requirements (Heckmann et al., 2018). Benzertiha et al. (2019) showed that when this insect is added in small supplemental quantities to the diet of broiler chicken, it did not have negative effects on nutrient digestibility, and it improves the health of the animals by reducing pathogenic bacteria associated with its microbiota. A replacement of 25–50% of fish meal with giant mealworm meal also improved the growth performance of Nile tilapia and increased the percentage of protein found in fish fed with this experimental diet (Jabir et al., 2012).
The black soldier fly Hermetia illucens has been one of the most widely used insects in the world for the industrial bioconversion of organic waste into products with high protein value (Barragan-Fonseca et al., 2017; Dicke et al., 2020; Müller et al., 2017); H. illucens larvae can also be used directly as food for animals (e.g., for aquaculture of fishes and for poultry and pig breeding) (Barragan-Fonseca et al., 2017; Müller et al., 2017). Additionally, this fly is suitable for the bioconversion of low value products such as residues from agro-industry, crops, and food waste into high value products that can be reincorporated into the market (Cammack & Tomberlin, 2017; Sprangers et al., 2017).
Similarly, the housefly Musca domestica has been evaluated for the replacement of fishmeal; Ido et al. (2015) reported that the dietary supplementation of the red sea bream with housefly pupae resulted in better feed conversion and digestibility of plant protein, as well as the stimulation of its immune system response. Wang et al. (2017) found that Nile tilapia fed with M. domestica maggots had better muscle firmness and therefore better flesh quality. Similar results were reported by Shin and Lee (2021) for feeding Pacific white shrimp with natural and commercial products obtained from insects.
Insects as sources of bioproducts for disease prevention and treatment
Numerous bioactive compounds have been identified from extracts and natural products of different insect species. These compounds cover a wide range of applications due to their antimicrobial, anti-viral and anti-carcinogenic activity, as well as their analgesic and anti-inflammatory effects. Additionally, given the demand for new antibiotic compounds due to growing bacterial resistance in human and animal populations, a wide variety of insect peptide extracts and natural products have been studied for their antimicrobial properties. The discovery of new biologically active peptides and proteins have led to the chemical synthesis and production of recombinant proteins derived from insects (Riascos, 2021).
There are at least 40 species of insects in Colombia that have been studied regarding their production of natural products and biologically active compounds. Most records found for insects present in Colombia correspond to species of the orders Hymenoptera (51%), Diptera (15%), Blattaria (10%) and Coleoptera (13%). Other orders have lower percentages of total species reported, including Lepidoptera (5%), Dermaptera (3%), and Hemiptera (3%). The results above not only reflect a smaller amount of research activity at present for the orders with the lowest participation, but also the poor documentation of species in Colombia, considering that there are only 11,764 species recorded as compared to an estimate of more than 300,000 total species in the country (Amat-garcía & Fernández, 2011; GBIF, 2022). Table 2 provides a list of different compounds and substances with antimicrobial properties obtained from insects.
The order Hymenoptera comprises more than 153,000 described species and is one of the richest orders (Aguiar et al., 2013; Forbes et al., 2018). The species of interest investigated from this order in Colombia were from the families Apidae and Formicidae. Most of the substances and bioactive compounds studied from this order correspond to bee species and have been studied for their antimicrobial action against bacteria, fungi and other parasites.
Natural products such as honey, propolis, royal jelly, bee pollen, venom and wax have been widely studied for their medicinal properties (Alvarez-Suarez, 2017; Israili, 2014; Kwakman & Zaat, 2012). These compounds are either chemically synthesized by the insect itself or are derived from plants and subsequently modified by bees for their own uses (Alvarez-Suarez, 2017).
