Reducing Postharvest Loss of Stored Grains Using Plant-Based Biopesticides: A Review of Past Research Efforts

1. Introduction

Recently, food insecurity has become a serious issue in sub-Saharan African countries, which is reminiscent of the same issue in Asia many years earlier. The latest information showed that over the next 10 years, the world’s population is predicted to increase by more than one billion people reaching 8.6 billion in 2030 and rise up to 9.8 billion in 2050 and 11.2 billion by 2100 [1]. Most of this population rise is expected in developing countries that are already facing hunger and food insecurity. Reducing agricultural yield losses could significantly contribute to satisfying the anticipated higher global food demand and improving food security [2]. Postharvest loss by insects is one of the main challenges in improving the quality of food and the achievement of food security [3]. Insect pests are the most important biotic factors, which cause huge postharvest losses in grains that range from 30 to 40% [4, 5]. According to Abass et al. [4], after six months of maize storage, the larger grain borer, Prostephanus truncatus (Horn), caused 57% of the storage losses, followed by the grain weevil, Sitophilus granarius (Linnaeus), and lesser grain borer, Rhyzopertha dominica (Fabricius).

Despite previous efforts [6], insect-related postharvest losses continue to be a major problem [7, 8]. The maize weevil, Sitophilus zeamais Motschulsky, causes severe weight and quality losses in maize grain in Africa [9]. In developing countries, storage insect pests cause 20–30% loss of maize grain during a given storage period [5, 10]. The magnitude of losses varies from country to country and from region to region [11]. For instance, in Ghana, losses were as high as 50% [12], in Cameroon’s western highlands 12–44% [13], and in Benin 23% [14, 15]. In a study on postharvest losses in sub-Saharan African countries, cereals (maize and rice) incur losses of 25.6 to 27.4%, without interventions in a storage season and can be reduced when various types of loss prevention methods are applied [16]. In Ethiopia, 80% of all grain produced is stored at the farm or village level [17], which is vulnerable to insect pest attack. Tadesse and Basedow [18] reported that the proportion of damaged grains due to insect pests in Ethiopia reached up to 29.3% at farmers’ storages. Tadesse et al. [19] reviewed insect pests and molds associated with stored grains in Ethiopia.

The use of conventional pesticides for many years has led to problems in agriculture, the environment, and human health [20]. It caused genetic resistance and pest resurgence of insect species, left toxic residues in the treated products, caused handling hazards and health hazards to operators [21]. Insecticides cause direct toxicity to nontarget organisms such as beneficial parasitoids and predators. They reduce several terrestrial and aquatic animal and plant species, contaminate soils, drinking water, and food, and poison pesticide users and farmworkers, and affect nontarget organisms such as bees, other beneficial insects, fish, and birds [20]. Certain chemicals get concentrated in the food chain and cause lethal effects on food consumers [22, 23]. One of the ways to minimize these problems is using biodegradable pesticides that have greater selectivity and less persistence [24]. Products of plant origin are good biodegradable agents [25], which are a rich source of bioactive molecules [26]. They are effective and more biodegradable, cause less contamination to the environment, have less potential to produce resistance, and leave fewer residues in food [27–29]. Besides, they are more economical and environmentally friendly [30]. However, plant-derived pesticides are less understood in sub-Saharan countries [31]. Therefore, this review article was an effort to summarize the current knowledge and progress related to botanical pesticides.