Many beneficial health properties have been attributed to honey. In fact, the use of different types of honey have been approved for several clinical applications (Kwakman & Zaat, 2012). The antimicrobial activity of honey against Gram-positive and Gram-negative bacteria as well as fungus and viruses is well documented (Ahmed et al., 2018; Watanabe et al., 2014). Also, honey has been used to treat common conditions such as wounds, edemas, and ulcers due its anti-inflammatory effects (Almasaudi et al., 2016; Borsato et al., 2014).
Honey produced by stingless bees is highly regarded due to its medicinal properties (Fletcher et al., 2020; Nates-parra & Rosso-londoño, 2013). Many of the properties observed in stingless bee honey have been correlated to its high content of flavonoids and phenolic acids (Silva et al., 2013; Biluca et al., 2017; Ávila et al., 2018). Phenolic acids from different species exhibit different profiles, which are related to the different types of pollens, nectars, resins, and oils that are available for the bees (Ávila et al., 2018; Cardona et al., 2019).
A significant correlation has been observed between the antioxidant capacity of honey and its relevant amounts of some phenolic and flavonoid acids (Biluca et al., 2017). Due to its antioxidant effects, honey provides protection against free radical and reactive oxygen species, which are responsible for different pathologies such as disturbances in the metabolism and cardiovascular diseases (Ajibola et al., 2012). Also, the antioxidant activity of honey helps wound healing (Ahmed et al., 2018).
Inhibition by propolis of bacteria and fungus growth has also been reported. In addition, propolis has anti-inflammatory properties due its ability to modulate the immune response (Armutcu et al., 2015; Li et al., 2017; Touzani et al., 2019; Wang et al., 2015). Propolis from stingless bees contains several phenolic compounds that have antimicrobial properties against bacteria and fungus, including: flavonones, flavones, diterpenic acid and pentacyclic acids (Barrera et al., 2015; Çelemli, 2013; Sanches et al., 2017). The major chemical groups found in Colombian samples of propolis are diterpenes, triterpenes, benzophenones, flavonoids, alkylresorcinols and fatty acids (Barrera et al., 2015; Pardo et al., 2019; Rodríguez et al., 2012). Colombian propolis samples from several regions have active ingredients that provide protection against a wide variety of Gram-positive and Gram-negative bacteria of importance in health and food (Ferreira et al., 2011; Samara-Ortega et al., 2011; Só et al., 2015).
Moreover, bee venom has been extensively studied with regard to its antimicrobial and anti-inflammatory activity (Leandro et al., 2015; Lee et al., 2016). Bee venom of Apis mellifera has been tested in the treatment of diseases such as acne, neural inflammation, asthmatic inflammation, amyotrophic lateral sclerosis, atherosclerosis, arthritis and hepatic inflammation (Saad Rached et al., 2010; Kim et al., 2011, 2015; Suk et al., 2013; Lee et al., 2015; Lee & Bae, 2016).
The anti-tumor effects of bee products have also been studied. Honey has antiproliferative, antimutagenic and apoptotic activities on different types of tumor cell lines, including breast, liver, colorectal and prostate (Erejuwa et al., 2014; Jaganathan et al., 2014; Porcza et al., 2016). Also, bee venom reduces the proliferation of carcinoma cells and tumors (Premratanachai & Chanchao, 2014). In particular, bee venom has exhibited cytotoxic activity against different cancer cells, such as: breast, lung, cervical, liver, prostate, bladder, blood (e.g., leukemia), hepatic (e.g., hepatocellular carcinoma) and renal (Eze et al., 2016; Oršolić, 2012; Sobral et al., 2016).
The anti-carcinogenic activity of propolis has been documented for different types of cancer and it is related to its high content of phenolic compounds, which possess antiproliferative and cytotoxic effects on tumor cells (Bonamigo et al., 2017; Vit et al., 2015). Pardo et al. (2019) reported that Colombian propolis samples significantly reduced the cell viability of osteosarcoma cells, an observation that was correlated with its high content of benzophenones.
Ants of the Atta and Acromyrmex genera, including species such as Atta sexdens rubropilosa, Acromyrmex octospinouses and Acromyrmex subterraneus subterraneus, have been studied with regard to their ability to secrete antibiotic and antifungal compounds thanks to bacteria associated with their integument and their metapleural and mandibular glands (Lima et al., 2009; Samuels et al., 2013). Actinobacteria associated with their cuticles include Streptomyces and Pseudonocardia (Cavalheiro, 2017; Samuels et al., 2013). Their mandibular gland secretions contain tannins, terpenoids and pheromones which are able to inhibit a range of microorganisms (Lima et al., 2009; Samuels et al., 2013). The antimicrobial activity of these compounds and those secreted by their metaupleral glands have been tested in vitro against bacteria and fungus with very promising results (Lima et al., 2009; Wang et al., 2020).
Furthermore, myrmexins obtained from the venom of Pseudomyrmex triplarinus are a protein complex with anti-inflammatory and analgesic activities (Mans et al., 2016; Pan & Hink, 2000). There are reports indicating that indigenous groups use ants of the genus Pseudomyrmex as therapeutic agents in several ways: for example, they allow them to bite them in order to relieve joint pain and they crush them to relieve toothaches (Mushtaq et al., 2018).
The efficacy of products from several social wasps from the Vespidae family has been documented in the treatment of common respiratory conditions. Costa-Neto (2002) documented the use of honey from the social wasp Brachygastra lecheguana in northern Brazil for the treatment of cough and asthma. Similarly, indigenous groups in the region use infusions or preparations from Apoica pallens and Polistes canadensis nests to treat asthma and other respiratory conditions such as whooping cough (Costa-Neto, 2002; Costa-Neto et al., 2006). On the other hand, people in the region who have suffered strokes use inhalations of smoke from burned nests of Protopolybia exigua, Polybia sericea and A. pallens species for their therapeutic effects (Costa-Neto, 2002; Costa-Neto et al., 2006).
The venom of A pallens contains a great variety of proteins with different biological functions, including compounds that are neurotoxins, proteins of the type 6 lectin that have biological activity against pathogens, toxic peptides, and proteins with cytolytic and proteolytic action (Mendonça et al., 2019). Synoeca surinama venom showed potential antibacterial activity against Gram-positive and Gram-negative bacteria which was associated with the presence of antimicrobial peptides such as synoeca-MP (Dantas et al., 2019; Freire et al., 2020; Mortari et al., 2012). Also, venom from Protopolybia exigua exhibited antimicrobial activity due to the mastoparan peptides it contains (Mendes et al., 2005; Murata et al., 2009).
The order Coleoptera includes the largest number of insect species, with more than 380,000 species described (Zhang et al., 2018). Although it is the most diverse group, there are few reports of uses of Coleoptera species in medicine or applied studies that have obtained and identified bioactive molecules beneficial to humans. The studies reviewed here were related to species of the Tenebrionidae, Curculionidae, Cerambycidae and Dryophthoridae families.
Extracts of the whole body of Ullomoides dermestoides exhibited antimicrobial activity against several Gram-positive and Gram-negative bacteria (Morales et al., 2020); also, organic and aqueous extracts from this species exerted antioxidant and anti-inflammatory activity linked to the presence of phenols, flavonoids, quinones, fatty acids and monoterpenes such as limonene, alpha-terpinene and alpha-pinene (Mendoza & Saavedra, 2013; Mendoza et al., 2016; Morales et al., 2020). Furthermore, antiproliferative, cytotoxic and genotoxic activities have been documented in extracts of U. dermestoides (Dávila-vega et al., 2017; Deloya-Brito & Deloya, 2014; Mendoza & España-Puccini, 2016).
Whole-body extracts of Zophobas morio larvae inhibited the growth of various bacteria strains, which may be due to the presence of antimicrobial peptides (Mohtar et al., 2014). Also, the Curculionidae species Rhynchophorus palmarum and Rhina barbirostris have been used to treat common afflictions such as fever and headaches (Alves & Alves, 2011). There are also reports of the use of Rhinostomus barbirostris by indigenous people to treat these same conditions (Alves & Alves, 2011; Alves & Dias, 2010).