2. Historical Background of Botanical Pesticides

For many centuries, botanicals were used before other kinds of pesticides. They were used intensively by countries like Egypt, China, Greece, Italy, and India, where the use of the neem tree (Azadirachta indica Juss.; Meliaceae) was reported in the Veda, a large body of religious manuscripts written in archaic Sanskrit dated at least 4,000 years ago [32, 33]. The repellency effect of plant material has been exploited for thousands of years by human beings by placing bruised plants over the roof of the houses, a practice that is still widely used throughout developing countries. The use of plant extracts and plant parts in the form of powder as insecticides dates back at least as far as the Roman Empire [34]. During the reign of the Persian king Xerxes (400 BC), children were treated with dry flowers powders known as pyrethrum, Tanacetum cinerariaefolium Linnaeus (family, Compositae). Botanical insecticides were also considered an important product for pest management in Ancient China [35], Egypt, Greece, and India [36]. Historically, the use of finely ground chrysanthemum, Chrysanthemum cinerariaefolium (Trev) Bocc., flowers can be mentioned as the best-known example. According to preserved written documents, this plant played a very important role in fighting against obligatory ectoparasites such as lice and fleas [37].

In ancient Rome, granaries were often fumigated with various aromatic plants (Rosemary, Myrrh, and Juniper). Aromatic plants were also hung near the entry openings of the granaries. As a result, people revealed the repellent effects of aromatic plant substances [38]. From ancient times, the use of poisoned baits prepared as decoctions of Helleborus niger L. roots against rodents was common. In Persia, various plant oils were used to treat scabies caused by some mites, such as Sarcoptes scabiei L., in 1758 [39]. Later, some plants are also used for protection against phytophagous pests, with the development of intensive agricultural production. The first commercial botanical insecticide product used dated back to the 17^th century is nicotine obtained from tobacco leaves showed action against plum beetles [40]. Around the mid-eighteenth century, a new plant with insecticidal property known as rotenone was introduced. It was obtained from the roots of the plant, called Timbó–Derris spp. [37].

3. Major Stored Grain Insect Pests

Storage insect pests reduce grain quality during storage by feeding. This leads to a loss in weight, nutritional value, the viability of seeds, and they contaminate the grains and cause odor change, growth of mold, and heat damage. All these reduce grain quality and make them unsuitable for human food or animal feed [41].

Rajendran [42] listed more than 600 species of beetle pests, 70 species of moths, and about 355 species of mites causing quantitative and qualitative losses of stored products (Table 1). The particular insect pest species present in the storage depends on several factors; among them, grain type is important. All cereal grains and many stored legumes are infested by pests larvae either feeding or developing inside the kernel or outside intact kernels. The internal-feeding insects have been referred to historically as primary pests, while those feeding outside the kernels on broken and fine material have been referred to as secondary pests. Some of the most serious destructive insect pests of wheat are internal feeders, such as the lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), which lays eggs outside the kernel and the larvae bore into the kernel to complete development to the adult stage. In contrast, rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae), lays eggs directly inside the kernel. The red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae), the sawtoothed grain beetle, Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae), are the most common external-feeding pests of wheat. The maize weevil, Sitophilus zeamais Motschulsky, and the angoumois grain moth, Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae), are internal feeder insects, which are most commonly found in shelled corn (maize); external-feeding pests include C. ferrugineus; the flat grain beetle, C. pusillus (Sch ¨ onherr); O. surinamensis. Major internal-feeding pests of rice are R. dominica, S. oryzae, and S. cerealella [42].

Abass et al. [4] argued that among all the biotic factors, insect pests are considered the most important groups that cause huge postharvest losses in the grains ranging from 30 to 40%. Abass et al. [4] reported that after six months of maize storage, larger grain borer (Prostephanus truncates) was responsible for more than half (56.7%) of the storage losses, followed by losses due to grain weevil (Sitophilus granarius) and lesser grain borer (Rhyzopertha dominica).

4. Most Commonly Used Botanicals against Stored Grain Insect Pests

Botanicals possess active ingredients that act on storage pests. Many spices possess insecticidal activities, especially in the form of essential oils (Table 2) [71]. Spices are used to flavor foods and/or protect stored products from pests. Traditionally, slices of dried spices or ground spices are mixed with stored foods, but recently their extracts or oils have given encouraging results. These compounds do not leave toxic residues in the environment, are not toxic to mammals, and have medicinal properties for humans [72–74]. The characteristic flavors and odors derived from the volatile oils of spices are known to have various effects on insect pests, including stored grain insect pests [75]. They can be used sustainably to replace synthetic pesticides [76].