The order Diptera is one of the most diverse insect groups and includes approximately 160,000 species (Pape et al., 2011). Several species of the Calliphoridae family have aroused interest because of their potential usefulness in larva therapy, which is directly related to the anti-inflammatory and antimicrobial action of their larval secretions. Traditionally, Lucilia sericata maggots have been used to treat chronic and non-healing wounds through proteolytic digestion of necrotic tissue and through the removal of bacterial biofilms (Bian et al., 2017; Choudhary et al., 2016; Tamura et al., 2017; Tombulturk et al., 2018). Maggot extracts accelerate the healing processes of burn wounds and reduce levels of oxidative stress (Bian et al., 2017). Also, the excretion/secretion (ES) products of L. sericata can be used for the treatment of wounds in diabetic patients, as they increase NF-κB (nuclear factor kappa-light-chain-enhancer of activated B cells) activity and collagen synthesis and promote wound contraction (Tombulturk et al., 2018). Furthermore, the neotropical species Lucilia eximia can also be used in larval therapy, considering it has also demonstrated its effectiveness in the treatment of chronic wounds in both humans and animals. (Calderón-Arguedas et al., 2014; Retana et al., 2014; Wolff et al., 2010).
According to Wolff et al. (2010), L. eximia has been used in Colombia since 2002 in larval debridement therapy and for the reduction of the odor produced by bacterial decomposition in large wounds.
The larvae of L. sericata produce at least 47 peptides with antimicrobial activity against Gram- negative and Gram- positive bacteria (Pöppel et al., 2015). These antimicrobial peptides have been found in the hemolymph and in the excretion/secretion (ES) products from these maggots (Nygaard et al., 2012). Peptides isolated from ES products have exerted antimicrobial activity against a wide variety of microorganisms and parasites, including bacteria, fungus and the pathogen that causes leishmaniasis (Kruglikova, 2011; Kruglikova & Chernysh, 2011; Riascos, 2021; Sanei-Dehkordi et al., 2016).
The species Chrysomya megacephala and Sarconesiopsis magellanica are also promising insects for use in larva therapy and in the discovery of new bioactive compounds. The hemolypmh of C. megacephala larvae and pupae exhibited antibacterial activity against Gram-positive and Gram-negative bacteria (Sahalan & Omar, 2006). In addition, the salivary glands of C. megacephala contain a considerable variety of substances with antimicrobial activity and proteolytic enzymes (Tait et al., 2018). Moreover, the ES products of S. magellanica enhanced cell proliferation, tissue regeneration and wound healing due to the presence of proteolytic enzymes, serine proteases and antimicrobial compounds (Díaz-Roa et al., 2014, 2019; Góngora et al., 2015; Pinilla et al., 2015). It has also been demonstrated that the hemolymph and body fat extracts of S. magellanica conferred significant antibacterial activity (Góngora et al., 2015).
The antimicrobial peptides cecropin, attacin, defensin and diptericin, as well as lysozymes play important roles in the immune system of Musca domestica (Tang et al., 2014). These peptides have been tested against various bacteria and fungus strains (Jiangfan et al., 2016; Kawasaki & Andoh, 2017) and their expression can be induced by injuring or infecting the maggots (Dang et al., 2010; Jiangfan et al., 2016; Kawasaki & Andoh, 2017). An increase in the antibacterial activity of the hemolymph has also been observed in L. sericata maggots after septic injury (Valachova et al., 2014). Furthermore, the antimicrobial activity of the extracts and hemolymph of the Black Soldier Fly larvae (Hermetia illucens) is well reported (Müller et al., 2017; Park et al., 2015). Several antimicrobial peptides including cecropins, attacins and defensins have been identified and isolated from immunized H. illucens larvae (Elhag et al., 2017; Xia et al., 2021; Zdybicka-Barabas et al., 2017).
The order Blattaria includes approximately 7500 described species of termites and cockroaches (Evangelista et al., 2019). Some species of termites have been used in folk medicine. For example, Nasutitermes macrocephalus, Nasutitermes corniger and Microcerotermes exiguus have been used in traditional medicines to treat asthma, cough, flu, hoarseness, sore throat, and sinusitis (Figueirêdo et al., 2015; Ahmad et al., 2018). Moreover, the potential of the Nasutitermes genus as a natural source of antimicrobial peptides has been documented (Choudhury et al., 2017; Figueirêdo et al., 2015).
Periplaneta americana is an insect species that is widespread throughout the world, and it is considered to be a domestic pest (Luo et al., 2014). P. americana extracts and many derivate drugs are utilized in modern and traditional Chinese medicine to promote wound healing and blood circulation and for the treatment of fever, pain, ulcers, burns, chronic heart failure and cancer (Li et al., 2016; Nguyen et al., 2020; Shen et al., 2017; Zeng et al., 2019).
A broad range of compounds with antimicrobial properties have been obtained from P. americana extracts, such as the isoquinoline group, chromene derivatives, thiazine groups, pyrrole-containing analogues, sulfonamides, furanones and flavonones (Ali et al., 2017; Huang et al., 2017).
The anti-inflammatory and wound healing properties of P. americana extracts are associated with the promotion of keratinocytes, with endothelial cell proliferation, with fibroblast accumulation and with the secretion of related growth factors. In addition, P. americana extracts have displayed anticarcinogenic action and stimulate tissue cell regeneration (Luo et al., 2014; Zhao et al., 2017). The anti-tumor effects of P. americana extracts can be understood through different mechanisms of action, such as the induction of apoptosis, the reversal of drug resistance, the suppression of angiogenesis and the induction of cell cycle arrest (Zhao et al., 2017).
Bombyx mori is one of the world's most researched and best-known insects. This insect, which belongs to Bombycidae family, has been commonly reared to produce silk; however, a wide variety of peptides with significant antimicrobial activity have been found and isolated from it that have potential applications in medicine and agriculture (Buhroo et al., 2018; Chen & Lu, 2018; Islam et al., 2016). Cecropins, defensins, lebocin, lysozymes, attacin and moricin are peptides produced by Bombyx mori that have been well documented for their antibacterial properties (Buhroo et al., 2018; Islam et al., 2016).
Spodoptera frugiperda produces several immune system related peptides and proteins that have antimicrobial activity against Gram-positive and Gram-negative bacteria and fungi (Duvic et al., 2012). The presence of antimicrobial peptides of the cecropin, defensin and lysozyme families has been reported for S. frugiperda (Chapelle et al., 2009; Duvic et al., 2012; Riascos, 2021; Volkoff et al., 2003).
The order Dermaptera comprises approximately 2000 described species (Engel et al., 2015). In the research conducted for the present study, only one record was found for this order; conversely, several studies of the chemical profile of Forficula auricularia secretions have been reported. Both larvae and adults of F. auricularia secrete a strong substance to repel potential predators (Gasch & Vilcinskas, 2014; Gasch et al., 2013; Hoffman, 2014). However, these secretions have also exhibited antimicrobial properties against Gram-positive and Gram-negative bacteria, as well as against entomopathogenic fungi (Gasch et al., 2013).