Other plants are also used to combat stored grain pests (Table 3). The medicinal plants, Artemisia vulgaris L., Artemisia aucheri Boiss., Artemisia scoparia Waldst. et Kit., and Artemisia sieberi Besser, repel or poison Tribolium castaneum (Herbst) [123, 124]. Essential oils of Rosmarinus officinale L. (Rosemary) act against Sitophilus oryzae L. and T. castaneum [125]. Mentha piperita L. and Mentha arvensis L. have fumigant activity against T. castaneum [123, 125].

Still, other plants (other than spices and medicinal plants) act against storage insect pests (Table 3). Prakash and Rao [126] reported research results of 160 plant species against major insects of stored products, e.g., the neem tree, Azadirachta indica [127, 128]. According to Derbalah [129], Cassia senna L., Caesalpinia gilliesii Hook, Chrysanthemum frutescens L., Thespesia populnea var. acutiloba Baker, Bauhinia purpurea L., Euonymus japonicus L., and Cassia fistula L. had good efficacy against T. granarium; C. senna was the most potent plant extract against T. granarium. Abdullahi [130] revealed that Vitellaria paradoxa has great potential against pulse beetle Callosobruchus maculates. The ethanol extract of bitter gourd, karanja, and urmoi protected wheat grains up to 30 days, with no side effects of seed viability after three months of treatment [131]. Lime peel oil effectively protected maize against weevil Sitophilus zeamais [130]; the powder (Curcuma longa L.) affected the normal physiology of the insects [132].

5. Nature of Botanical Pesticides and Their Mode of Action

6. Recent Development and Status of Botanical Insecticides against Stored Grain Pests

During the past few decades, the interest in using plant-based pesticides has increased, chiefly the natural origin with low mammalian toxicity [168]. In different parts of the world, attention has been paid to the exploitation of plant products as novel substances in plant protection. Because of low phytotoxicity, easy biodegradability, and the stimulatory nature of host metabolism, plant products possess the potential value in pest management [169]. Higher plants contain a wide spectrum of secondary metabolites such as phenols, flavonoids, quinones, tannins, essential oils, alkaloids, saponins, and sterols. Such plant-derived chemicals may be exploited for their different biological properties. In the context of agricultural pest management, botanical insecticides are best suited for use in organic food production in industrialized countries but can play a much greater role in the production and postharvest protection of the food in developing countries [36].

Accordingly, the use of green pesticides, particularly for stored grain pests, is being recommended globally, and the use of essential oils seems to be the best choice. Studies have shown that essential oils are readily biodegradable and less detrimental to nontarget organisms than synthetic pesticides [170]. The application of plant products, especially essential oils, is a very attractive method for controlling postharvest diseases and pests. The production of essential oils by plants is believed to be predominantly a defense mechanism against pathogens and pests [171].

Companies specialized in the production of botanical pesticides strive to improve the formulations, stabilization of the extracts, and consistent chemical pattern to answer the quality standards of the marketed products. According to Kleeberg and Ruch [172], the standardization of neem seed extracts, which show a large variation of azadirachtin content, is one of the keys to enhancing neem product commercialization. These requirements could be resolved with the marketing of synthesized molecules identical in every point to the natural molecule (i.e., organoleptic properties, degree of purity, and absence of residual solvents). Recently, several new substances have been reported in the literature as promising compounds for use as biopesticides [173], but more field research is necessary for assessing their efficacy on specific pest problems under diverse cropping systems.