Insects can also be used as a platform for recombinant protein production through the Insect Cell-Baculovirus expression system (Felberbaum, 2015; Kollewe & Vilcinskas, 2013; Van Oers et al., 2015). In this system, insect cells are infected with genetically modified bacuoloviruses, which replicate and use their cellular machinery for the expression of recombinant proteins (Contreras-Gómez et al., 2014; Kollewe & Vilcinskas, 2013;). In contrast with prokaryotic organisms, insect cells can make post-translational modifications to proteins (Felberbaum, 2015). Using this approach, insect cell cultures have been used for vaccine production, for gene therapy, as biosensors, for the production of viral vectors and in nanotechnology (Van Oers et al., 2015). The lepidopteran cell lines of Spodoptera frugiperda (IPBL-sf21-AE and its clonal isolate sf9) and Trichoplusia ni (BTI-Tn-5B1-4] are the most widely commercialized variants (Contreras-Gómez et al., 2014).
In this process, a scale-up of the insect cells is required to produce a large enough quantity of recombinant proteins (Van Oers et al., 2015) for effective use. In order to do this, recombinant proteins are usually produced in bioreactors to support insect cell growth and virus production (Gallo-Ramírez et al., 2015). However, the costs associated with the maintenance of the suspended cells and the equipment required remain considerably high. Thus, the use of insects as living biofactories has been proposed as an alternative to insect cell cultures (Gomez-Casado et al., 2011). By using insect larvae or pupae as biofactories, it is possible to obtain higher levels of recombinant protein expression of antibodies, enzymes, vaccines and hormones that are useful for diagnostic and therapeutic purposes (Zhou et al., 2011; Gómez-Sebastián et al., 2012; Salomon et al., 2021; Buonocore et al., 2021). As the life cycle of the silkworm (Bombyx mori), as well as its rearing and maintenance are well known, B. mori is a suitable model for the expression of heterologous genes through the whole insect model (Kato et al., 2010). At the time of the present study, both B. mori larvae and pupae have been used for the efficient production of relevant recombinant proteins (Kato et al., 2010; Kollewe & Vilcinskas, 2013; Manohar et al., 2010). In addition, the expression of recombinant proteins in the silk gland of B. mori has become an interesting alternative to produce valuable pharmaceutical proteins as well as human- and animal-derived proteins (Zdybicka-barabas & Vilcinskas, 2016).
Since 1998, different companies have produced vaccines and therapies based on baculovirus expression technology which have been approved for use with humans and in veterinary medicine (Cox, 2021; Felberbaum, 2015; Van Oers et al., 2015). Some examples include vaccines and therapies for influenza, papilloma virus, swine fever and porcine circovirus, as well as pharmaceutical products for gene therapy and immunotherapy (Felberbaum, 2015; Milián & Kamen, 2015; Van Oers et al., 2015).
Insects as enzyme sources
Insects produce a wide variety of enzymes that allow them to make use of multiple organic substrates for feeding (Mika et al., 2014). Insect-derived enzymes include hydrolytic enzymes, cellulases, lipases and oxidative enzymes that provide interesting alternatives in industrial biotechnology applications (Alves et al., 2019; Mika et al., 2013).
Food proteins such as gluten and casein can cause immune reactions and allergies in some people. Celiac disease, which is caused by wheat gluten and similar proteins from oat, barley and rye requires sufferers to maintain diets with many restrictions that affect their quality of life (Mika et al., 2013, 2014). In this regard, Mika et al. (2014) found that enzyme extracts from several beetles considered to be cereal pests can be used to hydrolyze gluten, casein, rice protein and bovine serum albumin. According to the authors, serine and cysteine peptidases were the most common extracts found (Mika et al., 2014).
The hydrolytic enzymes alpha, beta, gluco- and iso-amylase are digestive enzymes produced by plants, animals and microorganism in order to degrade starch and glycogen (Mika et al., 2013). Although amylases are mostly obtained from bacteria and fungi, they can also be found in insects (Mehrabadi et al., 2011; Mika et al., 2013). Amylases have been widely studied for their applications in the pharmaceutical, food, brewing, paper, detergent, and textile industries (Saini et al., 2017). In particular, Easa et al., (2017) performed an extraction of crude amylase from Z. morio which exhibited high enzymatic activity. Also, Mehrabadi et al. (2011) obtained and characterized alpha-amylases from the midgut of several coleopteran pests.
On the other hand, termites have displayed an interesting capacity for lignocellulose degradation. The mechanism they use is not only mediated by the microbiota associated with their hindgut but is also due to the action of hydrolytic enzymes in the host (Arneodo, 2018). The synergistic action of endoglucanases and beta-glucosidases contributes to cellulose degradation. Both endoglucanases and beta-glucosidases were detected in their salivary glands and midgut (Arneodo, 2018). Beta-glucosidases enzymes have also been found in the digestive tracts of the palm weevil R. palmarum and the lepidopteran species B. mori and S. frugiperda (Gyeong et al., 2005; Yapi et al., 2009; Watanabe et al., 2013).
DNA barcoding as a quality control measure for insect products
The authentication of an insect species is important not only for assuring its identity, but also for assuring biosafety, food security and the quality of insect products (Sgamma et al., 2017; Siozios et al., 2020). The morphological identification of a specific taxon to the species level requires a great amount of expertise and an advanced knowledge of the group of interest (Khaksar et al., 2015). Thus, traditional methods for species identification may prove to be impractical, as previous studies of commercially available products from insects have exposed mislabelling or incorrect attribution of species names (Siozios et al., 2020).
Based on the growing interest in developing new insect products, it is important to develop public policies that guarantee the authenticity of the raw material and that do not endanger consumers (Siozios et al., 2020). In this regard, DNA barcoding is a useful method for the rapid identification of specimens through the use of the mitochondrial fragment cytochrome oxidase subunit I (COI), which is widely used due to its variability among species of the same genus (Kress et al., 2015; Paz et al., 2011; Siozios et al., 2020).
Previously, DNA barcoding has been successfully used to identify and ensure the quality of products in the herbal and seafood industries, as well as other types of food products that are susceptible to misidentification or adulteration (Christiansen et al., 2018; Sgamma et al., 2017; Willette et al., 2017). Thus, it may be applicable for the identification and quality control of important insect products in the pharmaceutical, food and biotechnology industries.
DNA barcoding methods involve the amplification of a genetic marker and then its comparison to a template of voucher specimens (Kress et al., 2015). Consequently, the identification of insect species using this technique requires a reference database (Kress et al., 2015; Paz et al., 2011). However, despite the efforts to contribute data to global databases such as BOLD and GenBank, there is still a lack of information for Colombia. According to previous estimates, there are around 320,000 insect species in Colombia (Amat-garcía & Fernández, 2011), whereas the barcode sequences recorded in BOLD so far barely contain 1803 species.
This paper presents an overview of the uses and applications of a wide range of insects, many often considered pests, with an emphasis on those found in Colombia. The great diversity and distribution of insects throughout the planet implies their evolutionary success and high degree of genetic variability. Insects have also developed multiple adaptations and survival strategies that involve the expression of a wide variety of molecules associated with their immune systems, as well as a great degree of versatility that can be used to benefit humans.
Although Colombia is one of the most biologically diverse countries in the world, the work of species description is still far from done. There is still a lack of studies directed toward the recognition of important and beneficial insect species and their potential use.
The use of insects as food is influenced for the nutritional value that varies in the amount and quality of proteins, amino acids, and other chemical compounds that also vary among insects. This variability must be estimated and compared in local species and evaluated according to the breeding necessities and possibilities. Limitations related to communities’ behavior, preferences, and health issues, including the possible existence of allergies to chitin or other insect components, need to be addressed.
National and international production and marketing standards are not completely defined, and issues as bioeconomy and species conservation vs commercial use, must also be revised. Despite this shortcoming, it is considered that Colombia has great potential for the sustainable industrial development of insect-based products.
Availability of data and materials
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Pérez-Grisales, M.S., Uribe Soto, S.I. Insects as sources of food and bioproducts: a review from Colombia. JoBAZ 83, 56 (2022). https://doi.org/10.1186/s41936-022-00319-1