Pest management products from plants are also an important segment of the biopesticide market. Isman [36] discussed botanical insecticides from a global perspective as in 1980, <2% of all journal papers published were on botanicals insecticides, but the number exceeded 21% in 2011. There has been an explosive growth in reported studies of the insecticidal activity of plant essential oils, but this activity has not been reflected in the increased commercialization of botanical insecticides, at least not in the major North American and European markets. Much interest in botanical insecticides has come from China and other Asian nations, Latin America, and Africa, perhaps due to the potentially lower cost, local sourcing, and relatively lower mammalian toxicity. Particularly, those plant-derived extracts from local farmers are relatively cheaper in preparation and more convenient in application with lower cost due to the locally grown plants for local use compared to the use of synthetic ones [139, 174]. Globally, the demand for natural pesticides is growing [175, 176] due to the increasing interest in organically produced safe food. However, commercially available botanical insecticides have been largely limited to pyrethroids and neem, to a lesser extent, limonene, chenopodium, capsicum oleoresin, and garlic oils [176].

Significant numbers of studies have been reported regarding the use of botanical biopesticides against storage and field crop pests. The following have been reported: neem leaves against a variety of pests [177]; Clerodendrum serratum L. leaf extracts and powdered leaves and leaf extracts of Olax zeylanica Wall., against the rice weevil (S. oryzae L) [178]; Cichorium intybus L, Melilotus parviflora L, Chenopodium album L against Trogoderma granarium Everts [179]; methanolic extracts of medicinal plants against wheat pest Tribolium castaneum Herbst [180]; Phthorimaea operculella Zeller against the potato tuber moth [181]. Other essential oils from Eucalyptus nicholii Maiden and Blakely, Eucalyptus codonocarpa Blakely and Mckie, Eucalyptus blakelyi Maiden, Callistemon sieberi F. Muel., Melaleuca fulgens R. Br., and Melaleuca armillaris Sm. are used against S. oryzae, T. castaneum Herbst and Rhyzopertha dominica Fabricius [182], N. tabacum, T. vogelii, Ocimum gratissimum L., and Crassocephalum crepidioides S. Moore against the bean weevil [183].

Obeng-Ofori et al. [184] evaluated the bioactivity of materials from the leaves of Ocimum kilimandscharicum Labiatae against the beetles, Sitophilus granarius L., S. zeamais Motsch., Tribolium castaneum Herbst, and Prostephanus truncatus Horn. All plant pesticides reported up to 100% mortality after 24 hr exposure of adult insects to dried leaves and essential oil extract of the plant. Bekele [112] also evaluated the toxicity of different plant parts of Millettia ferruginea (Hochst.) against S. zeamais in maize seeds. Seed powder applied at 10%w/w to maize seeds was toxic to the weevil and caused a significant reduction in reproduction.

7. Constraints on the Use of Botanical Pesticides against Stored Grain Insect Pests

8. Conclusion

The use of plant secondary metabolites synthesized by some plant species as part of their natural self-defense against stored product insect pests seems to be an excellent alternative. Botanical pesticides (essential oils, flavonoids, alkaloids, glycosides, esters, and fatty acids) have various chemical properties and modes of action and affect insects in different ways, namely, repellents, feeding deterrents/antifeedants, toxicants, growth retardants, chemosterilants, and attractants. Thus, it is preferable to use botanical insecticides instead of synthetic insecticides and these botanical insecticides are recognized by organic crop producers in industrialized countries.

It is also important to raise awareness among farmers to use the botanical products as pesticides. In some areas in particular, high attention is now paid to raise awareness especially in developing countries where long-term projects are being designed and aimed at educating growers about the basic skills of manufacturing botanical pesticides.

Based on the number of scientific studies focused on the research of plant substances with insecticidal effects, it seems that commercial botanical insecticides should occupy an important position in the market. However, a better understanding of their mode of action, effects, and information related to regulatory issues is needed for their adoption. The scientific standardization may help further to raise their profile among the public and policymakers and hence enable them to realize their contributions to sustainability. Therefore, it is recommended to use botanical insecticides and conducting research to find new sources of botanical insecticides is very crucial.

Conflicts of Interest

The authors declare that they have no conflicts of interest.